The Claustrum, the External Capsule and the Extreme Capsule of Macaca mulatfa'

JOSEPH J. BERKE Laboratory of Comparative h'eurology. Depcutment of Am~ton~y, University of Michigan, Ann Arbor, Michiga?z

The claustrum is a sheet of gray matter tend beneath the rhinencephalic sulcus situated between the putamen and the (Ariens Kappers, '08; de Vries, 'lo). insular cortex. The external capsule bor- According to Landau ('19) and Faul ders the claustrum medially and separates ('26), the claustrum arises from a ventric- it from the putamen. Interposed between ular matrix, located at the palliostriatal the claustrum and the island is the extreme angle. This gray mass migrates ventro- caps&. Xlost of the interest in the claus- lateralward to lie behind the lower margin trum in past years has centered in onto- of the neocortex and underneath the genetic and phylogenetic studies. No rhineiicephalic cortex. Due to the neuro- biotaxic influence of the ascending fibers agreement has been reached amongst the of the lateral forebrain bundle, the anlage various investigators as to its significance of the claustrum becomes plate-like in and much controversy still exists. configuration. These last authors regarded At present, the knowledge of the fiber the claustrum as independent of both the connections of the claustrum is incom- striatum and the cortex, since their em- plete. The ways in which the basal gan- bryological studies showed no connection glia and the insular cortex are related to of the island with the claustrum during the claustrum and its surrounding cap- ontogenesis. This fact would not favor the sulcs present interesting problems. One theory advocated by Meynert ( 1884), Brod- might speculate that the claustrum serves mann ('09) and Rose ('28) that the as :I relay in the discharge; directly or by claustrum is a derivative of the insula. way of the basal ganglia: from the supple- Moreover, Landau ('23) reported a human mentary motor areas of the cortex to the case in which the insula was absent in tegmc-ntum of the midbrain. the presence of an ipsilaterd claustrum The two capsules that bound the claus- and Dodgson ('55) described a congenitally trum have also not been completely eval- malformed human brain in which the in- uated. There is no consensus regarding sula was present in the absence of the the functional significance or the fiber ipsilateral dorsal claustrum. Furthermore, componeiits of the cxternal and the ex- Macchi ('51) showed that the claustrum treme capsules and the claustrum. is developed before the island becomes differentiated. RET'IETV OF PERTINENT LITERATURE The topographical anatomy of the claus- v-cllious : earlier controversial theories re- arum has been described by Rose ('28). garding the development of the claustrum Klingler ('41), Macchi ('41, '47), and have been reviewed by Ariens Kappers, K511Bn ('51), and was reviewed by Rae I-Iuber, and Crosby ('36). Meynert (1884), ('54a). The claustrum has been divided Brodmann, ('09), Sterzi ('15), and Rose into a compact dorsal part, situated be- ('28) considered the claustrum a deriva- tween the putamen and the insular cortex, tion of the insular cortex. Brodmann ('09) and a ventral portion, which projects for- regarded it as a duplica.tion of the deepest ward into the white matter of the superior layer of this cortex. Ernst de Vries ('10) _-_____ A dissertation submitted in partial fulfillment felt that the claustrum was a part of the of the requirements for the degree of doctor of neopallium, drawn out subcortically to ex- philosophy in the University of Michigan.

297 298 JOSEPH J. BERKE

temporal lobe (Macchi, '51; Rae, '54b). the claustrum. Fibers from the insular The ventral claustrum is broken up into cortex enter the extreme capsule and some scattered masses of gray by the fibers of of them continue medially to become inter- the anterior commissure and by the un- mingled with the claustral network (Rae. cinate fasciculus (Papez, '45). Landau '54a) Interconnections between the claus- ('36, '37,'38) described a claustral exten- trum and the insular cortex have been sion beyond the island which he termed described by Berlucchi ('27) and by KatB the claustrum parvum. Kuhlenbeck ('24) ('38) in the cat, by Alettler ('45) ir; the stated that the claustrum was fused with mangabey, and by Rae ('54a) in human the anterior perforated substance. Whit- mateiial. However, simjlar studies 011 the aker ('21) found macroscopic continuity human brain by Cajd ('O2), Piiitus ('32) between the claustrum and the amygdaloid and Itlacchi ('48) failed to reveal these nucleus. However, the claustro-amygdaloid fascicles. connections have been denied by Volsch Destruction of the frontal cortex anterior ('06),Hilpert ('28),and Broclthaus ('38). to the motor area in monkeys produced Nevertheless it is generally considered that degeneration in the claustrum according to portions of the ventral claustrum lie adja- Bianchi ('22) and lesions in areas 9 and cent to the amygdala, the superior tem- 11 of the macaques permitted denionstra- poral gyrus, and the ventral part of the tion of fiber connections to the claustrum, frontal lobe (Rae, '54a). according to Mettler ('35a, '47). Con- A detailed study of the microscopic struc- tinuity between the ventral claustrum and ture of the human claustrum was made by the gyrus olfactorius lateralis was noted Rae ('54a). Other descriptions of the by vcin Economo in 1929. Macchi ('48, microscopic anatomy of this region have '51), Landau ('19), and Rose ('28) de- been reported by Pintus ('30, '31), Brock- scribed connections of the claustrum with haus ('38, '40), and Nacchi ('48). The the olfactory area. These were disputed dorsal and the ventral claustrum are histo- by Spiegel ('19) and by Brockhaus ('42) logically similar. Silver preparations show Berlucchi (cat, '27) and Papez (man, '45) a network of fine and medium-sized fiber dcmonstrated fibers originating from the fascicles extending in various planes, piriforni cortex and passing around the with the bodies of the claustral cells in the frontal surface of the amygdala to reach interstices. The cell bodies are triangular, the claustrum. ovoid, fusiform or pyramidal in shape, with Hiras'twa and coworkers ('38) described the fusiform cells most numerous near the fibers from area 22 of the temporal cortex external and extreme capsules, and the to the claustrum, in support of Volsch's other types distributed at random (Rae, ('10) contention that the claustrum of '54a). The fusiform cells, which are typ- apes had fiber connections with the tem- ically oriented with their greatest diam- poral lobe. Macroscopic continuity bc- eters in the vertical plane, have been stud- tween the ventral claustrum 2nd. the rimy&- ied by several observers (V. Bechterew, daloitl nucleus has been reporrcd (Pilitus. 1899; Spiegel, '19; Kuhlenbeck, '24). The '31; Macchi, '48), although no filler con- large number of this type of cell is re- nections have been found. However. in garded as characteristic of the claustrum. Didelphis, van der Sprenkel ('26) re- In the literature to date, scanty informa- ported fibers in the lateral olfactory nu- tion has accumulated concerning the fiber cleus, which reached the contralnteral ex- connections of the claustrum 2nd much ternal capsule and the claustrum by way controversy still exists concerning those of the anterior commissure. This state- connections which have been reported. An ment W~Ssupported by Fox, McKinley and exchange of fibers between the external Magoun ('44), who stimulated the lateral czpsule and the lateral border of the puta- part of the olfactory bulb in the cat and men has been described by Wilson ('14), recorded positive potentials in the claus- Kodama ('27), Pintus ('32),hlacchi ('48), trum Le Gros Clark and Meyer ('47) re- and Rae ('54a). These fibers are not nu- moved the olfactory bulb but were unable merous in any one field, however, and it is to find degeneration in the claustruin of uncertain whether any of them arise in the rabbit. CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 299

Claustronigral or claustrotegmental con- sule (Dejerine, 1895; E. Smith, '31; Lauer, nections were suggested by the experi- '45). mental lesions of Rosegay ('44) in the cat. The geniculotemporal bundle and the Recruiting waves have been displayed in ventral thalamic radiations contribute the claustrum from stimulation of the fibers to the capsules. Vestibular and ol- centromedian and the interlaminar nuclei factory fibers (Papez, '45) have also been of the dorsal thalamus (Starzl and Ma- described. Temporal projection fibers in goun, '51). the extreme capsule have been noted (Bucy Many theories have been presented re- and Kluver, '55). Fibers from the inferior garding the functions of the claustrum and thalamic peduncle turn into the basal these have been well summarized by Rae claustral complex. Other projection fibers ('54b). Certain observers (Randacio, from the ipsilateral motor cortex (Hira- 1882; Kuhlenbeck, '24; Macchi, '48, '51) sawa and Kariya, '36) are contained within have considered the claustrum as part of the capsules. Whether any of these fibers the olfactory complex. Physiological eri- terminate in the claustrum has not been dence (Fox et al., '44; Rae, '54b; Segundo determined. Fibers of the ansa lenticularis and Machne, '56) suggests that this area is originating in the caudate nucleus have a correlation center for olfacto-visceral- been regarded by Foix and Nicolesco ('25) somatic impulses. Pintus ('32) and Lan- as passing in the external capsule with dau ('36) believed that the claustrum is some termination in the claustrum. related to the production of speech. Ariens Kappers ('08) felt that the claustrum MATERIALS AND METHODS exerts some effect upon motor responses, In this investigation, the experimental a conclusion which has been supported by subjects used were monkeys (Macaca the results of Mettler et al. ('39) and Kaada mulatta). Nine animals, with weights ('51), who found that movements evoked ranging between 2 and 7.2 kilograms, were from cortical excitation were inhibited chosen without preference for sex. A when the claustrum was stimulated. physical examination and a neurological Enclosing the claustrum are the extreme testing were performed prior to each ex- capsule, laterally, and the external capsule, perimental procedure in order to insure the medially. These capsules consist of dense, selection of active, alert, and healthy ani- medium-sized and fine fibers, coursing in mals. many planes. These fibers form a plexus in The destruction of one or more portions which are found a few fusiforni and ovoid of the brain of each animal was achieved cells. The capsules contain association by cortical ablation or by electrical coagu- fibers from the superior and the inferior lation. The anesthetic for these operative longitudinal fasciculi, the uncinate f'ls- procedures was diethyl ether, administered ciculus. and the pyriform cortex (Papez, either by open drop method or by placing '29; hfettler, '35b; Ariens Kappers. Huber, cotton saturated with ether in close prox- and Crosby, '36; Lockard, '48; Bucy and imity to the nasal and the oral passages. Kluver, '55). No preoperative medication was employed. Commissural fibers to the claustrnm The experiments were performed using from the corpus callosum and the anterior sterile technique. commissure have been reported in many The stimulation of the surface cortex animals by Papez ('29), in rodents by was carried out through the use of a Grass Young ('36), in the bat by Humphrey ('35, Stimulator, Model 3C. Square wave im- '36), and in the macaque by Lauer ('45). pulses, of one millisecond duration, at the Marchi degeneration granules have been frequency of 40 cycles per second, and traced from the anterior commissure to the with an intensity varying from 3 to 7 volts, external capsule by Fox and Schmitz ('43) were employed for cortical excitations. and from the temporal lobe to the anterior Lesions deep within the brain were made commissure by Garol ('42a). The anterior according to selected coordinates (Atlas limb of the anterior commissure enters the and Ingram, '37) using a Lab-Tronics external capsule and is dispersed within Stereotaxic Instrument (Model 4) for de- it. forming an important part of this cap- livering a direct current of 300 micro- 300 JOSEPH J. BERKE

amperes for 60 seconds through a unipolar subsequent examination, an unwillingness electrode. A rectal plug served as the to use his right upper extremity in run- ground. ning. He was able to grasp weakly with Daily observations were made and test- the aEected limb when climbing. This ing performed postoperatively to determine extremity also showed a decrease in tonus, the effects of the experimental procedures. but was not flaccid. Periodic testing over Particular attention was given to differ- the next two weeks showed constant im- ences in behavior, changes in extra-ocular provement with a gradual return to nor- movements, and impairment of motor mal tone and use of the affected extremity. function, if such occurred. Each monkey However, the right wrist was carried in a was examined for spasticity, rigidity, and slightly extended position. inequality of tonus in the extremities. Re- 'Two weeks after the second procedure, sponses to auditory and \7isual stimuli were the animal was sacrificed and the brain assessed. perfused and prepared for microscopic After a 10-17 day period of observation, study by the Marchi technique. When the the animal was sacrificed with an overdose brain had been removed from the cranium, of Evipal, given intraperitoneally, and per- gross inspection showed a right frontal fused with 1000 to 1200 ml of 10% for- lesion involving area 6 and part of areas malin after insertion of a canuln through 8 and 9 (fig. 1). Destruction of left area the left ventricle into the ascending aorta. 6 and part of area 4 were noted (fig. 1). The brain was allowed to harden for These lesions involved the superficial cor- three to 7 days in three changes of 10% tex arid extended into the underlying white formalin and then, in most cases, photo- matter. graphs of the gross brain showing the loca- Microscopic observation showed lesions tion of the lesions were taken. The ma- in areas 8 and 9 on the dorsoiateral and terial was then prepared by the Marchi medial surfaces of the right superior method (Swank and Davenport modifica- frontal gyrus and in the rostra1 end of the tion, '34, '35; Davenport and Swank, '35; cingulate gyrus. These injuries involved M. Smith, '56). Normal material of the the superficial cortex and the underlying macaque brain stained by the Weil or pyri- white matter. The destruction extended dine-silver methods or with cresyl violet caudally to include a portion of the pre- was available for comparison from the motor cortex. A diffuse, fine degeneration Huber Neurological Collection. The Riley spread throughout the frontal cortex at Atlas ('43) proved a very useful aid in the rostra1 border of this lesion and ex- identifying some of the tracts arid nuclei. tended, by way of the corpus callosum, into the corresponding regions of the op- EXPERIMENTAL OBSERVATIONS posite hemisphere. Coarse and fine gran- ules could be traced from the corona ra- Protocol for monkey 1 diata, the subcallosal bundle and cingulate A right frontoparietal craniotomy was gyrus into, and throughout, the head of the performed upon a 3.6-kg male macaque. caudate nucleus. Fine granules in the The central fissure was visualized and dorsal tip of the cingulum spread back- cortical ablation of right area 6 was then ward and forward along short association carried out by means of a surgical aspi- bundles. Bundles of fibers were traced rator. through the head of the caudate nucleus The animal tolerated the procedure well. into the putamen by way of the gray During the next two weeks, he was active bridges connecting the two areas (fig. 13). and alert. No paralysis, paresis, or in- Contributions from the anterior limb of equality of tonus of the extremities could the internal capsule to the putamen were be detected. No other neurological ab- also noted. In the putamen some fibers normality was found on testing. terminated; others gradually worked their Ablation of left area 6 was then carried way medialward, through the globus pal- out following a left frontoparietal crani- lidus and throughout the zona incerta and otomy. Again the animal tolerated the nucleus of the field of Forel as components second procedure well, but revealed, on of the lenticular fasciculus to discharge CLAUSTRUM. EXTERNAL AND EXTREME CAPSULE OF MACAQUE 30 1 directly to the red nucleus and tegmental the extreme capsule were cortical associa- gray around it (fig. 14). Still other bun- tion fibers. dles coursed ventrally to enter the ansa All along the course of the lesion, fibers lenticularis and distribute with it to the were distributed from areas 8 and 9 into pars ventralis of the deep midbrain teg- the external capsule. Some granules could mental gray and into tegmental cell groups be seen ventrally within the capsular caudal to the red nucleus. To this system boundary. A few degenerated fibers turned were added corticotegmental fibers from medially into the putamen. However, the the area of the lesion which traversed the majority of the degenerated fascicles internal capsule to enter the globus pallidus coursed caudally within the external cap- directly where some fibers ended. Many of sule at the junction of the two capsular these were corticorubral and corticoteg- systems behind the putamen (fig. 16). mental fibers, which continued to the red Nevertheless, contributions from the ex- nucleus and the dorsolateral, lateral and treme capsule were traced a few at a time, ventrolateral tegmental areas around the through the claustrum into the external red nucleus by way of the lenticular fas- capsule. At the posterior end of the puta- ciculus (fig. 15) and the ansa lenticularis. men, fibers from the deep white matter at Corticotegmental fibers carried in the in- parietal levels swept obliquely into the ternal capsule, also coursed through the external capsule and passed medially be- lateral thalamic nuclei and nucleus ven- hind the lenticular nucleus into the com- tralis posterior pars lateralis to reach the bined external and extreme capsules. Other red nucleus and the ventrolateral, lateral fibers continued ventrally, in an oblique and dorsolateral tegmentum near this sublenticular or postlenticular course. nucleus (fig. 14). Then they turned above the capsule of the Degenerated fascicles were also followed lateral geniculate nucleus (fig. 17) to join from the whole length of the lesion into the corticotegmeiital fibers passing through the right corona radiata and then into the internal capsule into the ansa lenticularis region where the external and the extreme and discharged, as a common bundle, into capsules adjoin each other. Fibers in the the dorsolateral, the lateral, and the ventro- extreme capsule coursed ventrally and lateral tegmental areas around the red nu- caudovcntrally over the uncinate fasciculus cleus. A few fibers were traced into the into the superior and the middle temporal substantia nigra. gvri. Other degenerated cortical associa- The lesion in the left hemisphere de- tion fibers were traced to the inferior tem- stroyed thc dorsomedial and the dorso- poral and hippocampal gyri. These corti- lateral surfaces of the superior frontal cal association fibers were augmented by gyrus, involving superficial cortex and ad- some fascicles passing, a few at a time, jacent white matter of the premotor area. from the external capsule through the dor- Posteriorly. it extended into the motor cor- sal claustrum into the extreme capsule. tex. Some degenerated medium-sized and Whether any of these fibers terminated coarse fibers could be traced through the within the claustrum could not be ascer- corona radiata into the anterior limb of the tained due to their paucity and extremely internal capsule; others spread throughout fine myelination. Several small bundles in the white matter of the frontal lobe. Com- the extreme capsule passed laterally into missural fibers coursed by way of the cor- the insular cortex but could not be followed pus callosum into the contralateral hemi- for any great distance. sphere but could not be followed to their In addition to the cortical association terminations due to the bilaterality of the fibers, some Marchi granules were traced lesions. rostrocaudally in the extreme capsule to Fibers from thc corona radiata entered its confluence with the external capsule at the head of the caudate nucleus. These the posterior part of the lenticular nucleus fibers were less numerous than those enter- (fig. 16). Together with fibers in the ex- ing the caudate nucleus from the more ternal capsule, they were projected directly rostra1 lesion of the opposite side. The into the tegmentum of the midbrain. granules were traced throughout the ante- However, most of the fibers contained in rior limb of the internal capsule in the gray 302 JOSEPH J. BERKE bridges to the putamen where some fibers nucleus and the surrounding tegmental ended. Many fibers continued medially into gray. A few fine fibers were traced into the the globus pallidus and, through it, into the substantia nigra. ansa lenticularis and the lenticular fasci- Degenerated fibers from the lesion in culus. Over these fasciculi they discharged the motor cortex entered the internal cap- into the red nucleus itself, and into the sule. These were indicated by extremely dorsolateral, lateral and ventrolateral teg- coarse Marchi granules which continued mentum around this nucleus (fig. 14). To in the corticospinal tract. Destruction in this system were added corticotegmental the left medullary pyramid was very fibers which passed by way of the internal marked in comparison to the amount of capsule directly into the tegmentum. Ad- degeneration within the contralateral pyra- ditional fibers from the corona radiata mid (fig. 18). entered the dorsal thalamic peduncle and, intermingling with the fibers of this pe- Protocol for monkey 2 duncle, coursed through the lateral edge A 5.2-kg healthy male macaque was sub- of the lateral thalamic nuclei and across jected to a frontal craniectomy. The dura the nucleus ventralis posterior pars later- was reflected and the arcuate and prin- alis into the red nucleus and the tegmen- cipal fissures exposed. Using a scalpel, a tum around it. lesion was made directly above the caudal Degeneration granules were followed end of the principal fissure and this lesion from the site of the lesion into the region was enlarged with a surgical aspirator to of continuity of the external and the ex- involve the rostral margin of the arcuate treme capsules. Through the latter, corti- fissure (fig. 2). cal association fibers distributed to the A second dural opening was made at the superior, the middle, the inferior temporal, rostral end of the lateral fissure. With a and the hippocampal gyri. From the ex- surgical aspirator, area 11 (Mettler, '47) ternal capsule, a few degenerated fibers, at the ventral border of the lateral surface presumably association bundles, were of the brain was ablated. The wound was added to the extreme capsule by passing closed in the usual manner. through the dorsal claustrum and appeared These procedures were tolerated ex- to reach the insular cortex, but none tremely well. The animal displayed no seemed to terminate within the claustrum. signs of infection or other sequelae. Nine Predominantly, the fibers carried in the days later, a left dorsal spinocerebellar extreme capsule were cortical association tractotomy at the second cervical level was fibers. However, some fibers traversed the performed by another observer (Vachan- claustrum to join the external capsule anda, '59) which caused some hypotonicity directly: others entered it behind the lentic- and weakness of the left lower extremity. ular nucleus. Two weeks after the tractotomy, the ani- Along the length of the lesions, fibers mal was sacrificed and periused and the were distributed from the frontal lobe into brain removed. Gross examination re- the external capsule. From this capsule, vealed two left-sided lesions. The more a few extremely fine fibers coursed medially dorsal lesion, triangular in outline, was into the putamen, but could not be traced located dorsal to the principal fissure and for any great distance. The majority of rostral to the arcuate fissure. The second the fibers passed caudally, supplemented lesions destroyed area 11 (Mettler, '47). by other fibers from the corona radiata Microscopic examination revealed a de- along their course. Many worked their way struction of a portion of the inferior frontal ventrally and were joined by fibers of the gyrus, involving superficial cortex and ex- extreme capsule when the capsules be- tending into the white matter, at most came continuous posteriorly. Thus, the about 1.5 cm. The lesion in area 8 de- fibers ran medially and ventromedially, stroyed superficial cortex and involved the sublenticularly or postlenticularly, passing underlying white matter. over the capsule of the lateral geniculate Marchi granules were traced in serial nucleus (fig. 17) into the tegmentum sections from the lesion in area 11 into the where they projected directly into the red corona radiata and spread as diffuse, me- CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 303 dium-sized and fine granules, into the ules were traced from the extreme capsule frontal lobe. They also could be followed, into the insular cortex. These were very by way of the corpus callosum, into cor- delicate and could not be followed for any responding regions of the opposite hemi- great distance. From the external cap- sphere. Degenerated fibers from the left- sule, a few fine fibers were added to the sided lesion of area 8, joined and inter- extreme capsule after passing through the mingled with those from area 11. Degen- dorsal claustrum. None appeared to ter- erated fascicles coursed from one frontal minate within the claustrum. The fibers lobe through the corpus callosum to cor- carried in the extreme capsule were mostly responding regions of the opposite hemi- cortical association fibers connecting fron- sphere. tal with temporal lobes. A very few fibers were traced from the From the lesions, degenerated fibers subcallosal bundle, from the anterior limb were also distributed through the corona of the internal capsule, and irom the radiata into the external capsule. Most corona radiata into the caudate nucleus, of these fibers coursed within the capsule ipsilaterally, where they appeared to ter- but a few fine fibers appeared to pass me- minate in the caudate nucleus. Degener- dially into the putamen. These could not ated fibers also passed into the anterior be traced for any great distance due to the limb of the internal capsule and the com- delicacy of their medullation. The fibers mon external and extreme capsules on the within the external capsule (fig. 19) col- side of the injury and, aiter decussation lected in a bundle and passed ventrally, through the corpus callosum, to the cor- beneath the anterior commissure, toward responding capsules in the contralateral the base of the brain (fig. 21) where a few hemisphere. fibers entered the diagonal band of Rroca. On each side of the brain, from the The remainder of the fibers coursed me- anterior limb of the internal capsule, a dially and then dorsally to enter the ansa few fibers entered the putamen. Here lenticularis (fig. 13). Beneath the lentic- some fibers terminated and some continued ular nucleus they joined fascicles from the medially into the globus pallidus to join basal ganglia also turning into the ansa other fascicles from the internal capsule. lenticularis. The fibers that had run be- Degenerated fascicles were traced through neath the anterior commissure were dis- the lenticular fasciculus to the zona in- tinct from those of the ansa, as the latter certa and the nucleus of the field of Forel. bundle joined the lenticular fasciculus in Here part of these fibers ended, but others the zona incerta and the field of Forel. continued caudalward to discharge into However, in the field of Forel, the fibers the red nucleus. From the putamen cer- intermingled and became inseparable. It tain more ventral bundles passed into the it uncertain whether the degenerated fibers msa lenticularis to discharge to the nu- in the ansa ended in the nucleus of the cleus of the field of Forel or continued field of Forel or whether they were dis- directly into the lateral and the ventro- charged into the red nucleus and the teg- lateral regions of the tegmentum around mentum around the red nucleus. A very the red nucleus. Joining this system were few fibers remained in the external cap- fibers which passed irom the corona radi- sule and worked their way caudoventrally ata and the internal capsule into, and into the inferior longitudinal fasciculus. through the edge of, or across the lateral These remaining fibers were joined by de- thalamic nucleus to the lateral and ventro- generated fibers coming into this region lateral tegmental areas. A few fibers dis- from the extreme capsule to pass medial- tributed to the substantia nigra. ward beneath the ventral claustrum. As Degeneration granules from both lesions the external and the extreme capsules be- were present in the region of continuity came confluent posteriorly, some of the of the external and the extreme capsules. degenerated fibers from the two capsules From the extreme capsule, cortical asso- intermingled. They coursed medially, sub- ciation fibers distributed to the superior, lenticularly, or postlenticularly, to pass the middle, the inferior temporal, and over the capsule of the lateral geniculate the hippocampal gyri. A very few gran- nucleus and to project into the lateral and 304 JOSEPH J. BERKE ventrolateral tegmentum of the midbrain responding regions of the opposite hemi- together with the corticotegmental fibers sphere. A few degeneration granules were which had descended in the posterior limb seen in the frontal regions of the hemi- of the internal capsule. Some of the fibers sphere, on the side opposite the injury, in the corona radiata continued caudally but were extremely delicate and could not to parietal levels. They then turned into be followed for any considerable distance. the dorsal part of the external capsule, A few fibers entered the subcallosal passing obliquely medialward through the bundle and the cingulum of the left side. caudal end of the lenticular nucleus to reach the posterior limb of the internal No drgenerated fibers were seen in the capsule. Here they intermingled with caudale nucleus. However, some medium corticopontine and corticotegmental fibers and fine degenerated fascicles passed from in the posterior limb of the internal cap- the anterior limb of the internal capsule sule so that their ultimate termination into the putamen (fig. 22). Here some could not be ascertained. fibers terminated, but a few continued their course medially into the globus pal- Protocol for monkey 3 lidus where other fibers from the internal A left frontal craniectomy was doix on capsule were added. Certain of these com- a 5.10 kg male macaque which had under- bined fascicles coursed dorsally in the gone a left spinocerebellar tractotomy at lenticular fasciculus (fig, 20), through the Cz (Vachananda, '59) one week earlier. zona incerta and the field of Forel, to end Reflection of the dura permitted identifica- on the nucleus of this field. Others dis- tion of the arcuate and the principal fis- charged directly into the red nucleus. Ven- sures. Two lesions were made, one above trally, fibers were seen entering the ansa and one below the superior limb of the lenticularis, to pass. in part, to the rentro- left arcuate fissures. The inferior portion lateral and the lateral tegmental areas of the central fissure was exposed through around the red nucleus. To this system a second opening in the dura and the sen- were added corticotegmental fibers from sory cortex immediately caudal to this fis- the internal capsule and still other cortico- sure was ablated. tegmental bundles from the area of the The animal tolerated these operative lesions which traversed the internal cap- procedures extremely well. No changes in sule and turned medially through the behavior or neurological deficits resulted lateral thalamic nuclei and the nucleus from the brain operation. After two weeks, ventralis posterior pars lateralis to rcach the animal was sacrificed and perfused in the red nucleus and the ventrolateral and the usual fashion. On gross examination, the lateral tegmental regions around this the brain showed two frontal lobe lesions nucleus. in the region of the arcuate fissure (fig. 3). Degenerated fascicles, present in the left These lesions were almost continuous and corona radiata, were followed into the seemed to involve both surface cortex and rostra1 continuity of the extreme and the the underlying white matter. A parietal external capsules. In the extreme capsule. lobe lesion occupying the lower portion of fine Marchi granules indicated fascicles the sensory cortex about two centimeters traveling ventralward and caudorentral- above the lateral fissure was also noted ward to distribute to the superior and the (fig. 3). middle temporal gyri. Some fibers also Microscopic examination revealed two coursed to the inferior temporal and hippo- left frontal lobe lesions, above and below campal gyri. These cortical association the arcuate fissures. These involved the fibers were joined by a few fine degenerated superficial cortex on the dorsolateral sur- fibers passing across the dorsal claustrum face of the brain and extended into the from the external to the extreme capsule. underlying white matter. A diffuse, fine Whether any termination occurred in the degeneration spread into the corona radi- claustrum could not be determined. Little ata and throughout the frontal cortex at evidence for association fibers connecting the level of these lesions, and extended, by the frontal lobe with the insular cortex way of the corpus callosum, into the cor- was present. The components of the ex- CLAUSTRURI, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 305 treme capsule seemed to be primarily the latter, degenerated cortical association cortical association fibers. fibers to the temporal lobe were noted. Few At the rostral border of the lesion, fibers if any granules were found in the external were distributed from the frontal lobe into capsule. the external capsule (fig. 24). For the Some degenerated fibers from the sen- most part, these fibers traveled ventrally sory cortex were evident in the posterior and caudoventrally within their capsular limb of the internal capsule on the side of boundary to appear as clusters of fascicles the lesion. A few of these fibers turned just dorsal to the anterior commissure at into the putamen; some entered the globus the level of its decussation. Here the de- pallidus, the lenticular fasciculus, and the generated fascicles turned medially, paral- ansa lenticularis. These probably also dis- leling the anterior commissure, to enter the tributed to the red nucleus and the lateral ventral portion of the putamen, and then and the ventrolateral tegmentum around pass into the globus pallidus behind the and caudal to the red nucleus. At the decussation of the anterior commissure. caudal end of the lenticular nucleus, fibers In their course they were joined by other passed into the external capsule. Such fibers from the globus pallidus. The com- fascicles seemed to aggregate at parietal mon bundle continued toward the ansa levels and passed obliquely ventromedial- lenticularis where the fibers intermingled ward across the putamen into the posterior and became inseparable. Some fibers con- limb of the internal capsule. To this sys- tinued their course into the base of the tem were added degenerated corticoteg- hemisphere entering the diagonal band of mental fibers from the posterior limb of Broca. Other fibers from the ansa lentic- the internal capsule and still other cortico- ularis joined the fibers of the lenticular tegmental fibers which had turned through fasciculus in the region of the nucleus of the posterior part of the thalamus to reach the field of Forel. Some fascicles of both the red nucleus and the tegmental areas bundles ended in this nucleus: others pro- lateral and ventrolateral to it. jected into the red nucleus and the ventro- A few fine, diffuse corticospinal and lateral and the lateral tegmental area corticopontine fibers were traced from the around this nucleus. A few fine fibers re- level of the parietal lesion through the mained in the ventral part of the external posterior limb of the internal capsule and capsule. These fibers maintained their the base of the brain stem. They were position until they reached the posterior indic;ted by a few medium-sized or coarse part of the lenticular nucleus. Here they Marchi granules. turned medially, postlenticularly or sub- lenticularly. to join with fibers from the Protocol for monkey 4 inferior longitudinal bundle. The combined A left frontal craniectomy was per- fiber bundle passed over the capsule of the formed on a 7.2 kg male macaque, the lateral geniculate nucleus to discharge into dura was reflected and a cortical lesion the red nucleus and the lateral and ventro- was made in area 11 (hlettler, '47). Fre- lateral portions of the tegmentum. quent observations during the next two The lesion of the left parietal hemisphere weeks showed no impairment of motor involved a portion of the sensory cortex function and no change in behavior. NO at a position approximately two centi- other physical or neurological defects were meters above the lateral fissure. This le- noted. sion was superficial, destroying surface Two weeks after the operation, the ani- cortex without direct injury to the underly- mal was sacrificed and perfused and the ing white matter. Degenerated fibers, by brain removed. On gross examination. a the way of the corpus callosum, traveled left frontal lesion at the rostral end of the into the corona radiata of the opposite left arcuate fissure was noted (fig. 4). The hemisphere to intermingle with commis- destruction involved the base of the arcu- sural fibers from the frontal lesions. Coarse ate fissure and extended dorsally and ros- and medium-sized granules could be traced trally for approximately 1.5 cm. Involve- into the posterior limb of the internal cap- ment of the superficial cortex and the un- sule and into the extreme capsule. Within derlying white matter was found. 306 JOSEPH J. BERKlZ

Microscopic examination revealed a left ventrally in this capsule, into the superior, frontal lesion involving area 11, which de- the middle, and the inferior temporal and stroyed the anterior borders of both the the hippocampal gyri. The fibers that en- frontal and the temporal opercula and the tered the extreme capsule were predomi- rostra1 portion of the insular cortex. A nantly cortical association fibers, but some medium to fine granular degeneration was fibers appeared to traverse the dorsal claus- traced from the tip of the frontal oper- trum, a few at a time, to enter the external culum into the corona radiata, the anterior capsule. limb of the internal capsule, and the corti- Marchi granules indicated degenerated cal association bundles as far as the middle fibers extending from the insular cortex and the superior frontal gyri at the level into the extreme capsule (fig. 25). These of the lesion. A few degenerated com- were chiefly cortical association fibers con- missural fibers were followed into the necting frontal and insular cortices with contralateral cingulate gyrus and, by way superior, middle, and inferior temporal and of the contralateral corona radiata, to the hippoc:impal gyri. Coarse granules indi- superior, the middle, and the inferior fron- cated the presence of fascicles from the tal gyri, and into the anterior limb of the insular cortex through the extreme cip- internal capsule of the opposite hemi- sule, the dorsal claustrum, and the ex- sphere. ternal capsule to the lateral margin of the From the rostrum of the corpus cal- putamen. They could be traced for no losum, from the subcallosal bundle, and great distance within the putamen. Other from the internal capsule, a few fibers fibers were traced dorsally through the ex- passed into the caudate nucleus on the treme capsule and across the dorsal claus- side of the lesion. They continued through truni into the white matter of the frontal the anterior limb of the internal capsule lobe near the anterior limb of the internal and, by way of the gray bridges, to the capsule. putamen. These fibers in the putamen Medium and coarse granules indicated were augmented by fascicles from the in- degenerated fibers from the superior tem- ternal capsule and the corona radiata poral gyrus to the middle temporal gyrus. which turned into the putamen of each Similar fibers passed to the inferior tem- hemisphere. Here some fibers synapsed, poral and the hippocampal gyri. Many but others continued medially into the such fibers were traced to the extreme cap- globus pallidus, and, through it, into the sule arid through it to the inferior frontal lenticular fasciculus and ansa lenticularis gyrus. Others were carried in the extreme to discharge directly into the red nucleus capsule, but passed dorsomedially through and the lateral and ventrolateral tegment- the dorsal claustrum into the corona radi- tum around this nucleus. Joining this sys- ata. Medium-sized and large degenerating tem were corticotegmental fibers which fibers were traced from the temporal oper- continued from the corona radiata into the culum through the extreme capsule and internal capsule to course near the edge of dorsal claustrum into the external capsule. the lateral thalamic nucleus and across A few fibers traveled still more medially to nucleus ventralis posterior pars lateralis reach the ventrolateral margin of the puta- to reach the red nucleus and the lateral men. ‘These could not be followed for any and ventrolateral tegmentum around this great distance nor could fibers be found nucleus. Corticotegniental fibers from the ending within the claustrum. No degen- inferior frontal gyrus were also carried in eration was seen either in the ventral the internal capsule to the red nucleus and claustrum or in the amygdala. to the lateral and the ventrolateral tegmen- Cortical association fibers from the in- tum around its capsule. ferior frontal gyrus, the insula and the From the frontal lesion degenerated fi- superior temporal gyrus entered the ex- bers, after a partial decussation, entered treme capsule on the side of their origin the common external and extreme capsules or deciissated to the other side. Some of bilaterally. Some cortical association fibers the crossing fibers reached the extreme were distributed through the extreme cap- capsule on the contralateral side and con- sule to the insular cortex, others passed tinued caudoventrally in it. Bilaterally, CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 307 then, at the posterior end of the putamen, and the nucleus of the field of Forel, where, these fibers collected and joined fibers of after some synapse, they discharged into the external capsule passing over the cap- the red nucleus. sule of the lateral geniculate nucleus. Microscopic examination of the left Both groups of fibers projected directly into hemisphere showed destruction of the the red nucleus and the lateral and ventro- frontal and the temporal opercula as well lateral tegmentum around it. as of the insular cortex. The lesion ex- Fibers from the frontal cortex, the in- tended medially to involve the extreme cap- sula, and the temporal operculum were dis- sule, the ventral claustrum, the external tributed into the external capsule. A few capsule, and the ventrolateral margin of of these fibers passed medialward into the the putamen. A ventral extension of the lateral margin of the putamen, but the lesion involved the superior temporal gyrus majority of them were contained within and the lateral part of the middle temporal the capsular boundary passing caudoven- gyrus. From the left inferior frontal gyrus trally until they were joined postlenticu- degenerating fibers were traced into the larly by fibers in the extreme capsule. corona radiata and throughout the white Other degenerated fibers continued into matter of the superior and the middle the lateral border of the putamen but could frontal gyri. Fine Marchi granules were not be followed very far due to their deli- followed into the anterior limb of the in- cate medullation. ternal capsule and into the cingulate gyrus. From the lesion in the superior temporal Degenerated commissural fibers passed in- gyrus, degenerated cortical association to the corpus callosum to distribute contra- fibers turned ventrally into the middle laterally to the cingulate gyrus, throughout temporal gyrus. Connections with the in- the frontal lobe at the level of the lesion, ferior temporal and hippocampal gyri were and into the anterior limb of the internal also noted. Due to the extensiveness of the capsule. No Marchi granules were found island lesion anteriorly (which included in the caudate nuclei. Fibers from the the external and extreme capsules as well frontal operculum coursed into the junc- as the temporal operculum) the origin of tion of the external and the extreme cap- fibers turning into the external and ex- sules rostrally and into both the external treme capsules could not be determined. and the extreme capsules as they became However, contributions from the temporal separated more posteriorly. lobe were traced into both the external Degenerated fibers from the insular cor- and the extreme capsules posteriorly. De- tex were followed into the extreme capsule generating fascicles from the superior and (fig. 25). Some fibers radiated dorsally the middle temporal gyri crossed through toward the frontal lobe, others coursed the anterior commissure to distribute to ventrally in the extreme capsule toward the uncinate fasciculus, the inferior tem- the temporal cortex. Coarse and medium- poral gyrus and the hippocampal gyrus of sized degenerated fascicles from the island the opposite hemisphere. No fibers were extended medially through the extreme traced into the external capsule or to the capsule and the dorsal claustrum into the ventral claustrum of the right side. external capsule. Whether any synapse From the left frontal operculum, fibers occurred in the claustrum itself could not entered the anterior limb of the internal be determined. A few fine fibers coursed capsule on the side of the lesion and dis- medialward in the combined external and tributed, by way of the corpus callosum, extreme capsules to reach the posterior to the contralateral internal capsule. Bi- limb of the internal capsule (fig. 26). laterally, these degenerated fibers in the Other fibers turned ventrally and passed internal capsule turned ventrally into the obliquely, postlenticularly or sublenticu- globus pallidus. To this system were added larly, over the capsule of the lateral gen- fibers from the external capsule and the iculate nucleus to join corticotegmental corona radiata which coursed medialward fibers carried in the internal capsule and to reach the globus pallidus. Here some corticotegmental fibers passing through fibers ended; others continued through the the nucleus lateralis and the nucleus lenticular fasciculus to the zona incerta ventralis posterior pars lateralis of the 308 JOSEPH J. BERKE

dorsal thalamus. Still other corticoteg- bers interconnecting the injured cortical mental fibers in the ansa lenticularis were regions. A few fine fibers passed from the added to the common paths which dis- extreme capsule to the dorsal claustrum charged to the lateral and ventrolateral and into the external capsule. Whether tegmentum around the red nucleus. A any of these fibers ended within the claus- few corticonigral fibers were traced to the trum could not be determined, due to their substantia nigra. paucity and delicate myelination. Other Degenerated fascicles were traced from fibers remained within the extreme capsule the inferior frontal gyrus into the corpus coursing caudoventrally within the cap- callosum to reach the midline septa1 nu- sular boundary to join fibers in the external clei. Some of these were followed into capsule as the capsules became confluent the fornix system. Fibers from the ex- at the caudal end of the lenticular nucleus. ternal capsule, the internal capsule, and These were projected as a common bundle the superior temporal gyrus passed into into the dorsolateral and lateral tegmen- the anterior commissure to distribute to tum around the red nucleus. the opposite hemisphere. Fibers from the inferior frontal gyrus, from insular cortex (which traversed the Protocol for inonhey 5 extreme capsule and dorsal claustrum) , Following a left froiitotemporal crani- and from the superior and the middle tem- ectomy, the dura was reflected, the tem- poral gyri entered the external capsule poral operculum partly ablated, and the (fig. 27). A few extremely fine fibers insular cortex exposed in a 3-kg female coursed medially into the putamen where macaque. During the proceeding, a hemor- they were seen at the lateral margin. Some rhage occurred in the insular region, which fibers interconnected the islznd with the necessitated packing the area with gelfoam frontal cortex but the great majority of the so that further manipulation was con- fascicles passed posteriorly in the external sidered inadvisable. capsule. The more dorsal fibers swung Two weeks later a right frontal crani- ventromedialward behind the lenticular ectomy was carried out, the dura opened, nucleus; the others turned postlenticularly and the central fissure exposed. Stimula- or sublenticularly to join fibers in the pos- tion of the region just rostra1 to this fissure terior limb of the internal capsule. To- on the lateral hemisphere wall produced gether, as a common bundle, the fibers movcments of the contralateral upper ex- were projected over the capsule of the tremity. A lesion was made in this “arm” lateral geniculate nucleus (fig. 29) into area with a surgical aspirator. the lateral and dorsolateral tegmentum Following the experimental injury the around the red nucleus where thev came animal showed an unwillingness to use into association with corticotegmental fi- her left upper extremity and carried this bers which traversed the nucleus lateralis limb in a peculiar position of extension at and nucleus ventralis posterior pars later- the wrist and elbow. The tonus appeared alis of the dorsal thalamus. Some of these to be the same in the two upper extremities. fibers entered the pons with the cortico- When the brain was removed, following pontine fibers from the anterior limb of sacrifice and perfusion of the animal, a the internal capsule. This corticopontine right frontal lesion involving area 4 on the system originated in the frontal operculum. lateral surface posterior to the middle third A few fine fibers were traced into the sub- of the arcuate fissure was noted (fig. 5). stantia nigra. On the left side, removal of a portion of Corticotegmental fibers of many origins the frontal and the temporal opercula had and by several pathways were thus pro- been accomplished and there was a lesion jected into the lateral and the dorsolateral in the insula (fig. 6). tegmentum around the red nucleus. Fibers The extreme capsule contained degen- that traveled by way of the basal ganglia erated fibers from the frontal operculum, (fig. 28), fibers from the posterior limb of from the insular cortex (fig. 27) and from the internal capsule, fibers through the the superior and the middle temporal gyri. nucleus lateralis and nucleus ventralis These were predominantly association fi- posterior of the dorsal thalamus, and fas- CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 309 cicles that traversed the extreme and the The animal had a stormy postoperative external capsules all converged to a com- course due to rhinorrhea and difficult res- mon termination in the red nucleus and piration. No impairment of motor func- the lateral and the dorsolateral tegmentum tion or neurologic change in behavior was around this nucleus. noted up until the time she was sacrificed Microscopically, the lesion on the right and perfused about two weeks after the side involved the dorsolateral portion of experiment. area 4. A coarse granular degeneration ex- Microscopic examination revealed a le- tended into the corona radiata and distri- sion of the left middle frontal gyrus involv- buted into the dorsomedial portion of the ing the superficial cortex and extending superior frontal gyrus as well as to the into the underlying white matter. A left middle and the inferior frontal gyri. A few temporal lesion destroying the rostral por- degenerated fibers entered the dorsal part tion of the temporal operculum was also of the external capsule. No connection noted. with the extreme capsule was noted. Com- Marchi granules from the middle frontal missural fibers were traced into the corpus gyrus spread diffusely into the white mat- callosum, passing through the corona radi- ter, through the corona radiata, and into ata to the superior frontal gyrus and the the superior and the inferior frontal gyri. internal capsule of the opposite hemi- Degenerated commissural fibers traveled, sphere. From the ipsilateral internal cap- by way of the corpus callosum, into the sule, a few coarse fibers were followed into corresponding regions of the opposite hemi- the globus pallidus. These fibers lost their sphere. Degenerated fibers were followed heavy medullated sheaths, and whether also into the internal capsule and the com- they terminated in the globus pallidus or mon external and extreme capsule hilater- continued into the lenticular fasciculus to ally. An exceedingly few fibers from the reach the red nucleus could not be deter- subcallosal bundle and from the surround- mined. Some coarse fibers extended into ing white matter entered the head of the the dorsal thalamus and passed through caudate nucleus bilaterally and spread the nucleus lateralis and the nucleus ven- throughout it. Possibly some fibers termi- tralis posterior pars lateralis to the dorso- nated; a few passed into the putamen lateral and the lateral portions of midbrain through the anterior limb of the internal tegnieritum near the red nucleus. The great capsule by way of the gray bridges. hlost majority of fibers traveled as a dense bun- of the degenerated fibers from the frontal dle in the genu and the posterior limb of lesion passed ventralward, medial to the the internal capsule as the corticospinal anterior limb o€ the internal capsule, di- tract. passing through the pes pedunculi rectly into the putamen. Some of these and the base of the pons to form the pyra- fibers continued to the base of the hemi- mid. Some coarse granulation indicated de- sphere into the diagonal band of Broca generated heavily medullated fibers, which beneath the anterior commissure. A few were traced through the corpus callosum reachcd nucleus accumbens. A few me- to reach the contralateral internal capsule dium and fine Marchi granules were traced and then were followed down through the from the anterior limb of the internal cap- brainstem into the pyramid at medulla sule into the putarnen. A small number levels of degenerated fibers appeared medially in the globus pallidus where they were Protocol for monkey 6 joined by other fibers from the internal '4 left frontotemporal craniectomy was capsule. Some degenerated fibers were carried out on a 3.7-kg female macaque. followed from the globus pallidus into the After the dura was reflected, the arcuate ansa lenticularis; a few such fibers from and the principal fissures were identified the base of the hemisphere also turned dor- and a considerable pcrtion of area 8 (fig. 7) sally into the ansa lenticularis. Neither of dorsal to the principal fissure and rostral these contributions was large. Other de- to the arcuate fissure was ablated. A generated fascicles were followed, how- second lesion was placed in the temporal ever, into the lenticular fasciculus, to the operculum (fig. 8). zona incerta, and to the nucleus of the 310 JOSEPH J. BERKE field of Forel where some ended. Other of the corona radiata, and turned into the small fascicles continued to discharge into internal capsule at more caudal levels. the red nucleus. the tegmeritum dorso- Some fibers accumulated in the corona lateral, lateral and ventral to it, the nucleus radiata at parietal levels and passed di- of Darkschewitsch, and the oculomotor nu- rectly into the posterior limb of the internal cleus (entering its lateral side). Still other capsule. A few entered the external cap- degenerated fibers traveled along the ansa sule at the posterior end of the lenticular to reach the region behind the red nucleus. nucleus and traveled obliquely ventrome- Some fibers (and a few delicate fascicles dially across the dorsal part of the putamen from the internal capsule) turned medial- to reach the internal capsule. From many ward into and through the nucleus ven- areas fibers were traced through the tralis posterior pars lateralis to course to internd capsule. Some fibers of the the red nucleus and the surrounding teg- internal capsule turned off to the puta- mentum. Scattered Marchi granules were men and the globus pallidus bilaterally. found in the substantia nigra. Others turned medially through the nu- Marchi granules indicated that degener- cleus lateralis and the nucleus ventralis ated fascicles passed from the left frontal posterior pars lateralis to enter the red cortex into the common external and ex- nucleus and the dorsolateral, the ventral treme capsule rostrally on each side of the and the lateral areas of the tegmentum brain, those to the right hemisphere having adjacent to it. Joining this system were crossed through the corpus callosum. corticotegmental fibers carried in the pos- When the external and the extreme cap- terior limb of the internal capsuie which sules became separated, some degeneration discharged directly into the tegmentum of was seen in each. Fewer degenerated fi- the midbrain. Corticobulbar fibers in the bers were seen on the contralateral side inteinal capsule entered the oculomotor than on the side of the lesion. In the ex- nucleus ventrally to continue caudal to it. treme capsule, medium and fine degener- A few frontopontine fibers were noted. ated fibers were scattered ventrally and Marchi granules in the region of the caudoventrally toward the temporal lobe. lesion in the left temporal operculum were In the superior temporal gyrus, they were also identified in serial sections. A few augmented by fascicles extending from the medium and fine fibers traveled into the lesion in the left temporal operculum. To- extreme capsule. These were quite diffuse gether the degenerated bundles traveled to and could not be traced for any consider- the middle and the inferior temporal gyri. able distance within this capsule. No fibers A few fibers passed to the hippocampal passed into the insular cortex. This lesion gyrus. The cortical association fibers in was extremely small, however, and the de- the extreme capsde were joined by fibers generated fibers were very few and quite passing from the external capsule through diffuse, making this series quite unsatis- the dorsal claustrum. Whether any of factory for determining connections of the these terminated in the claustrum could temporal lobe with the frontal or the in- not be determined. Little evidence of con- sular cortices. However, a few fibers nections with insular cortex was found. spread from the lesion into the middle and The components of the extreme capsule the inferior temporal gyri and the hippo- are cortical association fibers. campal gyrus. Some Marchi granules were In the most rostra1 sections, a few de- found in the inferior longitudinal bundle; generating fibers were noted in the exter- a few Marchi-stained fibers traveled be- nal capsule. These coursed laterally neath the ventral claustrum to the ventral through the dorsal claustrum and entered part of the external capsule. No degenera- the extreme capsule as cortical association tion was seen in the ventral claustrum. fibers. No contribution to the putamen however. The degenerated fibers in the from the external capsule was seen. inferior longitudinal bundle and in the From the frontal lesion, fibers entered ventral part of the external capsule main- the anterior limb of the internal capsule tained their position in serial sections until directly to become corticobulbar fibers. they reached the posterior part of the puta- Others coursed in the association bundles men. Here, as a few diffuse fibers, they CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 31 1

turned medialward, postlenticularly or sub- Due to the involvement of the tip of the lenticularly, over the capsule of the lateral parietal operculum, Marchi granules were geniculate nucleus to reach the usual mid- present in the extreme capsule, the dorsal briin areas. A few fibers entered the sub- claustrum, and the external capsule. The stantia nigra. A few temporopontine fibers degenerated fibers represented by these were also identified. granules also entered the corona radiata to spread throughout the parietal lobe and Protocol for monkey 7 into the posterior limb of the internal cap- A temporal craniectomy was performed sule. Commissural fibers, by way of the 011 a 3.1-kg female macaque, the dura re- corpus callosuni, projected impulses to cor- flected and ablation of left area 22 (fig. 9) responding areas of the two sides due to accomplished with a surgical aspirator. the bilaterality of the lesions. A few fibers The animal showed no ill effects from the were traced to the cingulate gyrus on both experiment during the next 10 days. At sides. Several fine fascicles from the sub- the end of this period, a similar operation callosal bundle passed into the head of the was carried out in the opposite hemisphere. caudate nucleus and into the putamen During the succeedir,g two weeks, the ani- through the gray bridges. From the corona mal showed no demonstrable defects. radiata. from the posterior limb of the in- Then, she was sacrificed and perfused and ternal capsule, and from the external cap- the brain removed and prepared for study scle, fibers coursed into the putamen and, by the hiarchi technique through it, into the globus pallidus. be- Post mortem examination of the brain yond which some fibers could not be showed bilateral lesions of the posterior traced. Other fascicles entered the globus portion of each temporal operculum. The pallidus from the internal capsule and lesion in right area 22 (fig. 10) was continued through the lenticular f asciculus slightly deeper than that in aiea 22 on the and the ansa lenticularis to the red nucleus left. and the tegmentum lateral to it. To this Microscopic observation revealed bilat- system were added fibers from thc poste- eral destruction of a portion of the tem- rior limb of the infernal capsule and the poral operculum Tne lesion on the right corona radiata, traversing the nucleus side involved the base of the island and lateralis and the nucleus ventralis posterior transected the extreme capsule and the pars lateralis of the dorsal thalamus. All lateral third of the ventral claustrum. The these ended in the red nucleus and the left-sided lesion invch ed superficial tem- tegmental areas surrounding the capsule poral opercular cortex and the underlying of this nucleus. white matter. Injury to the edges of both Most of the fibers cairied in the extreme kft and right parietal opercula were noted. capsules were cortical association fibers. The lesions were essentially the same on They aroqe in parietal 2nd temporal oper- the two sides so the paths on the left side cula and intercocmcied pnrietal, insular, orily are reported. and temporal cor’tices. Some fine fibers re- Fibers from the temporal operculum mained in thc extrcine capsule working were traced into the extreme capsule. their way c~udoventrallvto join fibers in Some continued dorsally within the cap- the external c~psule.These various fibers sule to distribi-ite to the parietal operculum. extended dorsal to 2nd then medial to the Other cortical association fibers coursed lateral geniculate nucleus to enter the teg- ventrally into the middle and the inferior mentum laternl to the red nucleus. temporal gyri and into the hippocampal In the external capsule were fibers from gyrus. A few fine fibers passed through the parietal operculum and contributions from extreme capsule into the dorsal claustrurn the superior temporal gyrus which passed and through this area into the external through the dorsal claustrum. A few fine capsule. Whether any fibers terminated fibers were traced into the putamen. These within the claustrum could not be deter- were extremely delicate and could not be mined. A few fine fibers connected the followed for any considerable distance, superior temporal gyrus with the insular However, the majority of fibers remained cortex. within the external capsule as the extreme 312 JOSEPH J. BERKE

and external capsules became confluent superior colliculus as corticotectal fibers. behind the putamen. Here the degenera- In the tectum a few fibers crossed in the tion granules from the external capsule commissure of the superior colliculus. passed obliquely behind the lenticular nu- Numerous degenerating association fi- cleus to join corticotegmental and cortico- bers extended anteriorly in the superior pontine fibers in the posterior limb of the longitudinal fasciculus to connect the pa- internal capsule. As the external and ex- rietal with the frontal lobe. Fibers were treme capsules united ventrally, other fi- traced from this region into the cingulum bers from the temporal lesions in the oper- and to the cingulate gyrus, bilaterally. culum accumulated in a bundle which Commissural fibers passed into the corpus coursed postlenticularly and then sub- callosum at almost all levels Coarse. me- lenticularly over the capsule of the lateral dium-sized, and fine Marchi granules were geniculate nucleus directly into the red found in the corona radiata and in the pos- nucleus and the midbrain tegmentum. terior limb of the internal capsule. The Some of these fibers from the posterior degenerated fibers turned medialward into aspect of the superior temporal gyrus were and through the nucleus lateralis and the projected as corticopontine fibers. A few nucleus ventralis posterior pars lateralis to fibers were traced to the substantia nigra. discharge to the zona incerta, the red nu- cleus and the dorsolateral, lateral, and Protocol for monkey 8 ventrolateral tegmental arex around the The anterior portion of area 7 was de- red nucleus. Some of these fibers crossed stroyed in a 4.8-kg female macaque (fig. in the teginentum of the midbrain. In the 11 ). No evidences of the injury were seen posterior limb of the internal capsule were during the next two weeks. At the end of also parietopontine fibers, which passed in- the period the animal was sacrificed and to the pes pedunculi and entered the pons. perfused and the brain removed and pre- Fibers from the corona radiata entered pared for microscopic study. the anterior limb of the internal capsule hlicroscopic examination showed de- at frontal lobe levels. A few fibers entered struction of the parietal cortex an the the putamen. Here some of them could be dorsolateral surface, corresponding to area followed no farther, but other fibers 7. This lesion involved also the underly- coursed niedially into the globus pallidus ing white matter. Many diffuse, medium- where many more fascicles were added sized to fine granliles were present through- from the internal capsule. Fine degenera- out the parietal lobe :It the level of the tion granules were seen ventrally in the lesion and in the white matter of the dnq i Imticularis and could be traced along temporal lobe, the fusiform and the lingual fiber bundles projecting into the lateral, gyri, and the sagittal stratum. Degener- the dorsolateral, and the ventrolateral teg- ated fascicles were present in the white meiital areas of the midbrain. Degener- matter beneath the posterior part of the ated fibers in the globus pallidus turned insula. A few fibers entered the insular dorsally to enter the lenticular fasciculus, cortex, but the majority of the cortical the zona incerta, the nucleus of the field of association fibers corinected the parietal Forel and ultimately the red nucleus. To with the temporal lobe. Some Marchi gran- this system were added corticotegmental ules were also found in the tapetum, the fibers that discharged directly into the teg- alveus, the gyrus fornicatus, and the lin- mentum. These were carried in the in- gual gvrus. Numerous degenerated fibers ternal capsule. Similar discharge paths from the left corona radiata passed into were found in the other hemisphere. the splenium of the corpus callosum. They Cortical association fibers from the pa- connected the corresponding regions of the rietal lesion could be followed to the more two hemispheres. Fibers distributed to the caudal portions of the temporal lobe. lateral and caudal part of the pulvinar bi- These were traced rostrally in the inferior laterally, some fascicles having crossed in longitudinal fasciculus where they col- the corpus callosum. Some of the fibers lected at the caudal end of the lenticular ended in the pulvinar but others coursed nucleus. Some of these fibers were traced through the pulvinar (fig. 30) to enter the medialward, then postlenticularly or sub- CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 313

lenticularly over the capsule of the lateral the lateral and the caudal parts of the pul- geniculate nucleus to the tegmental areas, vinar before and after decussation. This including the red nucleus. relation was much more pronounced on A few fibers joined the corticopontine the left side, however. Here some fibers en- fibers in the posterior limb of the internal tered, but others continued into the supe- capsule as a contribution to this system rior colliculus (especially on the left side) from the temporal lobe. No Marchi de- as corticotectal fibers. Within the tectum, generation granules were seen in the ex- a few fibers crossed in the commissure of ternal capsule, the claustrum, or the ex- the superior colliculus. Some degenerated treme capsule. fascicles coursed directly into the tegmen- tum of the midbrain, as corticotegmental Protocol for monkey 9 fibers. A left parieto-occipital skin incision was In the inferior longitudinal fasciculus made, the parietal bone rongeured and the were cortical association fibers that could underlying dura reflected in a 5.5-kg be traced from the preoccipital area to the healthy male macaque. The dorsal portion temporal lobes of both hemispheres, a of area 19 and a small portion of the ad- partial decussation occurring through the joining area 18 were ablated (fig. 12). No corpus callosum. A very few fibers coursed motor defects were noted following this medially, postlenticularly or sublenticu- lesion. larly, over the capsule of the lateral gen- After two weeks, following the usual pro- iculate nucleus to reach the red nucleus cedure, the brain was removed and ex- and the midbrain tegmentum. amined grossly. A left preoccipital lesion Some cortical association fibers also involving the superficial cortex and the traveled anteriorly in the superior longi- underlying white matter of the dorsal por- tudinal fasciculus, connecting the parietal tion of area 19 was seen. A right-sided with the frontal lobe. Crossed fascicles destruction of surface cortex behind the reached the contralateral frontal area. central part of the sensory cortex was also From the corona radiata, fibers entered the evident. Coronal sections were made and posterior part of the cingulum. At almost the brain was stained using the Marchi all levels, degenerated fibers, as indicated . method. by Marchi granules, passed bilaterally into Microscopic examination of the brain the corpus callosum, from the corona ra- revealed a destruction of the left preoccipi- diata. A few fine fibers entered the nucleus tal cortex in the dorsal portion of area 19. ventralis posterior pars lateralis bilater- This lesion involved the underlying white ally, but their termination is uncertain. All matter and spread throughout the adjoin- of these various fascicles spread in the ing areas. Diffuse, medium and fine gran- ventral, ventrolateral, lateral, and the ules were present in the sagittal strata. dorsolateral tegmentum around the red nu- Association fibers connected the parietal cleus or in the red nucleus itself. Some with the temporal lobe, coursing into the crossing of fibers in the tegmentum was fusiform and the lingual gyri. A few fine noted. fibers were noted in the white matter be- DISCUSSION neath the posterior part of the insula. Patterns of body movement elicited by Some granules were seen also in the ta- the stimulation of cortical areas other than petum, the alveus, the gyrus fornicatus, the precentral motor cortex have been de- and the lingual gyrus. Degeneration from scribed in primates (Peele, ’44; Sugar, the parietal lesion of right area 5 was seen. Chusid and French, ’48; Fleming and However, the preparations were unsatis- Crosby, ’55; Travis, ’55; Crosby, ’56; Cros- factory for a study of the cortical projec- by, Humphrey and Showers, ’59; Schneider tion systems. Commissural fibers passed and Crosby, ’59; and others). The regions into the splenium of the corpus callosum that exhibited these movements are both and intermingled with degenerated fas- numerous and extensive. They have been cicles from the lesion on the left side. The named “supplementary motor areas” (Pen- terminations of these commissural fibers field and Welch, ’51) or “second” motor could not be determined. Fibers entered areas (Woolsey, ’47). The stimulation of 314 JOSEPH J. BEKKE

these regions does not produce discrete, ber of extrapyramidal avenues of descent highly specialized movements. These sec- have been found in anatomical and physio- ond motor areas also have a somewhat logical studies (Mettler, '35a, '35b; Levin, greater threshold for excitation than does '36; Ward, '48; Crosby and Henderson, the motor cortex. '48; Meyer, '49; Wall and Davis, '51; Lem- Foerster ('31) reported a pattern of men, '51; Poirier, '51; Jasper, Ajmone- gross body movements from the stimula- Marsan, and Stoll, '51; and many other tion of area 6. This pattern was still de- observers). monstrable after area 4 had been ablated, Dusser de Barenne, Garol and McCul- which suggested that the movements were loch ('40) reported a discharge pathway a result of independent functioning of area from area 5 and the premotor cortex into 6. Similar findings have also been reported the putamen and the globus pallidus. by Horsley and Schaefer (1888); Vogt and From the globus pallidus, fibers course Vogt ('26) ; Woolsey and Settlage ('50), into, arid through the lenticular fasciculus Erickson and Woolsey ('51), Penfield and and the ansa lenticularis (Woodburne, Welch ('51), and Travis ('55). The two Crosby, and McCotter, '46; Laursen, '55). latter groups of observers amplified this Some fibers terminate in the zona incerta pattern and carried it on to the medial sur- and in the nucleus of the field of Forel. face of the cerebral hemisphere rostra1 to I-Iowevcr, others continue into the red nu- the precentral cortex. cleus, the interstitial nucleus of the median Ipsilateral facial movements of both the longitudinal fasciculus, the nucleus of upper and the lower face, were elicited in Darkschewitsch, and the tegmentum sur- monkeys by the stimulation of the pre- rounding the red nucleus dorsally, later- central gyrus (motor cortex) above the ally and ventrally. Descending systems subcentral dimple (Lauer, '52). Similar from the red nucleus and the midbrain movements have been found by Garol tegmentum into the spinal cord have been ('42b) in the cat. Ipsilateral responses of well documented. the extremities from stimulation of the From the anterior portion of the tem- motor cortex itself were reported by Bucy poral lobe of Mncaca mulatta, Poirier ('51) and Fulton ('33). followed fiber bundles into the pulvinar. A primary motor eye center, located in Crosby ('56) traced degenerated fibers in area 8 above the principal fissure, has long Marchi preparations from the temporal been known (Vogt and Vogt, '26; Foerster, pole into the putamen and globus pallidus. '31; Penfield and Rasmussen, '50). The Lenimen, in 1951, reported projection path- pattern of eye movements on it were de- ways from areas 19 and 22 into the basal scribed by Crosby, Yoss and Henderson ganglia, the substantia nigra, the red nu- ('52) and others. From a portion of the cleus, and the tegmentum of the midbrain. insula in the monkey, Frontera ('55) has The supplementary motor areas appear also reported the presence of a second to function as a region of discharge for motor area. Later, ('56), he regarded this association areas which have received im- region as concerned largely with visceral pulses from various cortical centers dom- functions. inated by auditory, visual, gustatory, and The preoccipital and the occipital re- olfactory stimuli. Visceral sensory re- gions have shown conjugate horizontal eye sponses and the gross movements of the deviations upon stimulation. A detailed face and the extremities that are asso- pattern of eye movements from these re- ciated with the discrete, specialized motor gions of the macaque has been described acts and by which the individual's per- by Crosby and Henderson ('48), Hender- sonality is expressed (Crosby, Humphrey son and Crosby ('52), and was reviewed and Showers, '59), may serve as important by Crosby ('56). functions of these areas. The gross move- Corticofugal pathways discharging from ments of the contralateral face and ex- some of the supplementary motor areas tremities probably are made possible by have been described. Some of these fibers incomplete substitution of the functioning reach lower centers by way of the pyra- of additional motor areas for that of pri- midal tract. However. a significant num- mary motor areas, after destruction of the CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 315 precentral motor cortex or the pyramidal external capsule. Some of these bundles tract . coursed caudoventrally within this cap- Lesions in the frontal. temporal, insular. sule until the external and the extreme parietal, and preoccipital cortices were capsules became confluent at the posterior made as a part of this experimental study. part of the putamen. Here the fascicles From these regions. many avenues of dis- turned medially, postlenticularly or sub- charge to lower centers were demonstrated lenticularly, over the capsule of the lateral in the AIarchi preparations of the monkey geniculate nucleus and through the pos- brains. Cortical association fibers spread terior limb of the internal capsule. to reach l'rom the lesions into the ipsilateral corona the red nucleus and the tegmentum around ladiata and into the white matter of the it. Fiber contribution from the extreme s;inie hemisphere. Commissural fibers capsule appeared to add to this projection course by way of the corpus callosum into system but formed a minor component. the corresponding regions of the opposite Corticotegmental fibers that followed a hemisphere. slightly different course were also noted Corticofugal fibers. as indicated by me- within the external capsule. From the tl iu ni-sized an d fine degeri era tion gr anu1 e s . frontal cortex. degenerated fascicles. indi- ~vei'c, traced from the lesions. A few me- cated by medium and fine granules. en- dirim and fine fiber bundles from the suh- tered the external capsule from the corona cdlosal liiiiidle. from the anterior limb of radiata At the h.el of the decussation of the internal capsule. and from the corona the anterior' commissure. these fibers ixdiatn passed into the head of the caudate turned medialw:i~d into the putamen. nucleus in frontal lobe lesions. Here some traveled behind the anterior cormnissure, fi !I c' r s t e 1,111in ate d but o the r s entered the and reached the ;msa lenticularis to ter- putmic.11 and or the globus p:illidus where minate in the tegmeiituni ai~ound and the!- were ,joined by corticostriate and cor- cr?udal to thc. red nucleus. In another in- ticopalliclal fibers from the internal cap- stance. fiber Imndles left the externd cap- sulc. \lnny of these bundles discharged sule uid turiietl i.cntrally toward the base hy iv;iy of' the globus pallidus 01' c-'ii,ectly of the heniisphc~~c~\vherc> some fibers ended iiito the lenticular fxcicalus to end in the in the diaqonal b:rncl of Broca. The major- /ona incerta and in the iiucleus of.' the ity of these filiers contiiiueci their course ficltl of' Foi~l.Other fibei,s conti!!licd to dorsnll y to tl1c 2\11 s a lent icul :iris. the %ona thc. rcd nucleus. the interstitial nucleus of' inccrtn. the tiiiclcus of the field of Forel. t 11 c ni cdi ;I n 1on qit u din ;I 1 fascicu 1u s . :in d ;rnd tlrc, tcgiiieiituni arouiid thc 1,ed nu- tiic Iiiicleus of Darkschewitxch Sonic fns- cleus. A f'cw fi!, l'roni the cstrcnic, cirp- c' i c 1 CJ s t LI rned 1.t.n t r :illy in to the an s a le n - sule p:issecl t h roii I?; h t li e doiwl el ~ILIs t ruin ticiilaiis thiuiiqh which the! entewcl thc 10 joiii this systfc'in. tciyientLTm \.entr:il ~111dcaudal to the red Destruction of the posterior parietal aiid ii~rcleirs.Cor~ticoriilii~al and corticoteLyneii- the piwccipital cortices produced derren- . c,irrieci in the internal capsule. ei.ated fascicles w1iic.h were followed into joiiied this system and were projected di- the postlcmticulai, dii isioli of the posterior 1 cxctly into the red nucleus and the teg- limb of the intemal capsule. These cor- iiic~iitiini of the niicltir~iin In addition. tic o t ec t nl an d c or t i c o tcgin en t a 1 hin dle s c'oi~ico~~ul~i~aland corticot~,:rnie~ital fihe1.s coursed through the puhhar and the pos- fi~onithc. coron~~radiata and the internal terior part of' the nucleus lateralis and the c:i!)sule entered the nucleus lateralis and caudal portioii of nucleus 1,entralis poste- iiucleus 1-entralis posterior pars lateralis of rior pars latei~alisof the dorsal t1ial:imus. tlic doi,sal thidanius. These bundles passed A few degencxited fibers ente1.ec1 the in- into. and through. the zona incerta and the ternal capsule and the globus pallidus iiucleus of the field of Forel to reach the where soiii~of thcse fibem ended. The red nucleus and the teginentum surround- remainder continued into the ans:i lenticu- ing this nucleus. laris aiid the lenticular fnsciculus. A l-ery Following frontal, temporal. anterior pa- few granules were noted in the caudal part rietal. and insular lesions. degenerated of the external kind the extreme capsules. corticotegimental fibers were traced to the Thus. it appeal's thut the posterior areas 316 JOSEPH J. BERKE of the brain discharge into the tegmentum treme capsule. A few delicate fascicles postlenticularly, whereas the more rostra1 turned laterally into the insular cortex. regions project primarily into the tegmen- After destruction of portions of the tum by means of the internal capsule, the island. medium and fine Marchi granules basal ganglia, and the external and the were followed into the extreme capsule. extreme capsules. Many of these bundles turned dorsally to Following destruction of area 4, coarse reach the inferior frontal gyrus. Cortical and medium Marchi granules were present association fibers interconnected the in- in the genu and posterior limb of the in- sula with the temporal lobe. ternal capsule. The degenerated fibers Although the great majority of fibers in were followed into the pes pedunculi and the extreme capsule are cortical associa- pyramid ipsilaterally. A few commissural tion bundles, a very few corticotegmental fibers traveled a similar course on the fibers were found. These fibers worked contralateral side. Fiber contributions in- their way caudoventrally within their cap- to the pyramidal tract from the premotor sular boundary until the external and the cortex were also noted. A very few fibers extreme capsules became confluent at the from the motor cortex appeared to turn caudal end of the putamen. At this poiIit. into the globus pallidus and into the ex- the fascicles joined corticotegmental f oers ternal capsule on the side of the lesion. in the external capsule and turned post- but the great majority of fibers were found lenticularly or sublenticularly over the cap- in the internal capsule. sule of the lateral geniculate nucleus And Corticopontine fibers from the frontal. through the posterior limb of the intirnal parietal, and the temporal cortices were capsule to project into the tegmentum seen. A few corticonigral fibers were around the red nucleus. A few fibers were traced from the frontal and the temporal exchanged between the external and the lobes into the substantia nigra. extreme capsule passing through the dorsal The extreme capsule contained fibers claustrurn. Whether any of these fibers that originated in frontal, parietal, tem- terminated in the claustrum could not be poral, and insular cortices. These fibers determined with certainty. were predominantly cortical association ‘The frontal and the parietal lobes con- fibers. From the superior, the middle, and tributed fibers to the extreme capsule from the inferior frontal gyri, fibers passed into the corona radiata. From the temporal the uncinate fasciculus to reach the supe- lobe and the island, fascicles also reached rior and the middle temporal gyri. Other the external capsule after passing through fibers were traced to the inferior temporal the extreme capsule and the claustrum. and the hippocampal gyri. The frontal The external capsule contained a few lobe was also connected with the insula by cortical association bundles from the fiber bundles that turned out from the extreme capsule. However, cortical pro- extreme capsule. These fibers could not jection fibers formed its major components. be followed for any considerable distance These arose from the frontal. parietal. in- within the insular cortex due to their ex- sular. and temporal lobes. Finely medul- tremely delicate myelination. lated fibers coursed medially from the ex- Degenerated fibers from lesions of the ternal capsule into the lateral border of parietal cortex were traced into the ex- the putamen. Such fibers were not nu- treme capsule. Cortical association fibers merous and could be traced only for short interconnected the parietal and the tem- distances due to their extremely delicate poral lobes. A few bundles entered the myelin sheaths. An avenue of cortical pro- insular cortex. These also were extremely jection to lower centers is found then in fine fascicles that were soon lost. the external capsule, which is conveniently Following lesions of the superior and the situated as a pathway for the discharge of middle temporal gyri, degenerated fibers supplementary motor areas. Some degen- were demonstrable in the extreme capsule. erated fibers, as indicated by medium and These traveled in the uncinate fasciculur fine degeneration granules, turn medially. to the frontal operculum. Also temporo- leave the external capsule, and enter the parietal fibers were seen within the ex- ventral part of the putamen at anterior CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 317 commissure levels. These bundles con- trum. However. the majority of these fas- tinue their course into the globus pallidus cicles are fibers of passage. Whether any toward the ansa lenticularis; some termi- fibers terminate in the claustrum is still nate in the zona incerta or in the nucleus questionable. of the field of Forel, others extend beyond Collaterals from the extreme and the ex- into the tegmentum around the red nucleus ternal capsules probably end near claustral as a part of the corticotegmental discharge cells. However, silver preparations showed system. a tangled network of indistinct fibers, giv- Fascicles in the external capsule extend ing no support to this idea. The Marchi toward the base of the hemisphere. Here material in this study did not contribute some fibers end in the diagonal band of any additional information in this regard Broca. Most of these fibers, however, turn due to the extremely fine myelin sheaths dorsally into the ansa lenticularis to reach that the claustral fibers possess. The claus- the tegmentum around the red nucleus. trum may offer some fiber contributions to Still. a third corticotegmental pathway the external and the extreme capsules. to enters the external capsule. These cortico- insular cortex, and to the putamen. Ex- fugal fibers gradually work their way perimental proof for this concept is still caudoventrally within their capsular lacking. boundary until the external and the ex- Mettler, Ades, Lipman, and Culler ('39) treme capsules become confluent at the inhibited a cortically evoked movement hy caudal end of the putamen. Here these simultaneous stimulation of cortex and fibers are joined by the few additional bun- claustrum. Kaada ('51 ) obtained similar dles that remain in the extreme capsule. results from excitation of the claustrum of Together, these fascicles travel medial- cats and monkeys. The present material is ward, postlenticularly and then sublenticu- not able to add much anatomical evidence larly, over the capsule of the lateral genicu- to substantiate these results. late nucleus and through the posterior limb If corresponding pathways exist in hu- of the internal capsule, to end in the teg- man brains, the corticotegmental fibers inentum around the red nucleus. that discharge through the external and the From frontal lesions, some fiber bundles extreme capsules assume clinical impor- course caudally into the superior longi- tance with the destruction of the genu and tudinal fasciculus and accumulate at pa- the posterior limb of the interiial capsule rietal levels. Many of these then swing due to hemorrhage or degenerative proc- into the region of junction of the external esses. Lesions of these types involve both and the extreme capsules and pass ventro- the pyramidal tract and the extrapyra- medially across the dorsal tip of the puta- midal fibers projecting through the inter- men to reach the posterior limb of the nal capsule and through the basal ganglia internal capsule. These fibers presumably by way of the lenticular fasciculus. Vol- add in part to the corticotegmental dis- untary, highly specialized movements of charge system. the contralateral face and the extremities The claustrum, in the beginning of this are lost as a result. Remaining functions study, was regarded as a possible region of become dependent upon the degree of sub- synapse in the relay for the discharge of stitution that is possible by means of the extrapyramidal systems from the cortical unimpaired projection systems from the second motor areas to the tegmentum of supplementary motor areas relaying the midbrain and the reticular gray. Ap- through the external and the extreme cap- parently, this relation is not demonstrable. sules into the tegmentum of the midbrain. Fibers from frontal, temporal, and in- Although the corticorubral and the cortico- sular areas sweep into the claustral region. tegmental fibers from individual second The external and the extreme capsules ex- motor areas are not numerous altogether, change fibers through the dorsal claustrum. these fibers constitute a considerable dis- In this experimental material, there is charge system. some evidence that temporal area 22, the SUMMARY premotor, and the more rostra1 portions of From the areas studied, fibers that ter- the frontal cortex contribute to the claus- minate in the claustrum are not numerous. 318 JOSEPH J. BERKE

Probably short collaterals are exchange4 Bechterew. W.v. 1899 Die Leitungsbnhnen in1 with the insular cortex and the basal Gehirn und Ruckenmark, 2nd ed. A. Georgi, $an- Leipzig. glia. Area 22. premotor cortex, and fron- Berlucchi. C. 1927 Richerchc di fine anatomia tal areas rostra1 to the precentral gyrus sul claustruni c sull' insula del gattc. Riv. contribute fibers to the claustrum. Most of Spcr. Frcniat.. 51; 125-157. Biancl-ti, L. 1922 Mechanism of the Brain and these are fibers of passage. Silver prepara- Function of' tlie Frontal Lobes. E. S. Livingston, tions showed no definite fibers heginning E:di~iburgh. or ending within the claustruin. Brockhaus. H. 1938 Zur nornlalen und patho- logischen Anatomic des Mandelkerngcbietes. J. The external capsule is composed pri- Psvchol. Neur., 49: 1-136.

marily of corticotegrnerital fibers. A few -. -~ 1940 Die Cvto- und Myeloarchitektonik cortical association fibers are presciit. dcxs Cortcx clausiralis uiid des Claustrun~beim h~enscl~en.Iliid.~ 49: 250-348. The extreme capsule is primarily a corti- Brotlmann. K. 1909 Vergleiclicndc Lokalis:i- cal association bundle iiiterconnc:ctin,.r tionslelire der Grosshirnrinde. J. A. Bartli. frontal. insular, and temporal corti 1.eipzig:. 324 pp. Purietal and temporal lobes also exch:ii.!ge Biicy, 1'. (C.. :ind J. F. Fulton 1933 Ipsilateral rcpresciitation it1 the motor and prcmotor cor- fibers through it. tcx of moilkeys. Brain, 56: 318-342. The external capsitle s impor- '. C.. ancl ll. Kliivcr 1955 An anatomical taiice due to the fascicles VES from tigtitioii 01 the temporal lobe in the nioii- ai'ea 3 and from the supplernentury motoi' 2M(~~,r~~,t~mri/c(/fo. J. Coiiip. Neur., 103: 151b252. areas as discharge pathways into thc, teg- Cii,j;il. S. 13;iiiihi v 1902 Stutlicn ubcr die Him- inciiturn of the midl)i,ain. It becoincs clin- rind(, dw M~*nschcii( 1900-1906). Traiisl. .J. ically sig1iific:int whcn lesions of the gmu I gross responses iii:iinni:ili::ii niitlbr:!iii and isthmus r(,gi(ins. thi.oitql1 thcxii dischargc to inotoi' ccntc:i's i)y v-ay of the tcgiiic'titiini. ~~o~icc~rnc~lin autoiii:iiic chc, iii(ivc>- nil>. Neur.. 88: 53-92. A C I< N O\\' 1.1:. I)(; M I.: NTS T, I~~~~~~~~II~~~~anti n4. J. SIIO\Y~.~C Ai?ordiiunr:cn. Vcrl)in:luiigen uiid 'pi::, a7It!lOr {vishcs to c~xpwsshis :ippre- rlcr supplcmc,iit~ircn incitririsc'lieri ci;ltioti to thc Lini\.c.i.sity of' Rlichjgari Aled- 1~iii:I~:ii. h4ctlizillische GriindlacciiI'(irs(~liu,ifi.2: C;corg l'liicnic. Siutiqart, YOI. 2. yp. 101b12-I. ic:il Scl~oollor thc- I)octot. 1,ottis I\/Icm,iti (J!.osl,v. 11. c.. I:. I:.. Yoss and ,I. TI'. Hc~Iltlerild !(I iiiid tlrr~iuyhniitlbrain levels. J. couy:IqcBmc'iit and direction ha (~(Jlll]>.hr('LIL. 357-383. illyc'stiqaiioil possiijl(>, T~c'tc.chnical assist- ~)~ivc~~~~ioi~t.11. A,. ;itid K. I.. S\r:ink 1935 RI:i:.c,hi ~taiiiin: nietliotl. 111. Artef'acts aiid cff'ccts (11 Llllcc'of the late Ni.. i;coi~l?;c~Sinith mc1 of p(,rl'kisiiiii. Stain 'l'c~lr.,70: 45- 53. 111.. Jmles Turlcy :iiitl MY.1"aul Syiin!.'1 :1rv Ikirriiic~..I. 1895 ?n;iioniic. tles Ccntrt.5 Ncr- 50 qr;~tefully ;IC hi I IJW~~CIjitd . \.C~CI\. ,I. Roiiff. Paris. D,itlxs(i~i. R4. C. 13. 1955 A congciiital iii,!I- LITF,R AI'I! RE C:1'1 Ell I~irii~~itio~i(11' in>ular curtex ill iii:in. involvilig ihr claiistriiiii iind ccrtain subcortic;il ccntc~s. ,\tl:i\. 11.. :ind \V. R. Iiipriiiii 1937 T~ip(igraph~ ,I. Conip. Neur., 102: 341-364. of' thr I)rain stciii (11 the rhesns mo~~lteywitli Ihissw (I(, B:ircwic J. C. IT. \V. Carol ;illd If7. S. special ref'crcijcc to the dirncepllalo~~.J. Comp. McCullocli 1940 Physiological ncuronograph-. Neur.. 66: 263-289. 01' tlic c,ortic.o-strintiII connections. Ites. Publ. Ayig12s Kappers, C. U. 1908 \Veiterc Miiteiliiii- Assoc. Nrrv. Mcnt. Dis.. 21: 246-266. ycn iiher tlie Phylogc~nese des Corpus striatun1 Ilrickson. T. C.. :ind C. N. \V~oolsey 1951 013- ulltl des Tlialanius. Anat. Anz., 33, S. 321. wrvatioiis oii thc supplcnicntary motor re:^ of' AriCiis Kappers. C. U.. G. C. IJuber :ind E. C. niiiii. Trails. Am. Neur. Assoc., 76: 50-56. Crosby 1936 Coniparative Anatomy of' thc Fat11. .I. 1926 The ontogenctic devclop~i~entoi Pu'ervous System of Vertebrates, Including Man. the cl:iustruni in ~nanniials. Konin. Aknti. Thc nfacmilla~iCo., New York, 2 vols. Ani\terti;im, 29: 642-G47. CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 319

Fleming, J. F. R.. and E. C. Crosby 1955 The brate forebrain. Kungl. Fisiogr. Sallsk. Handl. parietal lobe as an additional motor area: The N.F., 62: 3-34. motor effects of electrical stiinulation and abla- Katb, H. 1938 Zur Faserbeziehung der Area 52 tion of cortical areas 5 and 7 in monkeys. J. bei der Katze. Z. Mikr. Anat. For&.. 44: 606- Comp. Neur., 103: 485-512. 615. Foerster, 0. 1931 The cerebral cortex in man. Klingler, J. 1941 Ein zerlegbares hlodell der Lancet., 221: 309-312. Vorder- und Mittelliiriikerne des Menschen niit E‘oix. C.. and J. Nicolesco 1925 Les Noyaus Einschluss der angrenzenden Rindenpartien. Gris Centraux et la Region Mesencephalo-Sous- 2. Aiiiat. Entwgesch.. 111: 1-90. Optique. Masson et Cie, Paris. Kodama, S. 1927 Uber die sogenannten Basal- Fox. C. A,, W. A. McKinley and H. W.Magoun ganglien. 11. Pathologischanatoniische Unter- 1944 An oscillographic study of olfactory sys- suchungen mit Bezug auf die sogenannten tem of cats. J. Neurophysiol., 7: 1-16. Basalganglien und ihre Adnexe. Schweiz. Arch. f. Neur. u. Psychiat., 20: 209-261. Fox, C. A,, and J. T. Schmitz 1943 A Marchi Kuhlenbeck, €3. 1924 Uber den Ursprung der study of tlie distribution of the anterior com- Basalganglien des Grosshirns. Anat. Anz.. 58: missure in the cat. J. Comp. Neur.. 79: 297- 49-74. 3 14. Landau, E. 1!319 The comparative anatomy of ontera. J. G. 1955 Preliminary report on the the nucleus amyndalae. tlie claustrum and the results of electrical stimulation of the island insu1;ir cortex. .J. Anat.. 53: 251-262. of Reil ill the macaque. Anat. Rec.. 121: 296. 1923 Zur Kenntnis der Beziehung des .~ 1956 Some results obtained by elec- Claustrums zum Nucleus amygdalae und zur trical stiinulation of tlie cortex of the island Area pirif‘ormis. im speziellen zum Tractus of Reil in tlie brain of the nionkev (Mncticci olfactorius. Schw-eiz. Arch. Neur. Psychiat.. 13: 7t~it/ttttt~).J. Comp. Neur., 10,s: 365-394. 39 1-404. Carol; H. TV. 1942a Cortical origin and dis- 1936 Quelques nouvelles considerations tribution of cornus callosuni and anterior corn- sur l’avant mur. Arch. Anat. Strasbourg. 23: inissure in the cat. J. Neuropath. Exp. Neur., 165-1 81. 1 422-429. 1937 Un nouveau champ de substance 1942b Tlie “motor” cortex of the cat. grise dans le ceri‘eau humain. Bull. SOC.T’aud. Ibid.. I: 139-145. Sci. Nat., 59: No. 244. Henderson, J. Tr’.. and E. C. Crosby 1952 An 1938 Le claustrum parvum chez experimental study of optokiiietic responses. 1’Homnie. Mein. Soc. Vaud. Sci. Nat.. 41: 45-62. A.1l.A. Arch. Ophthal., 47: 43-54. Lauer, E. TI’. 1945 The nuclear pattern and Hilpert, P. 1928 Der Mendelkern des Men- fiber connections of certain basal telencephalic schen. J. Psychol. Neur., 36: 44-74. centers in tlie macaque. J. Comp. Neur., 82: Hirasawa. K.. and K. Kariya 1936 uber die 2 15-254. 1952 Ipsilateral facial representation korticalen extrapyramidalen Fasern aus den1 ___ in motor cortex of macaque. J. Neurophysiol.. motorischen Rindenfeld (Area 4a. b, c) beini Affeii (hlacacus Rhesus). Folia. Anat. Japon. 15: 1-4. 14: 603-620. Laursen, A. h4. 1955 An experimental study of the pat1iw:iys from thc basal ganglia. J. Comp. Hirasawa. K.. S. Okano and S. Kamio 1938 Bei- Neur., 102: 1-25. trag zur Kenntnis uber die corticalen extra- Le Gros Clark, XI’. E.. and M, hleyer 1947 Tlie pyramidalen Fasern der Area temporalis supe- terminal connexions of the olfactory tract in rior (Area 22) beini Affen. Z. Mikr. Anat. the rabbit. Brain. 70: 304-328. Forsch.. 44: 74-84. Leminen. L. J. 1951 An anatomical and ex- Horsley, V.. and E. A. Scliaefer 1888 A record perimen:al htudy of temporal and occipital of experiments upon the functions of the cere- association areas. J. Comp. Neur., 95: 521-560. bral cortex. Phil. Trans. Roy. Soc. Lond., I79B: Levin, P. 1936 The efferent fibers of the frontal 1-45. lobe of the monkey, Mtrcclctr 777 ~tltitt(t. Ibid., Humphrey, T. 1935 Certain relations and con- 63: 369-420. nections of the amygdaloid complex and of the Lockard; I. 1948 Certain developmental rela- commissures of the hemisphere in the bat. tions and filler connections of the triangular Anat. Rec., 61: 26. gyrus in prirnates. Ibid., 89: 349-386. -__ 1936 The telencephalon of the bat. I. Macehi, G. 1941 Considerazioni sull’ origine e The non-cortical nuclear masses and certain il significato del claustre nell’uonio. Ras. di pertinent fiber connections. J. Conip. Neur.; Biol. Umana. 2: 134-143. 65: 603-711. 1947 I1 problema del claustre uiiiano Jasper, H. H., C. Ajmone-Marsen and J. Stoll dal punto di vista ontogenetico. Pontiff. Acad. 1951 Electrophysiological studies of subcorti- Scient. Comment., 2: 205-240. cal connections of the anterior temporal region 1948 Sulla morfologia, struttura e rap- in cat. J. Neurophysiol., 14: 305-316. porti del claustre nell’uomo. I1 Cervello; 24: Kaada, B. 1951 Sornato-motor. autonomic, and 1-26. electro-corticographic responses to electrical 1951 Ontogenic development of the stimulation of the rhinencephalic and other olfactory telencephalon in man. J. Comp. Neur., structures in primates, cat and dog. Acta 95: 293-306. Physiol. Scand., 24: su~pl.83, 1-285. Mettler, F. A. 1935a Corticofugal fiber connec- Kallen, B. 1951 Embryological studies on the tions of the cortex of M~tctrca mztlnttn-the nuclei and their ho~nologization in the verte- frontal region. ]bid.- 61: 509-542. 320 JOSEPH J. BERKE

1935b Corticofugal fiber connections of cleus and clnustruni. J. Neurophysiol., 19: the cortex of Macucu .muluttn-the temFora1 325-339. region. Ibid., 63: 25-47. Smith, G. Elliot 1931 The nervous system. In: 1945 Fiber connections of the corpus Cunningham’s Anatomy, 6th ed. Wm. Wood. striatum of the monkey and baboon. Ibid., Baltimore. 82: 169-204. Smith, M. 1956 The recognition and preven- 1947 Extracortical connections of the tion of artefacts of the Marchi method. J. primate frontal cerebral cortex. 11. Cortico- Neur., Neurosurg. Psychiat., 19: 74-83. fugal connections. Ibid., 86: 119-166. Spiegel, E. 1919 Die kerme im Vorderhirn der Mettler, F. A,, fI. W. Ades, E. Lipman and E. A. Siiuger. Arb. Neur. Inst. Univ. Wien, 22: 418- Culler 1939 An extrapyramidal system. An 497. experimental demonstration of function. Arch. Sprenkel, H. B. van der 1926 Stria terminalis Neur. Psychiat., Chicago, 41: 984-995. and amygdala in the brain of the opossum Meyer, M. 1949 A study of efferent connections { Didelphis virgi.nia?za). J. Comp. Neur., 42: of the frontal lobe in the human brain after 211L254. leucotomy. Brain, 72: 265-296. Starzl. T. E., and H. W. Magoun 1951 Organ- Meynert, T. 1884 Psychiatrie. W. Braumuller, ization of the diffuse thalalnic projection sys- Wien, 288 pp. tem. J. Neurophysiol., 14: 133-146. Papez, J. W. 1929 Comparative Neurology. Thomas Y. Crowell Co., New York. Sterzi, G. 1915 Anatomia del sistem nervoso centralc dell’uonio. T. 1945 Fiber tracts of the amygdaloid 11. Ed. by A. Draghi, Padova. 1161 pp. region in the human brain, from a graphic reconstruction of the fiber connections and nu- Sugar. O.? J. G. Chusid and J. D. French 1948 clear masses. Anat. Rec., 91: 294. A second motor cortex in the monkey (Macacci Peek, T. L. 1944 Acute and chronic parietal ?nulattu). J. Neuropath. Exp. Neur., 7: 182- lobe ablations in monkeys. J. Neurophysiol., 190. 7: 269-286. Swank, R, L., and H. A. Davenport 1934 Penfield, W., and K. Welch 1951 The supplc- Marchi’s staining method and studies of some nientary motor area of the cerebral cortex. A of the underlying mechanisms involved. Stain clinical and experimental study. Arch. Neur. Tech., 9: 11-20. Psychiat., 66: 289-317. __- 1935 Chlorate-osmic formalin inethod Penfield, W., and T. Rasmussen 1950 The Cere- for staining degenerated myelin. Stain Tech., bral Cortex of Man. The Macmillan Co., New 10: 87-90. York, 248 pp. Travis, A. M. 1955 Neurological deficiencies Pintus, G. S. 1930 Struttura cellular e cito- after ablation of the precentral motor area in architettura dell’antimuro umano. Riv. Neur., Macucrr mulattu. Brain, 78: 174-198. 3: 289-312. 1931 Forma e connessioni griqie dell’ Vachananda, B. 1959 The major spinal affer- antimuro umano. Arch. Gen. Neur. Psichiat., ent systems to the cerebellum and the cerebel- 12: 16-28. lar corticonuclear connections in Macaca mu- -- 1932 Connessioni bianche dell’ anti- Zattu. J. Camp. Neur., 112: 303-351. muro umano. Ibid., 13: 9-20. Vogt, C., and 0. Vogt 1926 Die vergleichend- Poirier, L. J. 1951 Anatomical and experi- architektonische und die vergleichend-reizphys- mental studies of the temporal lobe of the iologische Felderung der Grosshirnrinde unter macaque. J. Camp. Neur., 96: 209-248. besonderer Berucksichtigung der menschlichen. Rae, A. S. L. 1954a The form and structure of Naturwiss., 14: 1190-1194. the huinan claustrum. Ibid., 100: 15-40. Volsch, M. 1906 Zur vergleichenden Anatomie 1954b The connections of the claus- des Mandelkerns und seiner Nachbargebilde. trum. Confinia Neurol., 14: 211-219. Arch. Mikr. Anat., 68: 573-583. Randacio, Prof. 1882 On the relations of the 1910 Zur vergleichenden Anatomie das nucleus taeniformis with the olfactory nerve. Mandelkerns und seiner Nachbargebilde. Ibid., J. Anat. Physiol., 16: 151-152. 76: 373-523. Riley, 1943 An atlas of the basal gan- H. A. Vries, E. de 1910 Bemerkungen zur Ontogenie glia, brain stem and spinal cord. Williams and und Phylogenie des Claustrums. Folia. Neuro- Wilkins Co., Baltimore, 708 pp. biol., 4: 481-513. Rose, M. 1928 Die Ontogenie der Inselrinde. Zugleich ein Beitrag zur histogenetischen Rin- Wall, P. D., and G. D. Davis 1951 Three cere- deneinteilung. J. Psychol. Neur., 36: 182-209. bral cortical systenis affecting autonomic func- Rosegay, H. 1944 An experimental investiga- tion. J. Neurophysiol., 14: 507-517. tion of the connections between the corpus Ward, A. A. 1948 The cingulate gyrus. Area striatum and the substantia nigra in the cat. 24. Ibid., 11: 13-23. J. Camp. Neur., 80: 293-322. Whitaker, J. R. 1921 Anatomy of the brain Schneider, R. C., and E. C. Crosby 1960 A study and spinal cord, 5th ed. E. S. Livingston, Edin- of shifts of tonus and motor dysfunction from burgh. brain lesions in primates. Proc. 2nd Interna- Wilson, S. A. K. 1914 An experimental re- tional Neurobiological Congress, Amsterdam, search into the anatomy and physiology of the Sept. 1959. In press. corpus striatum. Brain, 36: 427492. Segundo, J. P., and X. Machne 1956 Unitary Woodburne, R. T., E. C. Crosby and R. E. responses to afferent volleys in lenticular nu- McCotter 1946 The mammalian midbrain CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE 32 1

and isthmus regions. Part 11. The fiber con- TYoolsey, C. N., and P. H. Settlage 1950 Pattern nections. 4. The relations of the tegmentum of localization in the precentral motor cortex of the midbrain with the basal ganglia in of Muctrcci mukrttn. Fed. Proc., 9: 140. Mncnca mulattn. J. Comp. Neur., 85: 67-92. Young, M. W. 1936 The nuclear pattern and

TVoolsev.,, C. N. 1947 The somatic functions of fiber connections of the non-cortical centers of the central nervous system. Ann. Rev. Physiol., the telencephalon of the rabbit. J. Comp. Neur., 9: 525-552. 65: 295401. I t

PLATE 1

EXPLAXATION OF FIGURES

1 Brain 1. Ablation of areas 4 and 6 on left side. Right lesion involves areas 6, 8 and 9. 2 Brain 2. Lesion in areas 6 and 9 of the left hemisphere 3 Brain 3 showing lesions of the left hemisphere anterior and posterior to the arcuate fissure. A second lesion in the sensory cortex is also noted. 4 Brain 4 showing a lesion of left area 11 5 Brain 3 demonstrating an area 4 lesion of thc right hemisphere. 6 Brain 5 showing left sided lesions of the frontal and temporal opercula. An insular lesion has also been made.

322 CLAUSTRUiM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE PLATE 1 Joseph J. Berke

323 PLATE 2

EXPLANATION OF FIGURES

7 Brain 6 showing lesion of area 8. 8 Brain 6 showing a left superior temporal lesion. 9 Brain 7 demonstrating a left area 22 lesion. 10 Brain 7 with lesion of right area 22. 11 Brain 8 showing a lesion of area 7. 12 Brain 9 showing lesions in area 5 and preoccipital cortex of the left hemisphere.

324 CLAUSTRUM, EXTEFiNAL AND EXTREME CAPSULE OF MACAQUE PLATE 2 Joseph J. Berke

325 PLATE 3

EXPLANATION OF FIGURES

13 Photomicrograph showing Marchi degenerating fibers coursing from the caudate IIU- cleus into the putamen by way of the gray bridges. C, caudate nucleus: I, internal capsule; P, putamen. Brain 1. Marchi stain. :< 17.5. 14 Photomicrograph showing degeneration granules in the red nucleus (R). and the tegmentum surrounding the red nucleus. T. tegmentuin; 0. oculoinotor nerve; R. red nucleus. Brain 1. Marchi stain. >: 35. 15 Photomicrograph showing degeneration in the lenticular fasciculus (L) and in the internal capsule (I). Brain 1. Marchi stain. i 35. 16 Photomicrograph showing degenerated fascicles from the combined external and extreme capsules (C) passing caudal to the putainen (P) to the posterior limb of the internal capsule (I). Brain 1. Marchi stain. A 50. 17 Photomicrograph demonstrating Rlarchi granules in fascicles coursing over the capsule of the lateral geniculate nucleus (L.G.) into the tegmentum of the midbrain. D.T.. dorsal thalamus; I, internal capsule. Brain 1. Marchi stain. ?: 17.5.

18 Comparison of the pyramids (P) bilaterally. Brain 1. Marchi stain. ,(~17.5.

326 CLAVSTRUM, EXTEFNAL AND EXTREME CAPSULE OF LlACAQUE PLATE 3 Jiiiepli J. Berke

327 PLATE 4

EXPLANATION OF FIGURES

19 Photomicrograph showing Marchi granules in fascicles (arrows) leaving the external capsule (E.c.). C, claustrum; Ex. c., extreme capsule; I, insula; P; putamen. Brain 2. Marchi stain. x 17.5. 20 Photomicrograph showing degeneration granules in the lenticular fasciculus (L), I. internal capsule. Brain 3. Marchi stain. x 35. 21 Photomicrograph showing Marchi granules in fascicles (arrow) coursing at the base of the hemisphere (B.H.). A, anterior commissure. Brain 2. Marchi stain. x 17.5. 22 Photomicrograph showing Marchi granules in fibers passing across the ventral portion of the putamen (P), A, anterior commissure. Brain 3. Marchi stain. x 35. 23 Photomicrograph showing Marchi granules in fascicles (arrows) turning into the ansa lenticularis. G, globus pallidus; 0, optic tract. Brain 2. Marchi stain. i: 17.5. 24 Photomicrograph showing Marchi granules in the external capsule (E). Some of these course into the putamen (P), others continue within the external capsule. C, claustrum. Brain 3. Marchi stain. i: 50.

328 CLAUSTRUM, EXTERNAL AND EXTREME CAPSULE OF MACAQUE PLATE 4 Joseph J. Berke

329 PLATE 5

EXPLAh'.\TION OF FIGURE 5

25 Photoiiiicrograpli showing Marchi granules in fibers Ientwing the extreme capsule (E) from the insula (I). Brain 4. Marchi stain. ,: 50. 26 Photoniicrograpli showing Xlarchi pr:inules i!i sulilenticular fascicles from the coiiiiiioii external and extreme capsules (C) coursing toivard the posterior limb of the internal

capsule (I). P; putameii: L. G.. lateral geiiiculate nucleus. Brain 4. Alarchi stain. :% 35,

27 Photomicrograph showing a11 insular lesion ivith 8dcgcneratioiifrom the insula (I) aid massive destruction of the extreiiie ('2x.C.I and the external (E.c.) capsules. P. puta- inen. Brain 5. ILIarchi stain. :.: 33. 28 Photomicrograph showing degeneratioo granule., in the lenticular fasciculus. zoiia iiicerta (Z.1.) and the nucleus of the field of' Forel (F.F) Blain 5. Marchi stain. 17.5. 29 Pliotciiiiicrograj~lislio\sing rlegeiieratioii gr'iiiiiles over tlic capsule of the lateral genicu- late nucleus (L.G.) to enter the tegiiieiitum of 11if midl~rain. I. iiiteriial cnp'ule: P. putameii. Braiii 5, Marchi stain. 17.3.

30 Pliotoiiiicrograp!i sho\viiig degeiierated fascicles coursing across thc pulviiiar ( P.) P.L.. posterior limb 01 the internal capsule. Br:iin H nI;irchi stain. 17.5.

530 CLAUSTRUM, EXTERNAL AND EXTREME CAPSTJLL OF MACAQUE PLATE 5 Joseph J. Berke

331