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Home , Corona radiata, External capsule, Extreme capsule, Habenular commissure, Internal capsule

Somatovisceral Motor Patterns in the Insu1a't2

MARY JANE C. SHOWERS3 AND EDWARD W. LAUER4 Central Nervous Sgstem Research Unit of the Kresge Medical Research, University of Michigan Medical School, Ann Arbor, Michigan

This brief study was made as a cor- acteristics of the . Ruch and ollary to previous experimental work on Patton ('46) suggested that a taste center additional motor areas of the macaque may be found in the precentral operculum monkey. The region of the island cortex and insula of chimpanzee. Sugar, Chusid is shown in figures 6A and B, as it relates and French ('48) found a second motor to the opercular areas of the matching area in macaque lying on the lateral and . Although there is not general the medial walls of the frontoparietal oper- agreement as to the homology of the in- culum and posterior part of the insula. sula (von Bonin and Bailey, '47, Frontera, Their experimental results included move- '56) of monkey with that of man, it ap- ments of the face, the and the pears that two varieties of cortex can be eyes, along with changes in respiration. distinguished in both. Von Bonin and Frontera ('55) obtained distinct move- Bailey ('47) describe agranular cortex at ments of the face and the contralateral the limen as the dominant histologic fea- upper and lower extremities when he ex- ture, although some granular cortex is plored the ventrocaudal part of the insula found in the caudal part of the insula. by use of an inductorium on monkeys an- Several authors (von Bonin and Bailey, esthetized with barbiturates and ether. '47; Kaada, Pribram and Epstein, '49 and Some of these same areas gave rise to Kaada, '51) emphasized the presence of shoulder and upper extremity movements discernible rostra1 motor cortex and cau- accompanied by shivering and salivation dal sensory cortex in the island. when Frontera ('56) repeated his previous Frontera's ('55) description of the ma- work under a somewhat different opera- caque insula will be used as reference tive procedure. here. Branches of the middle cerebral ar- Kaada, Pribram and Epstein ('49) elic- tery divide the island into a dorsorostral ited alterations in blood pressure and portion and a ventrocaudal portion without respiration from stimulation applied par- there being evidence of true gyri and sulci ticularly to the region of the limen of the (fig. 6A). The dorsorostral insula is cov- insula. Kaada ('51) extended these ob- ered by the frontoparietal operculum of servations to include the anterior sylvian the Walker ('40) areas 6, 4, and 1, and and ectosylvian gyri of cats and dogs. the ventrocaudal region by the temporal With stimulation of these gyri there were operculum of area 22 of the superior tem- such results as closing of the eyes and poral gyrus (fig. 6B). pupillary dilation, piloerection, salivation, licking, swallowing and chewing move- REVIEW OF THE LITERATURE ments, micturition and defecation. Wall Frontera ('56) described the negative results of Grunbaum and Sherrington ('03) IGrateful acknowledgment is given to the and Leyton and Sherrington ('17), who Parke-Davis Pharmaceutical Company for the investigated the island of Reil in chimpan- monkeys provided for this experimentation. %Thisstudy was financed in part by research zee, orangutan and gorilla using an induc- grants BF-7479 and B-1442 from the United torium and bipolar electrodes. However, States Public Health Service Division of Neuro- a number of experimental results can be logical Disease and Blindness. tabulated that suggest the nature of an 3 Present address: Department of Biology, Our Lady of Cincinnati College, Cincinnati 6, Ohio. additional motor area and cortical auto- * Present address: Department of Anatomy, nomic regulator in the functional char- University of Michigan, Ann Arbor, Michigan. 107 108 MARY JANE C. SHOWERS AND EDWARD W. LAUER and Davis ('51) also found changes in tion. Finally, the entire insular surface respiration and blood pressure from the was stimulated in a serial order for both region of the insula close to the orbital the dorsorostral and the ventrocaudal re- cortex. An extensive study of the results gions as shown in figure 2. Differentia- of stimulation of the insula was carried on tion of the results obtained from excitation by Hoffman ('51) and Hoffman and Ras- of the insula was made from those ob- mussen ('53). They ascertained highly tained by stimulation of the surrounding discrete changes in blood pressure, res- frontal, parietal and temporal opercular piration and gastrointestinal tone during cortices. the stimulation of the insula. Livingstone The collation of the data obtained ('55) included the insula in his review from the 6 islands is depicted in figure 2. of mechanisms and psychosomatic There appeared to be a pattern estab- function. In the work of Penfield and lished by the somatomotor effects. It was Faulk ('55) there is a resume of most possible to elicit movements of the face of the experimental work cited above and (figs. 6 G, H) by stimulation of all regions a report of the stimulation and the re- of the insula. These movements included moval of the insula of man, as observed muscular contractions of the lips, nose, over a 10-year span of time. In the last eyelids and masticatory muscles. The fa- observations, along with those of Poole cial movements tended to be homolateral ('54), sensorimotor responses, which in- and bilateral in relation to the excitation. cluded epigastric distresses, nausea and In successive order, laryngeal, neck, upper vomiting and changes in intestinal elimi- extremity (figs. 6C, D), trunk, lower ex- nation, were prominent features related to tremity (figs. 6E, F) and tail movements disorders in the insula of man. The clin- were obtained from the rostra1 to caudal ical observations were based upon cases expanse of the insula in both the dorsal of epilepsy, tumors, surgery and stimula- and the ventral aspects of the island. The tion of the and island of movements from the rostrodorsal bank of Reil. the insula tended to be bilateral and homo- lateral, while those from the caudoventral CURRENT EXPERIMENTATION bank tended to be contralateral and bi- Cortical stimulation was performed with lateral. All of these movements were gross a blunt-tipped silver wire insulated with and similar to those characterized by plastic tubing and a metal rectal plug Crosby ('56) as additional motor responses. served as the indifferent electrode. A Grass While a similarity between the dorsal stimulator (model S4B) was the source and the ventral portions of the island was of square wave pulses with a frequency evident in the somatomotor responses ob- of 40 per second, duration 1 msec., and tained, there was a difference in the vis- intensity of 7 to 10 v. The observations, ceral behavior observed upon stimulation testing, experimental procedure and mi- of the two regions. With electrical excita- croscopic technique were carried out as tion at the limen, and extending to the previously recounted in Showers ('59). caudal tip of the dorsorostral portion of In the stimulation of the three Macaca the island, there were alterations in res- mulatta monkeys, the right and the left piration, heart action, blood pressure and insular regions were explored separately, gastrointestinal tone, salivation and se- and in a composite plan as indicated in cretion of mucus (fig. 6G). During the figures lA, B, C. The limen, as it ap- stimulation and the placing of a destruc- proached the orbital cortex, was compared tive lesion, respiratory rate was slowed, with the caudal tip of the insula (figs. lA, labored, stertorous, and finally, apneic. B). The area on either side of the middle Respiratory rate changes from 52 to 30 to cerebral artery was explored as shown in 0 times per minute were accompanied by figures lB, C. The region described as increased salivation and production of mu- dorsorostral (figs. lA, B, C) was contrasted cus. Laryngeal movements and secretory with the ventrocaudal area (figs. lA, B, C) changes concomitant with respiration were in their respective responses to stimula- visualized by means of a laryngoscope. INSULAR PATTERNS 109

A 4

10 B

C Fig. 1 A, diagram of insular stimulation done on animal CLSS. B, diagram of insular stimulation done on animal CLSS. C, diagram of insular stimulation done on animal CLS4.

Cardiac rate was increased from a pre- tion of the dorsorostral insular cortex. operative 100 pulsations per minute to a Engorgement of cerebral blood vessels, in- tachycardia exceeding 200 pulsations per creased edema of the brain and bleeding minute during stimulation and destruc- in the operative field suggested a rise in 110 MARY JANE C. SHOWERS AND EDWARD W. LAUER

FACE LOWER EXTREMITY; TAIL CARDIOVASCUL4R;RESPIRATORY CHANGES GASIXOINTESnNAL CHANGES

LOWER EXTREMITY

RESPIRATORY CHANGES CARDIOVASCULAR CHANGES FACE GASfROINTEESTINAL CHANGES LOWER EXTREMITY TAl L NECK;SHOULDER, $%:$- RESPIRATORY CHANGES FACE CARDIOVASCULAR CHANGES LOW GASTROINTESTINAL CHANGES UPPE NECK SHOULDER NECK;SHOULDER;UPPEREXrREMIN LARYNX TRUNK TRUNK NECK RESPIRATORY CHANGES SHOULDER CARD1 OVASCULAR CUANGES RESPIRATORY CHANGES GASTROINTESTINAL CHANGES SECRRORY CHANGES Fig. 2 Diagram summarizes somatovisceral responses from stimulation of the insula. blood pressure at this time, also. Stimu- perspiration. The animals were sleepy for lation across the dorsorostral insula in the two to three days following the experi- region giving rise to the somatic move- ment. Sleep periods tended to alternate ment of the trunk musculature concomi- with hyperkinesia, and a lethargy was tantly produced an increase in the gastro- noticeable for 6 days in two instances. intestinal motility which could be seen All of the animals had marked oral and felt through the abdominal wall. movements without vocalization. Smack- Simultaneous with the placing of a de- ing of lips, protraction and retraction of structive lesion in this region, micturition the tongue, and sucking of the tongue and defecation to the extent of diarrhea against the palate were noticeable. These occurred. Pupillary dilation (fig. 6G) ap- movements persisted throughout the ob- peared with excitation of the dorsorostral servation period. Increased elimination insular area toward the limen, and pupil- was present in the animals, both in quan- lary constriction with the stimulus ap- titative and periodic output following the plied at the more caudal part of this strip experimentation. However, autopsy ex- of cortex. amination of the gastrointestinal mucosa In the postoperative course of observa- did not reveal any gross changes. There tion of two to 4 weeks, several features was no increase in the food and water of altered behavior were present among intake during the postoperative course. the three animals. All three animals had a marked drop in body temperature which Microscopic study averaged 1.28"C following the experi- Examination of the microscopic slides mental procedure. Piloerection occurred prepared by Swank-Davenport ('35) modifi- and was sustained for 4 weeks. Shivering cation of the Marchi technique gave equiv- was minimal, about 10 minutes, compared ocal evidence because the presence of in- to that previously observed (Showers, '58, jury to the regions of the three opercular '59). Sweat tests performed on the ani- cortices obscured the nature of degenera- mals showed a very slight increase in tion from the lesions in the insula. Com- INSULAR PATTERNS 111

parison with previous work (Showers, ward inferior temporal and hippocampal '58, '59) seems to provide additive data gyri and the basolateral part of the amyg- for the course and the relations of cer- dala. There is some transfer to the oppo- tain intercortical pathways. Frontoparietal site hemisphere by way of the anterior opercula of areas 6, 4 and 1 and orbital commissure. Degenerating fascicles in the gyrus 12 contributed fibers to the external were followed into the and extreme capsules, , su- superior and the middle temporal gyri. A perior longitudinal fasciculus and corpus diagram of these pathways is indicated callosum to distribute to adjacent frontal in figures 3A and 5. and parietal convolutions of the same and Those fibers from the degeneration of opposite sides (figs. 3A, 4, 5). Some fibers the lesion in the superior temporal gyrus, appeared to be directed into the insular area 22, were observed coursing down- cortex by the (fig. 5). ward through the inferior longitudinal fas- A few fascicles extended into the cingu- ciculus and anterior commissure to ter- lum toward the cingulate gyri (fig. 5). minate in adjacent middle and inferior An equally substantial portion of degen- temporal gyri, and amyg- erated fascicles entered capsules externa dala. There was a suggestion that such and extrema to extend downward into the fibers were directed upward into the cap- inferior longitudinal fasciculus and to- sules externa and extrema for distribution to the frontoparietal convolutions and in- External and ezrerne capsules sula. Variable degeneration appeared in the medial and the lateral septal nuclei, the , the and the . In their course to the and parolfactory area (precommissural

W A

I Pcrolfcctcry area

Fig. 3 A, diagram of frontal and parietal con- tributions to capsules externa and extrema. B, diagram of corticothalamic and corticotegmental pathways. Fig. 4 Diagram of cortico-olfactory pathways. 112 MARY JANE C. SHOWERS AND EDWARD W. LAUER septum) the cortico-olfactory fibers, with or without crossing in the corpus cal- losum, passed in part through a dorso- ventral association system (external cap- sule), then ventral and ventromedial to the lenticular nucleus to reach their desti- nation. In part they accompanied the corpus callosum fibers medialward and, with or without crossing, turned ventral- ward near the midline to enter the parol- factory area. In addition there was consistent degen- eration into the medial geniculate nuclei on both sides in proportion to the size of the lesion in the superior temporal con- volution. Mingled with corticogeniculate fibers were external corticotectal fascicles passing from the superior temporal con- volution to the sublenticular part of the and into the superior col- liculus. The terminal degeneration evident in the heads of the caudate nuclei, and trace- able from them through the subcallosal bundles and the internal capsules into the corona radiata, seemed to have been derived from the opercular lesions. Sim- FRONTOCINGULATE TRACTS * FRONXmMPORAL and PARETOTEMPORAL TRACTS 5 ilarly, there were opercular fibers which CCRTICOMALAMIC TRACTS?' had entered the internal capsule to ter- CORTICOSTRIAE TRACTS 5 minate in the and surround- Fig. 5 Diagram of cortical association and ing tegmentum of the by way commissural pathways. of the ventral peduncle of the lateral fore- brain bundle (fig. 3B), or in the cerebral the field (fig. 3B). Some fibers in the peduncle as corticobulbar, corticospinal continue into the position and corticopontine components. A large of the pallidohypothalamic tract and dis- number of fibers are transmitted through appear in the lateral hypothalamic area the internal capsule and the fibers of the and the ventromedial hypothalamic nu- comb bundle to end in the cleus. and pars reticulata of the substantianigra. In the animal CLS2 a terminal degen- The lesions which intrude upon the eration appeared in the habenular gan- island cortex are characterized by a smal- glion on the right side, at the ends of ler caliber of degeneration granules which fibers which extend ventromedial to the stream directly across the capsule externa, and mingled with the and caspule extrema into pu- fibers of the inferior thalamic peduncle to tamen and globus pallidus. It is probable that some fascicles terminate in the clau- reach stria medullaris thalami and thence strum. Most of the terminal degeneration to the . A few fibers extend is in the and the nucleus ac- through the habenular commissure to the cumbens, although some of the fascicles contralateral ganglion. In this animal the extend through the globus pallidus and lesion had injured the orbital gyms of below it as this region is traversed by the area 12 on the right side. Animal CLS3 inferior thalamic peduncle (fig. 5). These has degeneration in the thalamic fascicu- latter fibers are dissipated as the nucleus lus and , the former ventralis lateralis, and nucleus medialis ending in nucleus ventralis lateralis, the dorsalis of the dorsal appear in latter in the nucleus of the field of Forel. INSULAR PATTERNS 113

The lesion had interrupted claustrum, portions of the insula gave a duplicate pat- and the anterior commissure. tern of gross body movements. These in- cluded changes in facial expression, move- DISCUSSION ments of upper extremities, trunk, lower Neuroanatomical implications of somat- extremities and tail in that order. This ovisceral results obtained by stimulation dual pattern was parallel in orientation of the cingulate gyrus have been discussed and rostrocaudal in direction upon the in Showers ('59). There appears to be a insula. considerable similarity between the experi- 2. Visceral changes in respiration, car- mental phenomena observed Prom both the diovascular phenomena, oral secretions insula and the cingulate gyrus. In each and gastrointestinal motility were included a dual representation of the body parts in the results of excitation of the rostro- could be ascertained that was independent dorsal bank of the insula. Thus the insula of the adjacent . Increased could be termed an additional motor area strength of stimulation to each region and a cortical autonomic regulator with a blended all of the gross type of additional convulsive seizure potential. motor area movements into a generalized 3. Neuroanatomical connections de- convulsive seizure. Visceral changes could scribed in this study included short asso- be elicited from both of these cortical re- ciation pathways from frontal, parietal gions which involved a variety of adjust- and temporal opercula into the insula and ments to the environment with aspects of an efferent pathway from the insula to emotional reaction. the lentiform nucleus. The latter pathway In this study, the microscopic data sug- interposes the island as a contributor to gests that the insula is connected with the the and to the surrounding opercular cortex and orbital hypothalamic centers moderating visceral gyri by an extensive network of short asso- mechanisms. ciation bands. The discharge pathway 4. Further documentation for vertically from the insula seems to extend directly oriented association and commissural in- across the external and the extreme cap- tercortical pathways of frontal, parietal sules into the putamen and the globus and temporal cortices is presented. pallidus. It would appear that these latter pathways are then contributing afferents LITERATURE CITED to the lentiform nucleus, the efferent fi- Babkin, B. P., and J. M. Van Buren 1951 bers of which, in turn, form the pallido- Mechanism and cortical representation of the hypothalamic tracts and the ansa and the feeding pattern. Arch. Neurol. Psychiat., 66: 1-19. fasciculus lenticularis. These connections Bonin, G., and P. Bailey 1947 The Neocortex would permit the insula to be linked with of Macaca mulatta. U. of Illinois Press, Ur- the visceral controls of the bana, 163 pp. and the extrapyramidal system via the Crosby, E. C. 1956 The role of the midbrain as a part of the discharge path from higher . centers. In: Progress in Neurobiology. J. A conspicuous feature in the visceral Ariens Kappers, ed. Elsevier Publishing Co., responses of the dorsorostral portion of the Amsterdam, pp. 217-231. insula was the presence of a sequence of Frontera, J. G. 1955 Preliminary report on the results of electrical stimulation of island of oral, respiratory, and gastrointestinal Reil in the macaque. Anat. Rec., 121: 296. movements along with increased salivary 1956 Some results obtained by elec- secretion. This has been referred to in trical stimulation of the cortex of the island dogs as a feeding pattern (Babkin and of Reil in the brain of monkey. J. Comp. Neur., 105: 365-394. Van Buren, '51) and it was apparent, ante- Griinbaum, A. S. F., and C. S. Sherrington 1903 cedent to epileptic seizures, in the clinical Observations on the physiology of the cerebral study done by Penfield and Faulk in '55. cortex of the anthropoid apes. Proc. Roy. SOC. Lond., B., 72: 152-155. SUMMARY Hoffman, B. L. 1951 An experimental study of the effects of electrical stimulation of the 1. Analysis of 6 experiments on three insular cortex on blood pressure, respiration macaque monkeys is described. Stimula- and gastric motility in Macaca mulatta. Thesis, tion of the rostrodorsal and caudoventral U. of Chicago, 65 pp. 114 MARY JANE C. SHOWERS AND EDWARD W. LAUER

Hoffman, B. L., and T. Rasmussen 1953 Stim- Ruch, T. C., and H. D. Patton 1946 The rela- ulation studies of insular cortex of Macaca tion of the deep opercular cortex to taste. Fed. mulatta. J. Neurophysiol., 16: 343-351. Proc., 5: 89-90. Kaada, B. 1951 Somatomotor autonomic and Showers, M. J. 1958 Correlation of medial electrocorticographic responses to electrical thalainic nuclear activity with cortical and stimulation of rhinencephalic and other struc- tures in primates, cat and dog. Acta Physiol. subcortical neuronal arcs. J. Comp. Neur., 109: Scand., 24: (Sup. 83) 1-285. 26 1-31 6. Kaada, B., K. H. Pribram and J. Epstein 1949 1959 The cingulate gyrus: additional Respiratory and vascular responses in mon- motor area and cortical autonomic regulator. keys from temporal pole, insula, orbital surface Ibid., 112: 231-302. and cingulate gyrus. J. Neurophysiol., 12: Sugar, O., J. G. Chusid and J. D. French 1948 34 7-356. A second motor cortex in the monkey (Macaca Leyton, A. S. F., and C. S. Sherringtoii 1917 mulalta). J. Neuropath. Exp. Neur., 7: 182- Observations on the excitable cortex of the 189. chimpanzee, orangutan, and gorilla. Quart. J. Swank, R. L., and H. A. Davenport 1935 Chlor- Exp. Physiol., 11: 135-222. ate-osmic-formalin method for staining degen- Livingstone, R. B. 1955 Some brain stem erated myelin. Stain Tech., 10: 87-90. mechanisms relating to psychosomatic func- tions. Psychosomatic Med., 17: 347-354. Walker, E. 1940 A cytoarchitectural study of Penfield, W., and M. E. Faulk 1955 The in- the prefrontal area of the macaque monkey. sula, further observations on its function. J. Comp. Neur., 73: 59-86. Brain, 78: 446-470. Wall, P. D., and G. Davis 1951 Three cerebral Pool, J. L. 1954 The visceral brain of man. J. cortical systems affecting autonomic function. Nturosurg., 11: 45-63. J. Neurophysiol., 14: 507-517.

PLATE 1

EXPLANATION OF FlCUItES

6A Right hemisphere of macaque dissected to show dorsorostral and ventrocaudal portions of insula. x 0.6. 6B Left hemisphere of macaque showing cortical areas and outline of insula on opercular cortex. x 0.5. 6C Animal CLS3 before stimulation of left insula. 6D Animal CLS3 after stimulation of left insula. 6E Animal CLS4 before stimulation of right insula. 6F Animal CLS4 after stimulation of right insula. 6G Animal CLS2 after stimulation of right insula. Note secretions from mouth and nose and left pupillary dilation. 6H Animal CLS3 during stimulation of left insula showing movement of face. C, D, E, F, G, and H are enlargements of l6-mm movie film. INSULAR PATTERNS PLATE 1 Mary Jane C. Showers and Edward W. Lauer

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