Efferent Projections of the Nucleus Caudalis of the Spinal Trigeminal Complex in the Cat

Home , Inferior colliculus, Lateral lemniscus, Pars reticulata, Pretectal area, Solitary nucleus, Subthalamic nucleus

Okajimas Fol. anat. iap., 47 : 377-405, 1971

Syosuke Kawamura

The Third Department of Anatomy, Okayama University Medical School, Okayama, Japan (Director : Prof. Kahee Niimi)

Introduction

The spinal nucleus of the trigeminal nerve can be divided into the nucleus oralis, interpolaris and caudalis arranged in a rostrocaudal sequence. Contrary to the first two nuclei, the nucleus caudalis shows a laminated structure and consists of the marginal, gelatinous and magnocellular parts, which are comparable with those of the posterior gray of the spinal cord (0 1 s z e w s k i, '50). Many attempts have been made to clarify the correlation between the structural difference of the spinal trigeminal nucleus and its functional characteristics by many authors (B r o w n, '58 ; C a r- penter and Hanna, '61; Wall and Taub, '62; Stewart and King, '63; Darian-Smith and Mayday, '63; Eisenman et al., '64 ; N o r d, '67). It is now accepted that the nucleus caudalis is primarily concerned with pain and temperature sense of the face. This is of interest in view of the exclusive pain and thermal function of the similar spinal 'cord structures. Other data, with regard to the fiber connections of the subnuclei of the spinal trigeminal nucleus, are further indications of a certain functional segregation within the nucleus (T or vi k, '56 ; C a r p e n t e r andHanna,'61 ; Stewart andKing,'63 ; Dunn and Matzke, '68). Nevertheless, as yet there has been no study to analyze the fiber projections of the different parts of the nucleus caudalis. The present study is designed to fill this lack in our knowledge, by means of the N a u t a-G y g a x technique following localized losions in various parts of the nucleus caudalis in the cat.

Meterial and Methods

Ten adult cats were used in the present study. Under Nembutal anesthesia, posterior fossa craniotomy was performed, and various 377 378 Syosuke Kawamura parts of the tuber cinereum of the medulla were destroyed with a small scalpel at different levels below the obex. After survival for 7 days, the animals were killed, under deep Nembutal anesthesia, by intracarotid perfusion with normal saline followed by a solution of 10% neutral formalin. The brains and upper spinal cords were removed, fixed in 10% neutral formalin for five days, and sectioned about 10 mm thick transversely. These cut blocks of the brains and spinal cords were stored in 10% neutral formalin for one month, sectioned serially at 30-40p on the freezing microtome and impreg- nated by the N a u t a and G y g a x ('54) technique. The terminology here employed has followed most closely that of Olszew ski ('50).

Observations 1. A case with the lesion in the pars marginalis of the nucleus caudalis (cat 8). The lesion in this case lies in the pars marginalis of the nucleus caudalis and the adjacent spinal trigeminal tract at rostral levels of the pyramidal decussation. There is a slight invasion into the pars gelatinosa (Text-fig. 1). The ascending degenerated fibers from the lesion are divided

Text-fig. 1. Transverse sections showing the site and extent of lesions (cross- hatched areas) in the nucleus caudalis in cats 8, 3, 5 and 10. Efferents of Caudal Spinal Trigeminal Nucleus in Cat 379 roughly into the intranuclear ascending, the crossed medial lemniscal and the crossed reticular ascending pathways. The intranuclear ascending pathway. Although some degenerated fibers ascend through the medial part of the spinal trigeminal tract, most of the degenerated fibers are directed medialward from the lesion and ascend through the pars magnocellularis of the nucleus caudalis where many degenerated preterminals are found. Rostrally they begin to form small bundles. At caudal levels of the inferior olivary complex, some of the degenerated fibers spread medially to end in the parvocellular reticular nucleus, and a few fibers continue further medially into the intercalated nucleus. In addition, some degenerated fibers are found to pass dorsomedially into the ventrolateral part of the cuneate nucleus, but no fibers can be traced to the nucleus of the solitary tract, the dorsal nucleus of the vagus, the hypoglossal nucleus or the lateral reticular nucleus (Text-fig. 3). Reaching the nucleus interpolaris, many small fascicles of degenerated fibers ascend through this nucleus where abundant preterminals are present. The degenerated fibers spreading into the reticular formation are relatively few in number. Only a few fibers run dorsally into the inferior vestibular nucleus. In the facial nucleus occasional fibers of passage are encountered. As the nucleus oralis is reached, the small fiber bundles begin to disperse within the nucleus and are distributed to the parvocellular reticular nucleus, but they cannot be traced medially beyond the root of the abducens nerve. A few degenerated fibers are directed dorsally to terminate in the medial part of the lateral vestibular nucleus (Text-fig. 3). Further rostrally the degenerated fibers spill over heavily into the main sensory trigeminal nucleus. Some of them are directed medially just ventral to the mesencephalic root of the trigeminal nerve to terminate in the dorsal part of the pontine reticular formation. No degenerated fibers can be followed to the motor trigeminal nucleus. At these levels a few degenerated fibers extend ventrally from the main sensory nucleus into the lateral lemniscus and are distributed in the ventral part of the inferior colliculus (Text-fig. 3). The crossed medial lemniscal pathway. This pathway, running ventromedially from the lesion, crosses the midline among the fiber bundles of the pyramidal decussation and then runs rostrally along the lateral edge of the uncrossed pyramidal tract . At inferior olivary levels the degenerated fibers are situated medial, ventral and ventrolateral to the inferior olivary complex, but do not enter there . At these levels a few degenerated fibers are seen to cross the midline to join the medial lemniscal pathway . Proceeding rostrally, the degenerated fibers of this pathway migrate laterally within the 380 Syosuke Kawamura

Text-fig. 2. Lesions in cats 1, 4, 6 and 7. For notes see Text-fig. 1. medial lemniscus. As the nucleus of the facial nerve appears, most of the degenerated fibers are concentrated in the region between the pyramid and the ventral spinocerebellar tract (Text-fig. 3). At levels of the trapezoid body the degenerated fibers ascend through the medial lemniscus between the root of the abducens nerve and the medial superior olivary nucleus. In the lower pons they are found mostly in the lateral portion of the medial lemniscus and partly in the lateral lemniscus. In more rostra! sections some of the fibers are seen to enter the ventral part of the inferior colliculus, but the majority ascend through the most lateral part of the medial lemniscus. At superior collicular levels a fair number of degenerated fibers leave the medial lemniscus in the dorsomedial direction to distribute in the superior colliculus, particularly in the stratum griseum intermedium. In addition, some fibers pass medially through the reticular formation to terminate in the lateral part of the central gray (Text-fig. 3). At the most rostral level of the superior colliculus, the degenerated fibers are crowded irregularly in the region among the red nucleus, the substantia nigra, the medial geniculate body and the central gray. A considerable number of degenerated fibers run laterally into the magnocellular part of the medial geniculate Efferents of Caudal Spinal Trigeminal Nucleus in Cat 381

Text-fig. 3. Drawings of transverse sections (unequal intervals) through the medulla oblongata, pons and mesencephalon of cat 8. In this and subsequent figures, degenerated fibeys of passage are indicated by coarse dots and preterminal degeneration by fine stipples. body, particularly its ventromedial portion (Text-fig. 4). In the posterior region of the thalamus, most of the degenerated fibers are found in the ventral part of the posteromedial ventral nucleus. Rostrally they divide into medial and lateral groups of fibers. The medial group consists of fine fibers crowded in the medial part of the posteromedial ventral nucleus, whereas the lateral group is composed of a small number of coarse fibers scattered in the lateral part of this nucleus. These two groups of fibers decrease in number rostrally and disappear at the level a little rostral to the middle of the posteromedial ventral nucleus. No degenerated fibers are seen in the other thalamic nuclei (Text-fig. 4). Other projection fibers. Besides the above two main pathways, the crossed reticular ascending pathway can be distinguished, though 382 Syosuke Kawamura

Text-fig. 4. Drawings of transverse sections through the diencephalonof cat 8.

it is small in amount in this case. Fibers of this pathway run ventromedially from the lesion together with those of the crossed medial lemniscal pathway to cross the midline among the fiber bundles of the pyramidal decussation. After crossing the midline, they diverge from the crossed medial lemniscal pathway to pass dorsolaterally and ascend through the reticular formation ventrolateral to the hypoglossal nucleus. Some of them are distributed to the adjacent portion of the reticular formation, a few to the nucleus interpolaris, and others to the nucleus reticularis pontis caudalis medial to the root of the facial nerve (Text-fig. 3). Moreover, some degenerated fibers are seen to run medially from the lesion and cross the midline dorsal to the central canal. A few of them enter the contralateral gracile nucleus, but the majority course laterally just dorsal to the nucleus of the solitary tract and terminate in the pars magnocellularis of the contralateral nucleus caudalis (Text-fig. 3). 2. Cases having relatively localized lesions in the nucleus caudalis without involvement of the adjacent reticular formation (cats 3, 5 and 10). The lesions in cats 5 and 10 involve the nucleus caudalis and the spinal trigeminal tract at middle and rostral levels of the pyramidal decussation. In cat 3 the lesion extends from the middle level of the iyramidal decussation to the most caudal level of the inferior olivary complex. The caudal part of the lesion is confined to the nucleus caudalis and the spinal trigeminal tract, while the Efferents of Caudal Spinal Trigeminal Nucleus in Cat 383 rostral part involves the cuneate fasiculus and slightly the adjacent reticular formation. In all of these cases, the lesions involve the pars marginalis, pars gelationosa and pars magnocellularis of the nucleus caudalis (Text-fig. 1). The ascending fibers from the nucleus caudalis are divided into the intranuclear ascending, the uncrossed reticular ascending, the crossed medial lemniscal and the crossed reticular ascending pathways. The intranuclear ascending pathway. The degenerated fibers of this pathway ascend, in small fascicles, largely through the magnocellular part of the nucleus caudalis and the parvocellular reticular nucleus. Some fibers, however, ascend through the medial part of the spinal trigeminal tract. In cat 3 the preterminal degeneration is found in the lateral cuneate, cuneate and gracile nuclei at middle levels of the inferior olivary complex. This may result from the lesion involving the cuneate fasciculus. In cats 5 and 10 where the posterior funiculus is spared, however, some degenerated fibers are

Text- 5. Drawings of transverse sections through the brain stem in cat 10 . 384 Syosuke Kawamura

also seen to enter the cuneate nucleus, but no degeneration can be seen in the lateral cuneate nucleus. In all of these cases some degenerated fibers are found in the dorsal part of the lateral reticular nucleus. Further course and termination of the intranuclear ascending fibers are essentially the same as those in cat 8, but their amount is larger (Text-fig. 5). The uncrossed reticular ascending pathway. Fibers of this pathway run rostromedially from the lesion to distribute in the nucleus reticularis ventralis at caudal levels of the medulla. As they ascend through the lateral reticular formation, they tend to form small bundles and spread extensively in the lateral and medial portions of the reticular formation at levels of the inferior olivary complex (Text-fig. 5). A few fibers enter the medial part of the dorsal accessory olive. In cat 3 occasional fibers are found to reach the ventral part of the nucleus of the hypoglossal nerve. The degenerated fibers, in small bundles, continue largely rostralward, though some fibers terminate in the gigantocellular reticular nucleus. Approaching the facial nucleus, a considerable number of degenerated fibers pass ventrally to terminate in the medial part of the facial nucleus, while some fibers run dorsally, into the medial vestibular nucleus. Proceeding rostrally, the degenerated fibers, rapidly decreasing in number, pass along the central tegmental fasciculus and terminate in the reticular formation dorsal to the red nucleus at superior collicular levels (Text-fig. 5). The crossed medial lemniscal pathway. As in cat 8, fibers of this pathway cross the midline mainly among fiber bundles of the pyramidal decussation and ascend just lateral and dorsal to the inferior olivary complex. In cat 3 a few degenerated fibers are found to terminate in the medial portion of the dorsal accessory olive. Proceeding rostrally, the degenerated fibers enter the medial lemniscus. At caudal levels of the facial nucleus, some degenerated fibers are directed medially to enter the nucleus of the raphe. A few of them cross through this nucleus and just dorsal to it. Such recrossing is conspicuous in cats 3 and 10, but is not observed in cat 5. At these levels some degenerated fibers leave the medial lemniscus in the dorsal direction to distribute in the ventral portion of the gigantocellular reticular nucleus. (Text-fig. 5). At levels of the superior olivary nucleus, although the degenerated fibers ascend largely through the medial lemniscus, a considerable number of degenerated fibers are also found in the medial trapezoid nucleus and dorsal to the medial superior olivary nucleus. Most of them are regarded as fibers of passage, but a few appear to terminate in the medial trapezoid nucleus. Passing rostrally, the Efferents of Caudal Spinal Trigeminal Nucleus in Cat 385 legenerated fibers gradually shift laterally in the medial lemniscus, a.nd scarcely any fibers can be observed in the medial half of the medial lemniscus at middle pontine levels. In cat 3, however, some fibers are also found in the medial portion of the medial lemniscus and a few of them run ventrally into the medial pontine nucleus. At inferior collicular levels the degenerated fibers are found largely in the region extending from the most dorsolateral portion of the medial lemniscus to the lateral lemniscus. Some of them enter the ventrolateral part of the inferior colliculus (Text-fig. 5). On approaching the superior colliculus, the degenerated fibers in the most dorsolateral portion of the medial lemniscus proceed dorsomedially just medial to the brachium of the inferior colliculus to enter the superior colliculus, where they are distributed mostly in the stratum opticum and stratum griseum intermedium and cover almost the entire cross sectional areas of these layers. Proceeding rostrally, they decrease in number, and scarcely any fibers can be found in the rostral third of the superior colliculus (Text-fig. 5). In addition, a few degenerated fibers leave the medial lemniscus in a medial direction to reach the central gray. Such fibers in cat 3 out- number those in cats 5 and 10. At posterior commissural levels the degenerated fibers are found in the region among the red nucleus, the substantia nigra and the medial geniculate body. They are concentrated in the region just ventromedial to the medial geniculate body, with some fibers passing into its magnocellular part. A few degenerated fibers run dorsally to distribute in the pretectal area, and extremely few fibers are directed dorsomedially to join the fibers of the posterior commissure and recross there (Text-fig. 6). In cat 3 a small number of degenerated fibers enter the red nucleus and the medially adjacent portion of the reticular formation. It is, however, difficult to determine whether they terminate in the red nucleus. In addition, a considerable number of degenerated fibers are seen in the zona incerta and the field of Fore 1. In cat 10 a. few such fibers extend ventrally into the subthalamic nucleus (Text-fig. 6). At caudal levels of the thalamus the degenerated fibers enter the most posterior part of the posteromedial ventral nucleus and begin to divide into medial and lateral groups. Fibers of the medial group are distributed in the dorsomedial part of the posteromedial ventral nucleus, the parafascicular nucleus and the centre median nucleus. Some of the degenerated fibers in the parafascicular nucleus proceed medially to recross through the most caudal part of th€ massa intermedia to enter the parafascicular and centre median nuclei on the side ipsilateral to the lesion. In more rostral section 386 Syosuke Kawamura

Text-fig. 6. Drawings of transverse sections through the diencephalon in cat 10.

degenerated fibers are distributed to the paracentral and lateral central nuclei of the opposite side (Text-fig. 6). In the medial central nucleus occasional fine degenerated beads are found, in addition to the coarser fibers of passage to the contralateral side, but their exact termination cannot be determined. A small number of fibers are also found in the most ventral part of the dorsomedial nucleus, but most if not all of them appear to be fibers of passage. Further rostrally, fibers of the medial group, decreasing in number, become restricted mainly to the paracentral nucleus. Scarcely any fibers are seen at levels rostral to the lateral . geniculate body. Fibers of the medial group in cat 3 disappear at more caudal levels than those in cats 5 and 10. Fibers of the lateral group proceed rostrally through the ventrolateral part of the posteromedial ventral nucleus, where some fibers terminate. During their rostral course they gradually shift dorsolaterally to lie in the lateralmost part of the posteromedial ventral nucleus. Rostrally they decrease in number and disappear at about the middle levels of the posteromedial ventral nucleus. In cat 3 fibers of the lateral group are more abundant than those in cats 5 and 10, particularly in the dorsolateral part of the posteromedial ventral nucleus. A small number of them enter the medial part of the posterolateral ventral nucleus at middle levels of the lateral geniculate body. Most of the degenerated fibers are still found in the posteromedial ventral nucleus at levels where fibers of the medial Efferents of Caudal Spinal Trigeminal Nucleus in Cat 387 group disappear, and pass further rostrally through it to end in the ventral part of the lateral ventral nucleus. During their course a small number of degenerated fibers pass ventrolaterally into the ventral part of the thalamic reticular nucleus at the most caudal level of the optic chiasm. The crossed reticular ascending pathway. Fibers of this pathway run medially from the lesion to cross the midline among fiber bundles of the pyramidal decussation and spread widely in the paramedian reticular nucleus of the opposite side. At levels of the inferior olivary complex the degenerated fibers, forming a number of small bundles, are crowded around the root of the hypoglossal nerve and ascend through the gigantocellular reticular nucleus, where some fibers are seen to terminate (Text-fig. 5). As the nucleus of the facial nerve appears, a number of degenerated fibers run ventrally into the medial part of the facial nucleus, and some fibers are directed dorsally to enter the medial vestibular nucleus. At levels of the trapezoid body, although some fibers pass laterally into the nucleus oralis, most of the degenerated fibers are seen to accumulate ventral and ventrolateral to the genu of the facial nerve and ascend mainly along the central reticular fasciculus. At superior collicular levels some fibers run dorsomedially to enter the ventral part of the central gray of the midbrain, but the majority pass further rostrally and end in the reticular forination dorsal to the red nucleus (Text-fig. 5). No fibers can be followed as far as the thalamus. 3. Cases with lesions in the nucleus caudalis and the adjacent reticular formation (cats 1, 4, 6 and 7). In every case the lesion involves the pars marginalis, pars gelatinosa and pars' magnocellularis of the nucleus caudalis. In cats 1 and 7 the lesions are situated in the dorsomedial part of the nucleus caudalis and the medially adjacent reticular formation. The lesion in cat 7 is rather small and lies at the most caudal levels of the pyramidal decussation. In cat 1, however, the lesion is fairly extensive and extends throughout the entire levels of the pyramidal decussation. Its rostral portion involves the cuneate fasciculus and the lateral part of the cuneate nucleus. This results in degeneration of the internal arcuate fibers. In cats 4 and 6 lesions are found in the ventrolateral part of the nucleus caudalis and the ventromedially adjacent reticular formation. The lesion in cat 4 lies at levels of the caudal half of the pyramidal decussation, and the lesion in cat 6 extends from the rostral level of the pyramidal decussation to the obex, involving the dorsal spinocerebellar tract (Text-fig. 2). The ascending degenerated fibers in these cases are divided into 388 Syosuke Kawamura the intranuclear ascending, the uncrossed reticular ascending, the crossed medial lemniscal, the crossed reticular ascending and the uncrossed medial lemniscal pathways. The intranuclear ascending pathway. The course and termination of this pathway are essentially similar to those in eases with lesions confined to the nucleus caudalis. In cat 7 the degenerated fibers, mostly in bundles, ascend in the dorsomedial part of the nucleus caudalis, but not in the ventrolateral part. At levels rostra! to the middle of the nucleus interpolaris, however, they spread in the whole area of this nucleus, including its ventrolateral part (Text-fig. 7). In cat 6 some degenerated fibers pass through the main sensory trigeminal nucleus to reach the mesencephalic trigeminal nucleus. In addition, degenerated fibers are found to pass medially from the lesion. Some of them terminate in the nucleus of the solitary tract ; other fibers cross through the posterior commissure of the medulla and run into the opposite gracile nucleus and further laterally into the pars magnocellularis of the nucleus caudalis (Text-fig. 7).

Text-fig. 7. Drawings of transverse sections through the brain stem in cat 7. Efferents of Caudal Spinal Trigeminal Nuclues in Cat 389

In cat 6 a large number of degenerated fibers are found to enter the cerebellum through the inferior cerebellar peduncle. This may be due to the involvement of the dorsal spinocerebellar tract in the lesion. The uncrossed reticular ascending pathway. This pathway shows almost the same distribution as in cats 3, 5 and 10, except that a considerable number of fibers run dorsomedially into the ventral part of the central gray at superior collicular levels. The crossed medial lemniscal pathway. Many degenerated fibers from the lesion proceed ventromedially to cross the midline among the fiber bundles of the pyramidal decussation and surround the inferior olivary complex of the opposite side. No degenerated fibers are seen in the main olivary nucleus. In cats 7 and 1, however, degenerated preterminals are found in the medial part of the dorsal accessory olive (Text-fig. 7). Proceeding rostrally, the degenerated fibers within the medial lemniscus gradually shifts laterally. At the level Of the caudal end of the facial nucleus some degenerated fibers leave the medial lemniscus to pass medially into the nucleus of the raphe, and a few of them recross the midline. In addition, only a few fibers lying just dorsolateral to the medial lemniscus reach the ventromedial part of the facial nucleus. At lower pontine levels some of the degenerated fibers in the medial part of the medial lemniscus run ventrally into the medial pontine nucleus and dorsally into the tegmental reticular nucleus of the pons, as in cat 3. In cat 7 some fibers leave the medial lemniscus in the ventrolateral direction and end in the lateral pontine nucleus (Text-fig. 7). At more rostra:I levels the degenerated fibers in the medial lemniscus shift more laterally and ascend largely in the lateral part of the medial lemniscus and partly in the lateral lemniscus. As the inferior colliculus appears, some of the degenerated fibers in the lateral lemniscus run dorsally into the ventral part of the inferior colliculus. At caudal levels of the superior colliculus a few degenerated fibers can be traced to the lateral portion of the pars reticulata of the substantia nigra in cats 1 and 7. Further rostrally, a considerable number of fibers begin to leave the main mass of the degenerated fibers in the medial and dorsomedial directions. The medially directed fibers pass through the reticular formation into the central gray. The dorsomedially running fibers enter the superior colliculus, where most of them terminate in the stratum opticum and the stratum griseum intermedium, but a few fibers run medially to recross through the commissure 390 Syosuke Kawamura

Text-fig. 8. Drawings of transverse sections through the diencephalon in cat 7. of the superior colliculus. At posterior commissural levels most of the degenerated fibers are found medial to the medial geniculate body, and some of them run laterally into its magnocellular part (Text-fig. 8), In the caudal thalamus, the degenerated fibers begin to divide into medial and lateral groups. Fibers of the medial group are distributed to the medial part of the posteromedial ventral nucleus, the parafascicular nucleus and the centre median nucleus. Some fibers recross the midline through the massa intermedia to enter the parafascicular and centre median nuclei on the side ipsilateral to the lesion. Such fibers are more abundant than those in cats 3, 5 and 10. At middle levels of the lateral geniculate body, fibers of the medial group end in the medial half of the posteromedial ventral nucleus, the lateral central nucleus and the paracentral nucleus. The degenerated fibers in the posteromedial ventral nucleus disappear at levels just rostral to the lateral geniculate body, while those in the intralaminar nuclei continue somewhat more rostrally (Text-fig. 8). In addition, a number of degenerated fibers are seen in the field of Fore I. In cat 7 some such fibers reach the subthalamic nucleus. Fibers of the lateral group are distributed mostly to the lateral part of the posteromedial ventral nucleus and partly to the medial part of the posterolateral ventral nucleus, and rostrally they shift Efferents of Caudal Spinal Trigeminal Nucleus in Cat 391 somewhat laterally (Text-fig. 8). In cat 6 degenerated fibers are seen in the lateral part of the posteromedial ventral nucleus, almost all of the posterolateral ventral nucleus and the ventral part of the suprageniculate nucleus. Some of them can be traced further rostrally to the ventral extremity of the lateral ventral nucleus, with a few fibers passing into the reticular nucleus. The crossed reticular ascending pathway. This pathway is essentially similar to that of cats 3, 5 and 10. In cat 6 degenerated preterminals are abundant in the nuclei interpolaris and oralis and the main sensory trigeminal nucleus on the side contralateral to the lesion. The uncrossed medial lemniscal pathway. This can be clearly distinguished from the other pathways, though it cannot be identified in cases with the lesions confined to the nucleus caudalis. Its fibers course ventromedially from the lesion and are crowded around the inferior olivary complex without crossing the midline and ascend through the lateral part of the medial lemniscus of the same side. They assume a course similar to the crossed medial lemniscal pathway, but do not terminate in the pontine nuclei and the substantia nigra. Within the posterior part of the thalamus the uncrossed medial lemniscal pathway divides into medial and lateral groups of fibers and disappear more caudally than those of the crossed pathway. Fibers of the medial group are scattered mainly in the parafascicular and andcentre median nuclei. These fibers are, at least in part, considered to come from the opposite side through the massa intermedia. Scarcely any fibers are found in the most caudal part of the posteromedial ventral nucleus. Proceeding rostrally, however, fibers of the medial group spread somewhat ventrally to reach the dorsomedial part of the posteromedial ventral nucleus and the paracentral nucleus (Text-fig. 8). In cat 4 the degenerated fibers are localized only in the parafascicular and centre median nuclei. In cat 6, however, the degenerated fibers extend rostrally as far as the caudal level of the optic chiasm ; they terminate in the lateral central and paracentral nuclei and the adjacent part of the posteromedial ventral nucleus. Fibers of the lateral group pass rostrolaterally through the ventral part of the posteromedial ventral nucleus, and are distributed in the ventrolateral part of the posterolateral ventral nucleus and the adjacent magnocellular part of the medial geniculate nucleus , with some fibers proceeding rostrally through the posteromedial ventral nucleus. In eats 4 and 7 the degenerated fibers are confined to the ventral Dart of the nosterolateral ventral nucleus At lAvAlq nf 392 Syosuke Kawamura the optic chiasm and soon disappear (Text-fig. 8). In cat 6 fibers of the lateral group further divide into dorsal and ventral fibers which are distributed in the ventral part of the lateral ventral nucleus and the posterolateral ventral nucleus, respectively.

Discussion The intranuclear ascending pathway. Early studies have shown that fibers arising in the nucleus caudalis of the spinal trigeminal nucleus ascend through the sensory trigeminal nuclei and the adjacent portion of the spinal trigeminal tract. This has been confirmed by recent experimental studies (Carpenter and Hanna,'61 ;StewartandKing,'n ;Dunn and Matzke, '68; Mogami et al., '68). Stewart and King suggested that the intranuclear ascending pathway originating in the nucleus caudalis distributes preterminals to all levels of the trigeminal nuclear complex in the medulla and pons and to other brain stem nuclei. According to Dunn and M a t z k e, the intranuclear ascending pathway can be divided into long ascending and short internuncial fibers. The latter fibers are confined to fascicles of fibers projecting through the subnucleus gelatinosus of the nucleus caudalis, while the former form an ascending system of fibers located ventromedial to the descending trigeminal tract. The present results confirm the existence of the intranuclear ascending fibers arising in the nucleus caudalis. In most of the present experiments these fibers pass rostrally through the spinal trigeminal nucleus and the adjacent portions of the spinal trigeminal tract and the reticular formation. In cat 8 with the lesion confined to the marginal part, however, the degenerated fibers ascend mainly through the spinal trigeminal nucleus and the adjacent spinal tract, and slightly through the dorsolateral reticular formation. Therefore, the intranuclear ascending fibers running rostrally through the reticular formation are considered to originate largely from the other parts of the nucleus caudalis, particularly the pars magnocellularis. In their course most of the intranuclear ascending fibers, forming many small fascicles, are distributed within the sensory trigeminal nuclear complex and the adjacent reticular formation, but some fibers enter the cuneate nucleus, the nucleus intercalatus and the vestibular nuclei. M o g a m i et al. ('68) found degeneration in the cuneate nucleus and the nucleus intercalatus following lesions of the nucleus caudalis. S e k i n o ('62) also described trigeminal fibers to the nucleus intercalatus. S t e w a r t and K i n g ('63) stated that some fibers of the intra- Efferents of Caudal Spinal Trigeminal Nucleus in Cat 393

nuclear ascending pathway enter the central gray and the tectum of the ipsilateral midbrain by way of the mesencephalic tract of the trigeminal nerve. In the present experiments, however, a few fibers pass into the ventral part of the inferior colliculus by way of the lateral lemniscus. No fibers can be traced to the superior colliculus via the intranuclear ascending pathway. The reticular ascending pathways. Since W allenb erg (1896) described the dorsal trigemino- - thalamic tract in the rabbit , there has been much discussion concerning the extralemniscal pathway from the spinal trigeminal nucleus. According to K u r u ('49), the dorsal trigemino-thalamic tract (tractus quinto-thalamicus reticularis) originates from the spinal trigeminal nucleus in man. Russell ('54), however, stated that no dorsal trigemino-thalamic tract exists in the cat, and those fibers previously described as forming such a tract are actually fibers of the lateral reticulo-thalamic pathway. N a u t a and K u y- p e r s ('58) also denied the existence of the dorsal tract from the spinal trigeminal nucleus. The trigemino-reticular fibers from the spinal trigeminal nucleus have been demonstrated by many authors (N a u t a and K u y p e r s, '58 Ste w art and K i n g , '63). The present observations confirm the existence of bilateral reticular ascending fibers from the nucleus caudalis. The course and amount of the degeneration of these pathways vary with the site and extent of the lesion within the nucleus caudalis. In the case with the lesion limited to the marginal part, only a few crossed reticular ascending fibers are found, though abundant reticular ascending fibers are present bilaterally in cases with lesions extending to all layers of the nucleus caudalis. This may indicate that the main source of the reticular ascending pathways is the magnocellular and gelatinous parts, particularly the former. Following lesions of the nuclei oralis and interpolaris in the cat, Carpenter and Hanna ('61) found degeneration in the dorsolateral reticular area near the ipsilateral spinal trigeminal nucleus, and the contralateral paramedian and gigantocellular reticular nuclei. On the other hand, Stewart and King ('63) stated that the contralateral gigantocellular nucleus is essentially devoid of degenerated fiber elements, while the most profuse degeneration above the level of the lesion appears in the parvocellular nucleus adjacent to the ipsilateral nucleus interpolaris. The present study reveals that the nucleus caudalis projects fibers extensively to the brain stem reticular formation mostly by way of the reticular ascending and the intranuclear ascending pathways, and partly via 394 Syosuke Kawamura the medial lemniscal pathway. Most of the fibers to the ipsilateral parvocellular reticular nucleus just medial to the nuclei caudalis and interpolaris appear to come through the intranuclear ascending pathway. However, a considerable number of fibers entering the paramedian and gigantocellular reticular nuclei are regarded as coming by way of the crossed and uncrossed reticular ascending pathways. The facial nucleus has been said to receive fibers from the nucleus caudalis on both sides, more intensively on the contralateral side (Stewart and King, '61 ; Sekino, '82; Mogami et al., '68; Dunn and Mat z k e, '68). The present study also indicates that the nucleus caudalis sends fibers to the facial nucleus bilaterally by way of the crossed and uncrossed reticular ascending pathways and the crossed medial lemniscal pathway. Since scarcely aty degeneration is found in the facial nucleus in the case with the lesion confined to the marginal part (cat 8), the facial nucleus is considered to receive fibers from the other parts of the nucleus caudalis, particularly the magnocellular part. Many authors found degeneration in the motor trigeminal nucleus after lesions in the nucleus caudalis (S tewart and K i n g, '61 ; Dunn and Matz k e, '68) and in the nuclei oralis and interpolaris (C a r p e n t e r and Hann a, '61). In the present experiments, however, no degeration is observed in the motor trigeminal nucleus following lesions of the nucleus caudalis. Ste w art and King denied the existence of the fibers from the nucleus caudalis to the mesencephalic trigeminal nucleus. The present study also supports this view. The present results indicate that the nucleus caudalis sends fibers to the vestibular nuclei by way of the uncrossed reticular ascending as well as the intranuclear ascending pathway. Dunn and Matzke ('68) described a few degenerated fibers passing medially from the intranuclear pathway to the vestibular complex. Many authors described the fibers from the nucleus caudalis to the hypoglossal nucleus (S t e wart and K i ii g, '61 ; S e k i n o, '62 ; M o g a mi et al., '68). Moreover, Stewart and King demonstrated that the trigeminal fibers extend into the dorsal nucleus of the vagus. According to the present observations, however, the nucleus caudalis sends no fibers to the hypoglossal nucleus or the dorsal nucleus of the vagus. Mogami et al. traced fibers from the nucleus caudalis to the ipsilateral nucleus of the solitary tract. The present study indicates that a few degenerated fibers are encountered in the solitary nucleus on the ipsilateral side in cases with lesions limited to the nucleus caudalis, but they appear to be fibers of passage. In cases involv- Efferents of Caudal Spinal Trigeminal Nucleus in Cat 395 ing the reticular formation, however, some degenerated fibers are found to terminate in the solitary nucleus. Since in all the cases examined the spinal trigeminal tract is involved more or less in the lesion, a possibility exists that preterminal degeneration in the solitary nucleus results from damage to the primary afferent fibers of the trigeminal nerve. According to K err ('61), the primary trigeminal fibers terminate in the upper one-third of the nucleus. In the present experiments, however, degeneration is found in the lower part of the solitary nucleus. Therefore, it is likely that the degeneration in the solitary nucleus is considered to result from the lesion involving the reticular formation. Stewart and King ('61) found degenerated fibers terminating in the dorsal cap and dorsal lateral margin of the ipsilateral medial accessory olivary nucleus following lesions of the nucleus caudalis. According to the present observations, however, preterminal degeneration is found in the medial part of the ipsilateral dorsal accessory olivary nucleus in cases having lesions of the nucleus caudalis with or without involvement of the reticular formation. In cats 3, 7 and 1 where the dorsal funiculus is more or less involved in the lesion, degeneration is present in the contralateral dorsal accessory olive. This may result from the dorsal funiculus, but not from the nucleus caudalis. There has been much discussion concerning the trigemino- cerebellar connections. Carpenter and Hanna ('61) affirmed the existence of direct fibers from the nuclei oralis and interpolaris to the cerebellum in the cat. Dunn and Matzke ('68) also traced some fibers from the nucleus caudalis to the cerebellum in the marmoset. Stewart and King ('63), however, failed to find degeneration in the cerebellum following lesions of the nucleus caudalis in the cat. In agreement with the last authors, the present study cannot demonstrate the direct cerebellar projection of the nucleus caudalis, and supports their assumption that the trigemino- olivary and trigemino-reticular fibers originating in the nucleus caudalis may be the primary axons of trigemino-olivo-cerebellar and trigemino-reticulo-cerebellar tracts. The medial lemniscal pathways. Earlier authors described the exclusively contralateral thalamic projection of the spinal trigeminal nucleus by way of the medial lemniscus (Walker, '39; Magoun and Kinley, '42; Russell, '54) . Most of the recent experimental studies with silver methods, however, revealed that the trigemino-thalamic fibers are distributed bilaterally with contralateral predominance (N a u t a and K u y per s, '58; Stewart and King , '63; Dunn and Matzke, '68). Ste- 396 Syosuke Kawamura wart and King reported that the nucleus caudalis gives rise to bilateral ascending fiber projections to the midbrain and thalamus through the lemniscal pathways as well as through the reticular formation. Carpenter and Hanna ('61), by contrast, described the degeneration of contralateral medial lemniscus following lesions of the oral and interpolar nuclei. The present results also indicate that in cases with lesions confined to the nucleus caudalis fiber degeneration is found in the contralateral medial lemniscus only, whereas degeneration can be traced rostralward through the medial lemniscus of both sides in cases with lesions of the nucleus caudalis involving the reticular formation. As to the trigeminal component of the medial lemniscus at pontine and midbrain levels, the present observations accord well with the results of earlier authors that the fibers from the spinal trigeminal nucleus ascend through the dorsolateral portion of the medial lemniscus and are distributed to the inferior and superior colliculi and the magnocellular part of the medial geniculate nucleus (Nauta and Kuypers, '58; Stewart and King, '63; Dunn and Matzke, '68). The trigemino-thalamic tract has been thought to terminate in the posterior ventral nucleus of the thalamus. According to C a r- pent e r and Hanna ('61), the fibers from the oral and interpolar nuclei project in a very discrete manner into the posteromedial ventral nucleus, but no fibers are observed to enter the intralaminar nuclei. Ste wart and King ('63), however, found degeneration in the intralaminar nuclei as well as in the posteromedial ventral nucleus after lesions in the nucleus caudalis. Recent electrophysio- logical studies have also supported these anatomical data (S t e w art et al., '64 ; S h e n d e et al., '68). The present study reveals that the crossed medial lemniscal pathway from the nucleus caudalis enters the posterior part of the posteromedial ventral nucleus and divides into medial and lateral groups of fibers. The former fibers are distributed to the dorsomedial part of the posteromedial ventral nucleus, and the parafascicular, centre median, paracentral and lateral central nuclei. Fibers of the lateral group enter the ventrolateral and lateral part of the posteromedial ventral nucleus. Some fibers in the parafascicular nucleus recross through the massa intermedia to enter the parafascicular and centre median nuclei on the side ipsilateral to the lesion. Such a recrossing was suggested by Mog am i et al. ('68). Of three ,subdivisions of the spinal trigeminal nucleus, the nucleus caudalis is considered to be the only nucleus to send fibers to the intralaminar nuclei. According to the present results, the Efferents of Caudal Spinal Trigeminal Nucleus in Cat 397 intensity of the degeneration in the intralaminar nuclei varies with the site of lesions within the nucleus caudalis in the rostrocaudal dimension. In cases with lesions in the caudal part of the nucleus caudalis (cats 7 and 4) the degenerated fibers in the intralaminar nuclei are more numerous and extend more rostrally than those in cases with rostral lesions (cats 6 and 3). Moreover, the projections of the nucleus caudalis to the posteromedial ventral nucleus appear to be organized in the rostrocaudal direction. Fibers from the rostral part of the nucleus caudalis are distributed more abundantly and extend more rostrally in the posteromedial ventral nucleus than those from the caudal part of the nucleus caudalis. The nucleus caudalis is composed of three parts arranged in layers : marginal, gelatinous and magnocellular. K u r u ('49) suggested that each of these parts sends separate fibers for different modalities of cutaneous sensation. According to his results, the marginal part is concerned exclusively with the pain and temperature sense and gives rise to the tractus quinto-thalamicus paralemniscalis. M o g- a m i et al. ('68) stated that the degeneration of paralemiscal quinto- thalamic fibers is observed following lesions of the marginal part in the cat. The present study reveals that in the case with lesion confined to the. marginal part degeneration is found in the crossed medial lemniscal pathway corresponding to the paralemniscal tract, although hardly any degeneration is observed in the reticular ascending pathways, particularly the uncrossed. In this case thalamic degeneration is present only in the posteromedial ventral nucleus, but no degeneration is observed in the intralaminar nuclei. In the posteromedial ventral nucleus degenerated fibers are found mostly in the medial part, and a few fibers in the lateral part. In cases involving each layer of the nucleus caudalis, however, the degenerated fibers in the posteromedial ventral nucleus are seen largely in its lateral part and a smaller number in the medial part, though marked degeneration is found in the intralaminar nuclei. M o g am i et al., by contrast, stated that fibers from the marginal part terminate in the more lateral and caudal part of the posteromedial ventral nucleus than those in cases with lesions extending to other layers of the nucleus caudalis. N a u t a and K u y p e r s ('58) traced degenerated fibers from the spinal trigeminal nucleus to the subthalamic nucleus. In the present experiments degeneration is found in the field of F ore 1, the zona incerta and the subthalamic nucleus following lesions of the nucleus caudalis with or without involvement of the adjacent reticular formation. However, the degenerated fibers in these subthalamic centers are much more abundant in cases with lesions extending 398 Syosuke Kawamura into the reticular formation. Therefore, it may be said that the degenerated fibers are, largely if not exclusively, attributed to the involvement of the reticular formation in the lesion. K u r u ('49) divided the secondary fibers from the sensory trigeminal nuclear complex into the tractus quinto-thalamicus reticularis, lemniscalis and paralemniscalis in man. Roughly speaking, the first corresponds to the reticular ascending pathways, and the second is comparable to the medial lemniscal pathway of the present paper in the cat. However, it is uncertain whether the last tract is to be included in the medial lemniscal or in the reticular ascending pathways.

Summary

Efferent projections of the nucleus caudalis of the spinal trigeminal complex of the cat were studied by the N a u t a-G y g a x technique. The efferent fibers from the nucleus caudalis are divided into the intranuclear ascending, the medial lemniscal and the reticular ascending pathways. The intranuclear ascending pathway ascends through the sensory trigeminal nuclear complex and the adjacent portions of the spinal trigeminal tract and the reticular formation. The marginal part of the nucleus caudalis contributes much fewer fibers to the fiber path ascending through the reticular formation adjacent to the spinal trigeminal nucleus than the other parts of the nucleus caudalis. The intranuclear ascending pathway gives off fibers mostly to the spinal trigeminal and main sensory nuclei and partly to the cuneate nucleus, the nucleus intercalatus, the vestibular nuclei, the dorsolateral reticular formation and the ventral part of the inferior colliculus. Through the crossed and uncrossed reticular ascending pathways, the nucleus caudalis is connected extensively with the brain stem reticular formation of both sides. The main source of these pathways appears to be the magnocellular part. The reticular ascending pathways send fibers to the paramedian and gigantocellular reticular nuclei of both sides, whereas fibers entering the ipsilateral parvocellular reticular nucleus appear to come largely through the intranuclear ascending pathway. The nucleus caudalis sends fibers to the facial nucleus by way of the crossed and uncrossed reticular ascending pathways and slightly via the crossed medial lemniscal pathway. A few fibers are also found to enter the medial part of the dorsal accessory olive and the lateral reticular nucleus from the uncrossed reticular ascend- Efferents of Caudal Spinal Trigerninal Nucleus in Cat 399 ing pathway. This pathway gives off fibers to the vestibular nuclei which receive fibers also from the intranuclear ascending pathway. The nucleus caudalis sends no fibers to the hypoglossal nucleus, the dorsal nucleus of the vagus nerve or the motor trigeminal nucleus. The nucleus of the solitary tract receives scarcely any fibers from the nucleus caudalis. The nucleus caudalis projects fibers to the thalamus by way of the crossed medial lemniscal pathway only. The uncrossed medial lemniscal pathway appears to originate from the reticular formation adjacent to the nucleus caudalis. In the medulla and pons the crossed medial lemniscal pathway gives off some fibers to the medial reticular formation. At midbrain levels it sends fibers to the inferior and superior colliculi, and the magnocellular part of the medial geniculate body. In the caudal thalamus the crossed medial lemniscal fibers divide into lateral and medial groups. The former fibers enter the ventrolateral and lateral part of the posteromedial ventral nucleus, while the latter fibers are distributed in the dorsomedial part of the posteromedial ventral nucleus and the intralaminar nuclei. Some fibers recross through the massa intermedia to enter the parafascicular and centre median nuclei of the side ipsilateral to the lesion. The caudal part of the nucleus caudalis scends more numerous fibers to the intralaminar nuclei than the rostral part. In addition, the projection of the nucleus caudalis to the posteromedial ventral nucleus appears to be organized in the rostrocaudal direction. Fibers from the rostral part of the nucleus caudalis are more abundant and extend more rostrally in the posteromedial ventral nucleus than those from the caudal part. The marginal part of the nucleus caudalis gives rise to fibers passing through the crossed medial lemniscal pathway 'to the posteromedial ventral nucleus, but not to the intralaminar nuclei. The nucleus caudalis projects a few fibers to the field of Fore 1, the zona incerta and the subthalamic nucleus. No evidence is found for the existence of the cerebellar projection of the nucleus caudalis .

Acknowledgment The author wishes to thank Professor K. N i i m i for his helpful suggestions and encouragement during this work and for his critical reading of the manuscript. 400 Syosuke Kawamura

Abbreviations

Bc, Brachium conjunctivum Os, Nucleus olivaris superior C, Nucleus cuneatus Pc, Nucleus paracentralis Ce, Nucleus cuneatus externus Pdc, Pedunculus cerebri Cern, Centre median nucleus Pf, Nucleus parafascicularis Cho, Chiasma opti cum Pm, Nucleus pulvinaris medialis Ci, Colliculus inferior Po, Nucleus posterior Cl, Nucleus centralis lateralis Py, Pyramid Cm, Nucleus centralis medialis R, Nucleus ruber Cp, Commissura posterior R1, Nucleus reticularis lateralis Cs, Colliculus superior Rt, Nucleus reticularis thalami Dv, Nucleus dorsalis n. vagi Sg, Nucleus suprageniculatus F, Nucleus n. facialis Sgc, Substantia grisea centralis Flm, Fasciculus longitudinalis Sn, Substantia nigra medialis So, Nucleus tractus solitarii Flp, Fasciculi longitudinales pontis Sth, Nucleus subthalamicus G, Nucleus gracilis Tl, Nucleus trapezoidalis lateralis Gld, Corpus geniculatum laterale Tm, Nucleus trapezoidalis medialis dorsale To, Tractus opticus Gmm, Corpus geniculatum mediale, Vei, Nucleus vestibularis inferior pars magnocellularis Vel, Nucleus vestibularis lateralis Gmp, Corpus geniculatum mediale, Vem, Nucleus vestibularis medialis pax s principalis VA Nucleus ventralis posterolateralis H, Nuclei habenulae Vpm, Nucleus ventralis posteromedialis Hg, Nucleus n. hypoglossi VC, Nucleus tractus spinalis n. lc, Nucleus intercalatus trigemini, nucleus caudalis Ld, Nucleus lateralis dorsalis VIP, Nucleus tractus spinalis n. Ll, Lemniscus lateralis trigemini, nucleus interporalis Lm, Lemniscus medialis VM, Nucleus motorius n. trigemini Lp, Nucleus lateralis posterior Vmtr, Tractus mesencephalicus n. Md, Nucleus medialis dorsalis trigemini N11, Nucleus lemnisci lateralis VOR, Nucleus tractus spinalis n. Npl, Nucleus pontis lateralis trigemini, nucleus oralis Npm, Nucleus pontis medialis VSP, Nucleus sensorius principalis n. Nr, Nucleus raphe trigemini Oc, Nucleus n. oculomotorii Vstr, Tractus spinalis n. trigemini 0i, Nuclei olivares inferiores Zi, Zona incerta

References

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Explanation of Plate

All figures are photomicrographs from transverse sections through the brain stem of the cat. N a u t a-G y g a x method. x 420 1. Axon and preterminal degeneration in the magnocellular part of the medial geniculate body on the side contralateral to the lesion. Cat 8. 2. Axon and preterminal degeneration in the subthalamic nucleus on the side contralateral to the lesion. Cat 10. 3. Axon and preterminal degeneration in the medial part of the posteromedial ventral nucleus on the side contralateral to the lesion. Cat 10. 4. Axon and preterminal degeneration in the lateral part of the posteromedial ventral nucleus on the side contralateral to the lesion. Cat 10. 5. Axon and preterminal degeneration in the parafascicular nucleus of the operated side. Cat 7. 6. Axon and preterminal degeneration in the paracentral nucleus on the side contralateral to the lesion. Cat 6. 405

Plate

S. Kawamura