The Trigeminal System in the Pigeon (Columba livia) I. PROJECTIONS OF THE GASSERIAN GANGLION JACOB L. DUBBELDAM AND HARVEY J. KARTEN * Department of Psychology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

ABSTRACT The central projections of the Gasserian ganglion were investigated in the pigeon, Columba liuia. Lesions were placed in the ganglion either by direct surgical exposure or stereotaxically, and following survival times of one to four days, the brains stained with the Fink-Heimer method. The main group of central axons bifurcate to form distinct ascending and descending branches, the tractus trigemini ascendens (TTA) and the tractus trigemini descendens (TTD). A smaller lateral tract also courses caudally (1TTD) separate of TTD proper to terminate in the nucleus cuneatus externus. The TTA projects topographically upon the principal sensory nucleus of the trigeminus, ending in both the pars dorsalis and a smaller pars ventralis. The neurons a t the point of bifurcation of the entering radix have been designated as the pars oralis of nTTD. The TTD distributes caudally to several distinct subnuclei a t each level, and extends into the cervical spinal cord. Relatively discrete regions corresponding to the pars interpolaris and caudalis were recognized. The projections to the cervical cord terminate in laminae I-IV. There was no evidence of projections to the cerebellum, or contralateral PrV or TTD. There was a small projection to the contralateral cervical spinal cord. No clear evidence of a projection to the nucleus solitarius was found. The distribution of primary trigeminal axons is compared to that described in other vertebrates. The sensory trigeminal system is one of the major afferent systems of the brainstem of all vertebrates, conducting extroceptive information from cutaneous sense-organs and proprioceptive information from the jaw muscles. To date, however, most of the research of the central sensory trigeminal system has been done in mammals and relatively little is known about the projections and organizations of this system in other classes of vertebrates. Earlier studies on the central connections of the irigeminal ganglion of birds (e.g., Brandis, 1895; van Valkenburg, '11; Wallenberg, '64; Weinberg, '28; Woodburne, '36), are based mostly on the use of normal material. More recently, Molenaar and Dubbeldam ('691, and Dubbeldam ('771, outlined the projections of the trigeminal ganglion in the mallard duck, using the Nauta method, and the Fink-Heimer ('67) methods, respectively, and several recent physiological and behavioral studies J. COMP. NEUR. (1978) 180: 661-678.

have been reviewed by Ziegler ('73, '74). No detailed report of the central projection of the primary trigeminal afferents in birds is available. This study describes the central projections of the Gasserian ganglion in the pigeon by use of the Fink-Heimer method. Comparison of our results with corresponding data from other classes of vertebrates may provide further insight into the fundamental pattern of organizations of this most pervasive vertebrate sensory system. MATERIAL AND TECHNIQUES

White Carneaux pigeons (Columba liuia) (Hillside Pigeon Farm) were anesthetized with equithesin and lesions were made in the

' Present address: Zoologisch Laboratorium der Rij ksuniversiteit, 2300 RA Leiden, The Netherlands. 'Present address: Department of Psychiatry and Behavioral Science S.U.N.Y., Stony Brook,New York 11794.

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JACOB L. DIJBBELDAM AND HARVEY J. KARTEN

trigeminal ganglion or in the root of the Vth nerve, proximal to the ganglion. In seven animals the lateral aspect of the ganglion was exposed and a lesion was made with a small scalpel. Visual control of the lesion during the operation was often impaired by associated hemorrhage. In the remaining animals a n electrolytic lesion was made stereotaxically using an insulated insect pin, the position of the ganglion was estimated with the help of the atlas of Karten and Hodos ('67). Lesions were made with cathodal current a t 0.51.0 ma for 10-15 seconds. The brains were cut a t 26 pm on a freezing microtome in transverse (8 pigeons), sagittal (4) or horizontal planes (4) (Karten and Hodos, '67). Each eighth section was stained with the Fink-Heimer I method and adjacent sections were stained with cresylecht violet. In some cases additional sections were stained for both degeneration and Nissl, thus one Fink-Heimer section/l04 p was available. Drawings of the sections were made with help of a Wild camera lucida. The ganglia and part of the nerves of the operated side were stained in Marchi fluid (4 cases) or in Sudan Black B (Rasmussen, '61). The Marchi stained sections were dissected and examined under a stereomicroscope. The

Sudan Black B stained ganglia were embedded in albumin and cut a t l o p on the freezing microtome. Each tenth section was mounted in glycerin. In these sections fibers and ganglion cells are visible. The area of the lesion and the degenerating fibers are marked by the presence of irregular black grains. The heads of three more animals were dissected under an operating microscope in order to study the course of the main branches of the Vth nerve. DESCRIPTION

The peripheral parts of the Vth nerve In the pigeon the three main branches of the trigeminal nerve are the ramus ophthalmicus (ROp), the ramus mandibularis (RMd) and the ramus maxillaris (RMx) (fig. 1). The three branches converge in the ganglion semilunare (ggl. Gasseri or ggl. trigeminale). Within the ganglion, the ophthalmic portion is relatively segregated from the maxillo-mandibular portion (fig. 2). The maxillary and a mandibular portion however, were fused, rendering it difficult to make differential lesions in these latter portions. Two types of ganglion cells can be recognized: small, dark type cells (Gaik and Farbman, '73) in the medial part of the ganglion and larger, light type cells more laterally.

Abbreviations

An, nucleus angularis Bc, brachium conjunctivum bl.v., blood vessel Cb, cerebellum Cbd, tractus spinocerebellaris dorsalis CbL, n. cerebellaris lateralis CC, canalis centralis cd, pars caudalis of n'ITD CE, n. cuneatus externus FD, funiculus dorsalis FL, funiculus lateralis FLM, fasciculus longitudinalis medialis FU, fasciculus uncinatus FV, funiculus ventralis GC, nn. gracilis et cuneatus ggl V, ganglion trigeminale (Gasseri) IM, n. intermedius 10, n. isthmo-opticus ip, pars interpolaris of nTTD La, n. laminaris La. I, I1 etc., lamina I, I1 etc. LoC, locus ceruleus LOpt, lobus opticus LS, lemniscus spinalis ITTD, tractus externus (lateral TTD) Lx, site of lesion Mc, n. magnocellularis M V, n. motorius N.V Mx-Md, maxillo-mandibular portion of gg1.V N I, I1 etc., nervus I, I1 etc. n VII, X etc., n. motorius N VII, X etc.

nTTD, nucleus of the tractus descendens ofNV 01, n. olivarius inferior Op, ophthalmic portion of gg1.V or, pars oralis of nTTD OS, n. olivarius superior PaM, n. paramedianus PH, plexus of Horsley PL, n. pontis lateralis PM, n. pontis medialis pPd, v, n. paraprincipalis pars dorsalis, pars ventralis PrVd, v, n. sensorius principalis N V pars dorsalis, pars ventralis R, nn. raphes Rgc, n. reticularis gigantocellularis RMd, ramus mandibularis of N V RMot V, motor root of N V RMx, ramus maxillaris of N V ROp, ramus opthalmicus of N V Rpc, n. reticularis parvocellularis RST, tractus rubro-spinalis RxV, motorfibers of N V S, n. solitarius Ta, n. tangentialis TS, tractus solitarius 'ITA, tractus ascendens nervi trigemini TTD, tractus descendens nervi trigemini VeD, formatio vestibularis descendens VeM, n. vestibularis medialis VeS, n. vestibularis superior

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

663

Fig. 1 Schematic drawing indicating the distribution of the peripheral branches of the Gasserian gangli on in the pigeon.

RMd contains sensory as well as motor fibers (cf. Barnikol, '53). A number of short offshoots innervate the adductor complex of the lower jaw. A major branch of RMd is the N. pterygoideus which innervates the muscles of the protractor pterygoidei complex. The main sensory branch enters the mandible and bifurcates. A rather thin branch innervates the caudal part of the horny skin of the mandible. The other thicker branch gives offshoots to the ventral feathered skin of the rostral part, particularly the tip, of the lower jaw. ROp and RMx are purely sensory nerves. The RMx runs ventrally through the orbit and innervates the skin rostral to the eye; a small number of fibers penetrate the horny skin in the caudal part of the upper bill. The ROp is embedded in the connective tissue that surrounds the eye. Rostra1 to the eye a branch splits off to innervate the skin rostral to the orbit. The main branch is enveloped in the same sheath of connective tissue with the olfactory nerve. It sends branches to the nasal area and the rostral part of the upper bill.

The central projections The location and extent of the lesions were verified in the sections of the ganglia (fig. 2). A rather complete lesion was obtained in two cases, one cut in the sagittal plane, the other one in the transverse plane. The other lesions damaged only part of the ganglion. In these cases mainly the mandibular portion was affected, but depending on the place of the le-

sion, proximal or distal within the ganglion, the maxillary and ophthalmic portions were also occasionally involved. In one case, cut in horizontal plane, the lesion is far distal in the ganglion and affects virtually only the maxillary branch. In virtually all cases there was a t least slight damage to the optic lobe. The resulting degeneration did not interfere with that of the trigeminal nerve and could be readily recognized, as the projections of the optic lobe have been studied extensively. (Karten, '65; Hunt and Kunzle, '7'6). Within the brainstem impressive terminal degeneration as well as fiber degeneration of the trigeminal system is visible after a survival time of 28 to 48 hours. With four days survival the fiber degeneration is still distinct, but the terminal degeneration is less clear, especially in fields with fine boutonal grains.

General trajectory of the entering radix- TTA, TTD and lTTD The sensory trigeminal root enters the brainstem and divides into an ascending and a descending branch. The ascending branch or tractus ascendens nervi trigemini (TTA) turns dorsally and rostrally and projects mainly upon the principal sensory nucleus of the trigeminal nerve (PrV). The descending branch or tractus descendens nervi trigernini (TTD) descends through the myelencephalon and the first four segments of the cervical cord. In its caudal course i t projects upon several cell

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JACOB L. DUBBELDAM AND HARVEY J. KARTEN

A

B

E

Fig. 2 Reconstruction of a lesion in the caudolateral portion of the ganglion.

groups, the nuclei of the TTD (nTTD). Another group of neurons lies in the transitional area of TTA and TTD and may receive afferents from both branches. We named it the nucleus oralis of the trigeminal system (or). The most lateral fascicles of TTD are slightly segregated from the rest of the tract. In normal material these fascicles seem to be part of the TTD. In degeneration preparations, however, the lateral fascicles appear to have their

own route and terminal fields, and they can be considered to form a separate tract: the tractus externus or lateral TTD (ITTD). In all our cases both TTA and TTD were degenerating, suggesting that the two tracts are not grossly segregated in their locus of origin in the ganglion. After partial lesions of the ganglion, the regional distribution of fibers to the components of PrV and nTTD is more readily apparent as the lesser density of fibers permits the delineation of subdivisions of

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

these nuclei. Complete section of the Vth nerve results in such massive degeneration, that adjacent fields appear confluent and separation of cytologic subdivisions proved difficult. Basically, however, the same pattern of degenerating fibers and projections was found in all cases. No degeneration was observed in the tract of the mesencephalic trigeminal nucleus.

The projection areas of TTA TTA is a short ascending tract that penetrates the principal sensory nucleus V (PrV). PrV consists of two major divisions, a diffuse pars ventralis (Pr Vv) and a compact pars dorsalis (Pr Vd). The neurons of the ventral part (PrVv) are intermingled with the fascicles of TTA. TTA continues dorsally to encapsulate the PrVd. PrVd is a well circumscribed, roundish or oval nucleus in sagittal as well as transverse planes; it contains several subdivisions. The fibers of TTA sweep around the medial and caudal poles of PrVd and small fascicles penetrate the nucleus (figs. 3,4). The neurons of PrVd lie in clusters of two to four cells, which is very clear in Nissl preparations (fig. 10).PrVv is less sharply circumscribed and is directly contiguous with n. oralis of TTD. The cells of PrVv are slightly larger than those of PrVd and do not form clusters. Complete lesions of the Vth nerve result in dense terminal degeneration throughout PrVd and PrVv. In the latter rather coarse silver grains occur around and upon the cell bodies. In PrVd a very dense boutonal degeneration is present around the cell clusters (fig. 11); in this nucleus a medial field with less densely packed and finer boutons is visible in transverse sections (fig. 3:A). Partial lesions cause terminal degeneration in restricted areas of PrVd. Sagittal sections most clearly reveal that a lesion in the mandibular portion of the semilunar ganglion results in boutonal degeneration in the dorsal and caudal area of this cell group (fig. 9). When the maxillary and ophthalmic portions are involved terminal degeneration occurs also in more ventral and rostra1 areas. In all cases degenerating fibers and boutons can be seen in the PrVv, with the density depending on the size of the lesion. However, there is no obvious topographical distribution in PrVv. Lateral to PrV a narrow nuclear area is present, the nucleus paraprincipalis (pP). This nucleus can be seen in cross sections (fig.

665

3:A), but also it appears as a distinct nucleus in sagittal sections with a dorsal and ventral division (fig. 4:B,C). pP resembles a part of PrVd, but degenerating fibers or boutons were never clearly found in this nucleus. A few degenerating fibers were seen dorsal to PrV, but it is not clear whether these terminate in this area or eventually ascend into the cerebellum. However, no trace of degeneration could be found in the cerebellum. A third nuclear division receiving ganglionic projections lies a t the level of the incoming trigeminal root. The cells are, a t least partly, intermingled with fibers that ascend to PrV. The nucleus consists of large cells and contains rather coarse boutons. It is continuous with the PrVv above, and the TTD below. However, it is possible to delimit this nucleus from PrV, as it forms a transition area between the ventral part of PrV and the nuclei of the TTD (fig. 4). For the present we consider it to be a separate nucleus and call it the nucleus oralis (or). Crosby and Yoss, ('54) consider it to be a part of nTTD (DISCUSSION).

The nuclei of the TTD A large number of sensory root fibers of nerve V swing caudally to form the TTD. In the so called nucleus of the TTD (nTTD) several subdivisions can be distinguished. In this study, we will discern a pars interpolaris (nTTD, ip) and a pars caudalis (nTTD, cd), though a further subdivision of the cell groups may be possible. Cytoarchitectonic features of these subdivisions are illustrated in the atlas of the pigeon brain by Karten and Hodos, '67). The pars interpolaris (nTTD, ip) can be separated from the nucleus oralis, the border being a line between the N VII roots and the root of motor nerve V. Ip consists of several cell groups. A t the level of the vestibular root, clusters of relatively large neurons lie between the lateral fibers of TTD. More medially a group of slightly smaller cells is surrounded by degenerating fibers. In this medial portion, the terminal degeneration is more distinct than in the lateral cell clusters, the boutons being coarser in the former. The two cell groups can be considered to be a lateral and an intermediate part of the n. interpolaris. Ventral to the root fibers of N. IX a field of fine terminal degeneration extends medially to a point ventral to the solitary area (fig. 3:E). This field is considered to be a medial division of the n. interpolaris. Rare fine degenerating

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JACOB L. DUBBELDAM AND HARVEY J. KARTEN

fibers can be seen penetrating the solitary area, but no terminal degeneration was observed in the nucleus solitarius. Thepars caudalis (nTTD, cd) begins a t the level of N X and the obex. Here TTD begins to shift to the dorsal region of the cord. The nucleus appears in the middle of TTD and continues into the dorsal horn of the first few cervical segments. Rostrally the pars caudalis consists of large cells, but it lacks the laminated structure, characteristic of the dorsal

horn. The terminal degeneration shows the form of moderately coarse silver grains. The transition of this rostral part into the dorsal horn is not very distinct either in transverse, or in sagittal sections. The course of TTD is oblique to the midsagittal plane, thus in any single sagittal section various sagittal planes of TTD and nTTD are visible, rendering the distinction of cell groups along the rostrocaudal axis difficult (fig. 7). The dorsal horn of the first four cervical seg-

IT

Fig. 3 A-J: Distribution of the Gasserian ganglion upon the trigeminal complex in the pigeon. Transverse series. See text and Abbreviations. A, most rostral; J, cervical spinal cord. Coarse dots represent axons, fine stipple indicates terminal degeneration.

667

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

merits receives a substantial trigeminal projection and can be considered part of nTTD, cd. It has a dorsal cap of degenerating fibers, and is composed of four layers of terminal degeneration (figs. 6 , 7). These layers can be recOgnized best in transverse sections' Figure g shows the characteristics Of the various layers:

Layer I is a monolayer of rather large, fusiform cells ~

I

e

~presence ~of dispersed, ~

Layer 111 consists of medium size cells with large boutons. The presence of many cells marks the borderline between layers I1 and 111. Layers I1 + I11 constitute the The distinction substantia gelatinosa Rolandi (SG). between the two layers was apparent both on the basis

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tiny cells and fine dustlike boutons;

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JACOB L. DUBBELDAM AND HARVEY J. KARTEN

A

Fig. 4 A-C: Distribution of the Gasserian ganglion as seen in sagittal sections. A, medial; C, lateral. Spinal cord to the left. See text and Abbreuiations.

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

B

669

C

F Fig. 5 Charting indicates the distribution of the Tractus externus of TTD (1TTD) to the nucleus cuneatus externus. This charting shows the left side of the brain stem. The projection to nTTD proper is omitted for the sake of clarity. See text for description. of the size of argyrophilic particles in these layers, and also in the differential argyrophilia a t 24 versus 48 hours survival time following ganglionectomy. Layer IV is characterized by slightly larger and often triangular cells, that intermingle with the rather thick axon8 forming a ventral hilus.

After a complete lesion of the trigeminal ganglion dense terminal degeneration can be seen throughout the medio-lateral extent of the dorsal horn in C1-C4 (fig. 6). After a lesion in the mandibular part of the ganglion the degeneration is mainly restricted to the medial part of the dorsal horn; when the maxillary portion is involved, degenerating boutons are present in the intermediate portion of the area. The ophthalmic projection presumably occupies the lateral part of the pars caudalis of nTTD, though lesions confined to the ophthalmic division of the ganglion were not obtained. A small number of fibers cross in the cervical cord and terminate in the most medial part of the contralateral substantia gelatinosa.

The lTTD and its projection areas As mentioned above, we consistently noted the presence of a distinct tractus externus (1TTD). This tract consists of several fascicles of degenerating fibers that run caudally, parallel to the TTD but clearly separated from i t (figs. 3,5). Between lTTD and TTD small cells and a few larger cells and scattered degenerating fragments are visible. At the level of the entering nerves IX and X the lTTD shifts dorsally, taking a position along the periphery of the medulla. The fibers penetrate the nucleus cuneatus externus (CE).In this nucleus light terminal degeneration is present dorsal and dorso-medial to the degenerating fiber cap of the spinal trigeminal tract. DISCUSSION

The projections Essentially our data concur with the oldest descriptions of the trigeminal system in birds (e.g., Brandis, 1895; van Valkenburg, '11).

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JACOB L. DUBBELDAM AND HARVEY J. KARTEN

-. .-. __. La.V-VJ

FL

/

/ Fig. 6 Charting of the laminar distribution of degeneration within the dorsal horn of the spinal cord. Transverse section. Stipple indicates terminal degeneration. Indicates the presence of finer terminals in Layer I1 than in Layer iII. See figure 8.

These descriptions of the system, however, were based mainly on studies of normal material. The experimental data provide a more detailed picture of the distribution of the central projections of the Gasserian ganglion and can help to clarify some of the still existing uncertainties. Brandis (1895) described the presence of an ascending and a descending trigeminal tract. Cajal ('09-'11) noted that TTA and TTD result partly from a bifurcation of entering sensory root fibers. Other fibers either ascend in TTA or descend in TTD (cf. also Brandis, 1895; Crosby and Yoss, '54).The bifurcation of fibers offers an explanation for the consistent occurrence of degeneration in both TTA and TTD even after small lesions in the ganglion. It also implies the common origin of a t least part of the two tracts. This latter notion is supported further by electrophysiological data, from

which TTA and TTD appear to convey the same kind of information (data in birds: Zeigler and Witkovsky, '68; Silver and Witkovsky, '73; in mammals e.g., Eisenman et al., '63). The presence of an ascending and a descending tract might suggest a discontinuity in the projection fields of the trigeminal ganglion. Several authors (Woodburne, '36; Crosby and Yoss, '54)have suggested that the terminal fields of TTA and of TTD are segregated in birds. Our data, however, clearly show the continuity of the trigeminal projection areas in the pigeon. This continuity is particularly obvious in sagittal sections, but more difficult to recognize in transverse serial sections. Observations in the duck (Dubbeldam, '77) are in agreement with the present report. The continuity of the trigeminal projection fields does not imply a uniformity of the cell

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

,

Imm

671

I

Fig. 7 Charting of sagittal section showing the distribution of TTD at the bulbospinal junction, with the seemingly abrupt appearance of lamination at this level. More caudal projections to the spinal cord are not indicated on this charting as the spinal cord narrows and the dorsal horn tends to lie progressively more medially. See Abbreviations.

areas. In earlier studies, a principal sensory nucleus (our PrV) and a “nucleus of the spinal trigeminal tract” (our nTTD) were recognized (Brandis, 1895; van Valkenburg, ’11; Woodburne, ‘36). I t is, however, possible to differentiate the two divisions into distinct subnuclei. Thus PrV consists of separable dorsal and ventral parts (PrVd and PrVv respectively) (Craigie, ’28; Sanders, ’29; Stingelin, ‘ 6 3 , and TTD may be grossly subdivided into a pars interpolaris (nTTD, ip) and a pars caudalis (nTTD, cd). In the transitional area of TTA and TTD yet another cell group can be recognized, here referred to as pars oralis (or). However, i t is not entirely clear whether this cell group is a separate subnucleus, part of PrVv, of the rostralmost part of nTTD. In birds PrV projects upon the ipsilateral as well as the contralateral nucleus trigeminalis prosencephali (n. basalis; for discussion of the name n. trigeminalis prosenc. see: Cohen and Karten, ’741, though with no apparent “tha-

lamic” projection (Wallenberg, ’03; Zeigler et al., ’69; Dubbeldam and Wijsman, ’74). More recent findings of Karten (in preparation) indicate, that the quintofrontal tract arises from PrVd alone. The distribution of the afferent fibers to the n. trig. prosencephali differs between the two sides and is discussed a t greater length by Karten (in preparation). The nucleus paraprincipalis (pP) is a narrow band of cells that lies lateral to PrV. pP appears to be part of PrV, particularly in sagittal sections, yet we found no indication of a direct projection from the trigeminal ganglion upon pP. However, after injection of horseradish peroxidase into the region of the trigeminalis prosencephali (nPT or nucleus basalis) the perikarya of the n. paraprincipalis are heavily labelled with the reaction product (unpublished observation by Karten). This observation suggests the possibility that perhaps pP forms part of the ascending trigeminal pathway. Alternately, pP may repre-

672

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JACOB L. DUBBELDAM AND HARVEY J. KARTEN

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Fig. 8 Detailed charting of the dorsal horn a t approximately C-14-2. Coarse lines indicate degenerating axons. Small and large dots represent relatively smaller and larger terminal degenerating boutons. Compare Laminae I, 11, 111 and IV.

sent part of a lemniscal system projecting to a region adjacent to nPT but of a different modality (Leibler, '75; Ph.D. thesis). The pars oralis (or) is continuous with PrVv and lies a t

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Fig. 9A Charting indicating a topographic distribution of the ramus mandibularis within the PrVd. Sagittal plane. The mandibular branch terminates in the dorsal and caudal portion of PrVd. Caudal to the left, rostral to the right. B Location of the lesion within the ipsilateral Gasserian ganglion. C Schematic diagram indicating the relative domains within PrVd of each main branch of the ganglion. See Abbreviations.

the point of bifurcation of the incoming nerve root. Craigie ('28) emphasized the resemblance of his postero-ventral PrV and the rostral part of nTTD in the humming bird. In the pigeon, we also noted the general similarity of the cells of PrVv andor. It could be just a matter of slight differences in position in the different birds that determines whether the afferents to the pars oralis should be considered ascending or descending. In consequence, it is uncertain, whether this nucleus would be considered to be part of the nTTD or a nucleus of the TTA and thus may be even part of PrVv. Information about the efferent connections may provide more evidence about the character of the pars oralis. Injection of horseradish peroxidase into the nPT did not indicate that or projects upon nPT (Karten, in preparation). A comparable situation obtains in the study of mammals. Torvik ('56) described the nucleus oralis in the r a t to be the most rostral nucleus of the TTD complex. Experiments in the pig and the dog, using retrograde chromatolysis, however, suggested that the pars oralis projects upon the same area in the ventral thalamus complex as PrVv (Michael and

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

673

Fig. 10 Nissl-stained section of PrVd demonstrating the clustering of neurons. Cresyl Echt Violet. Magnification X 450.

Karamanlides, '70). Electrophysiological recordings in the cat led Darian-Smith et al. ('63) to the suggestion of a common function of PrV and the noralis. These data again could be reason to regard the nucleus oralis as a part of the principal V complex. However, serious ambiguity still exists in defining the boundaries of the various subdivisions. Pars interpolaris (ip) is composed of several cell groups that differ in size of the cells a s well as packing density. In this study, however, we will not try to differentiate this nuclear area into additional subgroups. There is no apparent trigeminal projection to the overlying solitary complex, though a field with fine degenerating fibers and terminal degeneration extends, ventral to the N IX, from the TTD to the lateral pole of the solitary complex. We consider this field to be a medial portion of the pars interpolaris. Some sparse degenerating fibers seem to penetrate into the n. solitarius ventro-lateralis anterior, but no terminal degeneration was visible.

The pars caudalis (cd) consists of two parts. The rostral part cannot be delineated sharply from ip, the main difference between the two subnuclei being the size of the perikarya. The rostral part of cd is continuous with the dorsal horn of the cervical cord. The dorsal horn of the segments Cl-C4 receives a n impressive projection from the trigeminal ganglion and is generally considered part of cd. The rostral part of cd lacks the laminated structure of the dorsal horn and the latter might be considered a separate subnucleus, e.g., the pars spinalis of nTTD (cf. Cohen and Karten, '74). In conformity with the studies in mammals, however, in the present account the term pars caudalis is maintained for both the rostral part of cd and the dorsal horn of Cl-C4. In the dorsal horn, four layers are recognized. Olszewski ('50) distinguished three subnuclei in this area in man: a subnucleus marginalis, a subnucleus gelatinosus and a subnucleus magnocellularis. Probably, these subnuclei correspond to our layer I, layer I1

+

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JACOB L. DUBBELDAM AND HARVEY J. KARTEN

Fig. 11 Dense terminal degeneration around clusters of neurons of PrVd. Fink-Heimer stain. Magnification x 440.

I11 and layer IV respectively. The resemblance of the lamination of the dorsal horn in the pigeon to Rexed's laminae in the cat is apparent (Rexed, '52, '54; Kerr, '70). Our data provide a more detailed picture of SG in C1C4 in the pigeon than that of van der Akker ('70). This author could only find a slight lamination in the dorsal horn. A more extensive discussion on the cytoarchitectonics of the spinal cord in the pigeon is given in the papers of Cohen and Karten ('74) and Leonard and Cohen ('75). Yet, even these subdivisions do not do justice to the multiplicity of nuclear groups in the nTTD. Presumably, a more detailed inventory of the differential afferentlefferents of each subnucleus is needed to clarify the identity of each of the several subnuclei. The tractus externus of N V (1TTD) might

be considered to be part of the TTD, but (a) it can be segregated from the TTD proper easily in transverse as well as sagittal sections (figs. 3, 4) and (b) it terminates separately from TTD. The presence of these fibers and the occurrence of terminal degeneration in the nucleus cuneatus externus is also depicted in a posthumously published paper by Wallenberg ('64). He considered the fascicles t o be part of the radix spinalis trigemini, (TTD). In a recent paper Molenaar ('74) described an "additional trigeminal system in the python" consisting of a lateral descending tract and associated nucleus. Molenaar relates the presence of this system to infrared detection in pythons and pit vipers. His suggestion is supported by the data of Schroeder and Loop ('76). By '11, van Valkenburg had already described the presence of a dorsal and a ventral part of

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

the TTD in the boa. He found no comparable tracts in other reptiles and considered the situation characteristic for snakes. His ventral portion of TTD clearly corresponds t o the lTTD of Molenaar ('74). We suggest that the tractus externus in the pigeon and the lateral TTD in the python and other snakes represent a similar neurological system. This implies that the nucleus of the lTTD in the python could be compared to the n. cuneatus externus in birds. Of course, this does not exclude the possibility that the prominent development of this system in certain species is related to the possession of a particular type of sense organ. If our suggestion is correct, it can be expected that this "lateral descending trigeminal system" is a more general feature in vertebrates. A major point of earlier concern had been the question whether or not there is a direct cerebellar projection from the semilunar ganglion. Sanders ('291, Weinberg ('28) and Whitlock ('52) described trigeminal root fibers projecting directly upon the cerebellum. These fibers may be collaterals of trigemino-mesencephalic fibers (Sanders, '29; Bortolami e t al., '72). Craigie ('28) described a trigemino-cerebellar projection originating from the anterodorsal portion of PrV. There are also electrophysiological indications for the existence of a trigemino-cerebellar projection (Azzena e t al., '701, but it is not clear from these data whether it is a direct or an indirect connection. Molenaar and Dubbeldam ('69) in a preliminary Nauta study of the trigeminal nerve in the duck found no degenerating fibers ascending into the cerebellum after a ganglion lesion. Our data, too, indicate that there is no distinct projection from the ganglion onto the cerebellum. Comparison of the situation in birds and that in other tetrapod vertebrates reveals a clear consistency in the overall pattern of the trigeminal sensory projections (cf. Ariens Kappers et al., '36). The main difference concerns the projections upon the solitary complex. In amphibians (Joseph e t al., '68; Fuller and Ebbeson, '73) as well as in mammals (cf. Torvik, '56) degenerating fibers and terminals were observed in the tractus and nucleus solitarius. Neither our data, nor observations in the duck (Dubbeldam, '77) provide evidence for a trigeminal projection upon the solitary complex in birds. Clarke and Bowsher ('62) report the presence of a small contralateral projection upon

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the pars interpolaris of nTTD in the rat. Electrophysiologically, Nord ('76) demonstrated in the cat that some neurons in the pars caudalis could be activated by stimulation of the ipsilateral as well as the contralateral tooth pulp. We could find no such crossing of fibers in the pigeon, except in the spinal cord, where a few fibers cross the midline dorsal to the central canal to the end in the medial most part of the contralateral dorsal horn. This concurs with the observations of Torvik ('56) in the rat. A more puzzling aspect of the study of Clarke and Bowsher ('62) is the description of terminal degeneration in the motor nuclei of N V and VII and in the ventral horn in the rat. Neither the study of Torvik in the rat, nor our findings in the pigeon sustain this observation. The ganglion semilunare The consistency in pattern of the projections after lesions of various size is remarkable in view of the dual embryogenetic origin of the trigeminal ganglion (ganglion semilunare or Gasserian ganglion). In the pigeon two types of perikarya were found, corresponding to the cell types described in the chick ganglion (Gaik and Farbman, '73). From his study on the embryology of the ganglion, Hamburger ('61) suggested that the large cells are of placodal origin, the small type of cells of neural crest origin. The differentiation of the latter groups differs in several respects from that of the placodal neuroblasts (Meyer et al., '73). From his experiments, Hamburger ('61) concluded that the somatosensory exteroceptive axons emerge from the placode-type neurons, the function of the neural crest cells of the semilunar ganglion being unknown. The distinction between the ophthalmic and maxillo-mandibular portions of the ganglion is independent of the presence of the two cell types (Hamburger, '61). In mammals, too, the presence of two cell types in the trigeminal ganglion is firmly established, e.g., in the rat (Peach, '71). Gobel ('74) has suggested that the small, dark type cells may be concerned with conveying thermal and nociceptive information. A further analysis of the differential projections of these two cell types in the ganglion is needed to clarify the significance of the two cell populations. Recent studies by Hokfelt suggest that the small cells include a contingent of cells containing substance P that may selectively project upon the spinal division of nTTD in rats (Hokfelt e t al., '75).

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Differential projections o f the branches o f N V Though we lack a complete series of lesions confined to either the mandibular, the maxillary or the ophthalmic portion of the ganglion, our data permit us to make some remarks about the differential projections of the three main trigeminal branches. From examination of the sections of the ganglia and branches, most partial lesions appear to cause damage to either the mandibular or the maxillo-mandibular portion of the ganglion. In these cases the terminal degeneration is restricted mainly to the dorsal and caudal area of PrVd; in all cases there is a t least some terminal degeneration throughout PrVv, but not as dense as after a complete lesion of the trigerninal root. In animals with a lesion of the mandibular portion alone, boutonal degeneration in PrVd occurs in a smaller area than in cases where the maxillary branch is involved. Kerr ('63) reports that in the monkey, the mandibular branch projects upon the dorsal part of PrV, the maxillary branch upon the intermediate and the ophthalmic branch upon the ventralmost part of PrV. On the basis of single-unit analysis, Zeigler and Witkovsky ('68)describe the same sequence of t.he projection zones in the pigeon. Such a distribution was not clear in the r a t (Torvik, '56). In our studies, the three branches do not seem to project simply into a dorsal, an intermediate and a ventral part, but upon three curved zones of PrVd, the mandibular zone being the most dorsal and caudal and the ophthalmic zone the most ventral and rostra1 (fig. 9). According to the description of van Valkenburg ('11) in birds, the mandibular fibers have a dorsal position, the maxillary fibers an intermediate position, and the ophthalmic fibers, the most ventral position in the TTD. This description concurs with observations in mammals (Torvik, '56; Kerr, '63). However, our observations indicate t h a t a topography exists in medio-lateral direction. Van Valkenburg also claimed the most dorsal, mandibular fibers extend farther caudally in the spinal cord than the most ventral, ophthalmic fibers. Kerr ('63) did not find this difference in distribution in monkeys. Our observations do not permit us to confirm or deny the observations of van Valkenburg ('11). We observed that after mandibular or maxillo-mandibular lesions, the terminal degeneration was confined to the medial part of SG

of the cervical spinal cord, whereas after a complete lesion of the ganglion, degeneration occurred throughout the SG. In addition, observations in the duck indicate that the maxillary branch projects upon the middle part of SG (Dubbeldam, unpublished observations). From these data it can be concluded that the maxillary and ophthalmic projections are restricted mainly to the intermediate and most lateral part of SG respectively. This conclusion concurs with findings in the rat (Rustioni e t al., '71). Functional aspects The nervus trigeminus in birds is known to innervate cutaneous sense organs in the bill, around the orbita and in the oral cavity, a s well as proprioceptive organs in the jaw muscles. Severing the branches of the fifth nerve appears to have two effects (Zeigler, '73): (a) the feeding efficiency is markedly reduced and (b) the responsiveness to food is clearly reduced. In ducks, as well, the two effects of trigeminal deafferentation on feeding behavior were observed (Zweers and Wouterlood, '73). At least three types of information are conveyed by the afferent trigeminal system: exteroceptive information from mechanoreceptors related to the act of feeding; proprioceptive information related to the pattern of activity of the jaw muscles and to the movements of the beak; and thermal and nociceptive sensations. From the work of Zeigler and Witkovsky ('68)and of Silver and Witkovsky ('73) there is clear evidence that the same general types of information cues are conveyed to both PrV and the nTTD. Zeigler and Karten ('73) demonstrated t h a t bilateral damage to either PrV, the quintofrontal tract or the nucleus trigeminalis prosencephali (n. basalis) produces similar impairment of the feeding behavior as does trigeminal deafferentation. nTTD does not contribute to the quintofrontal tract and its role in feeding behavior requires further clarification. Though the nuclei of TTD comprise a large portion of the trigeminal system, neither their secondary connections, nor their functional significance is adequately understood. Recently, Darian-Smith ('73) reviewed the literature on the structure and physiology of the trigeminal system, but the data are almost exclusively derived from studies in mammals. Several experimental studies show that parts of nTTD project upon motor nuclei of N V, VII, IX and X (e.g., in sheep: Roberts and

CENTRAL TRIGEMINAL PROJECTIONS IN THE PIGEON

Matzke, '711, upon parts of the reticular formation (e.g., in cat: Carpenter and Hanna ('61); in primates, Tiwari and King ('74); in sheep, Roberts and Matzke ('71)and upon the cerebellum (Carpenter and Hanna, '61). There are also reports of ascending intranuclear fibers in the TTD, projecting upon the more rostral cell groups (Tiwari and King, '74; Roberts and Matzke, '71). Sessle and Greenwood ('74) suggest t h a t the caudal trigeminal nucleus may facilitate the synaptic transmission of oro-facial sensory information in the rostral trigeminal nuclei via intra-nuclear ascending fibers. Tactile responses to stimulation of the beak and proprioceptive activity from the jaw muscles have been recorded in the cerebellum of the pigeon (Gross, '70) and duck (Azzena e t al., '70).Trigeminal projections to the cerebellum appear to arise from cells of Ip (Karten, unpublished observations) a s well as possible afferents from the n.cuneatus externus and the mesencephalic trigeminal nucleus. A more thorough analysis of the nTTD complex and its afferent and efferent connections is clearly necessary. ACKNOWLEDGMENTS

1. This study was supported by the following grants: Doctor J. L. Dubbeldam was supported by a n award from IBRO-Unesco and a Sloan Foundation Award to the Department of Psychology of the Massachusetts Institute of Technology and NIH Grant NS 08624. Doctor Karten was supported in part by a n NICHHD Career Development Award. 2. We are greatly indebted to Mrs. Margaret Goldstein and Mr. c. Anthony Corry for their skillful assistance in the preparation of the histological material. We would also like to express our gratitude to Mrs. M. VogelsangLiem for her secretarial help and to Mr. J. Simons for his assistance in the final preparation of the figures. LITERATURE CITED Akker, L. M. van den 1970 An anatomical outline of the spinal cord of t h e pigeon. Studies in Neuroanatomy. Nr. 8. van Gorcum and Go.,Prakke & Prakke, Assen. Ariens Kappers, C. U., G. C. Huber and E. C. Crosby 1963 The Comparative Anatomy of the Nervous System of Vertebrates, Including Man (Reprint 1960). Hafner Publ. Comp., New York. Azzena, G. B., C. Desole and G. Palmieri 1970 Cerebellar projections of the masticatory and extraocular muscle proprioception. Exp. Neurol., 27: 151-161. Barnikol, A. 1953 Zur Morphologie des Nervus trigeminus der Vogel unter besonderer Berucksichtigung der Accip-

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The trigeminal system in the pigeon (Columba livia). I. Projections of the gasserian ganglion.

The Trigeminal System in the Pigeon (Columba livia) I. PROJECTIONS OF THE GASSERIAN GANGLION JACOB L. DUBBELDAM AND HARVEY J. KARTEN * Department of P...
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