J. Anat. (1978), 126, 2, pp. 225-245
225
With 11 figures Printed in Great Britain
An atlas of the dorsal thalamus of the marsupial brush-tailed possum, Trichosurus vulpecula J. R. HAIGHT AND L. NEYLON*
Department of Anatomy, University of Tasmania, Box 252C, GPO, Hobart, Tasmania 7001, Australia
(Accepted 7 March 1977) INTRODUCTION
For our work on thalamocortical relationships in Trichosurus we required detailed knowledge of the nuclear and cytoarchitectural organization of its dorsal thalamus, but we soon realized that a description adequate for our purpose did not exist. Goldby's (1941) account of the possum thalamus is an excellent general introduction, but has illustrative limitations and employs nomenclature which to some extent has been superseded. Rockel, Heath & Jones (1972) and Hayhow (1967) have described certain areas in some detail, but a comprehensive analysis is lacking. The Australian Trichosurus occupies an important position in comparative anatomy. A diprotodontid marsupial akin to the kangaroos, wallabies, wombats and the koala, this possum (or phalanger) is representative of the more advanced of the two major lines of Australian marsupial radiation. Within the metatherian subclass, Trichosurus is far removed from the stem marsupial line, of which living members of the American genus, Didelphis, are often taken as representative. As will be seen, the thalamus of the Australian brush-tailed possum differs in many respects from that of the American opossums as described by Bodian (1939) and Oswaldo-Cruz & Rocha-Miranda (1967, 1968). The atlas is not presented with stereotaxic coordinates. There are two reasons for this. First, Trichosurus exhibits considerable variation in body size. The Tasmanian possums used in this study are, with an average body weight of 3-2 kg, the largest representatives of their species. Possums inhabiting the warmer and drier areas of Australia tend to be much less massive, averaging 2 kg or less. These differences are reflected in skull and brain size (see Table 1). Brain weights of adult animals can range from 7-8 to 14'6 g. Second, there is inconsistency of internal organization within the possum thalamus (Haight & Neylon, 1977a); a significant minority (c. 35 %) of possums collected in Tasmania displayed an arrangement of thalamic nuclei sufficiently different from the norm to defeat any attempts at precise stereotaxic generalization. Such intraspecies variability makes a well illustrated atlas all the more necessary in order that those interested in working with this animal are aware of the 'normal' condition and can use the information to locate and identify the sometimes displaced and distorted nuclei. MATERIALS AND METHODS
The brains of three normal possums were used to compile this atlas. An additional 40 'experimental' thalami were referred to in order to confirm our assessments of * Present address: Department of Therapy, Western Australian Institute of Technology, Selby Street, Shenton Park, Western Australia 6008. IS
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J. R. HAIGHT AND L. NEYLON
Table 1. Comparison of body weights, brain weights and skull sizes in Trichosurus gathered from three areas of South Eastern Australia
Locality Adelaide, South Australia Sydney, New South Wales Hobart, Tasmania
Skull measurements , I Average bizygoAverage matic width basilar length mm (N) mm (N) 49-2 (14) 72-9 (14)
Average body weight kg (N) 1-6 (14)
Average brain weight g (N) 9-4 (14)
2-3 (20)
11-1 (20)
52-8 (9)
77-3 (9)
3-2 (56)
13 0 (23)
55-9 (12)
84-7 (12)
nuclear boundaries and configuration. All animals, normal and experimental, were captured in southern Tasmania between mid-1974 and mid-1976. Body weights ranged from 2-1 to 4 5 kg with a mean value of 3-2 kg. On average, males were 0 3 kg heavier than females. The normal possums were anaesthetized and perfused intracardially with 0-9 % saline solution followed by 10 % formol saline. In two cases the brains were embedded in celloidin and sectioned at 30 ,um, one in the coronal and the other in the sagittal plane. Alternate sections were stained for myelin using the Weil technique, and for cell bodies using warm aqueous thionin. Both series were mounted in Depex (Gurr). The remaining normal brain was embedded in egg yolk, frozen and sectioned coronally at 50 ,um, the sections being stained with aqueous thionin and mounted in Depex. Experimental animals were perfused with saline followed by a paraformaldehyde-glutaraldehyde mixture (Haight & Neylon, 1978). These thalami were sectioned, either in the coronal or sagittal plane at 40-60 ,tm, and certain sections stained with aqueous thionin while others were processed to demonstrate the retrograde transport of horseradish peroxidase from cortex to thalamus. These experimental thalami were also used to define nuclear boundaries where applicable. Thionin-stained sections prepared by the different methods were compared to ascertain whether significant differences in cell shape and staining properties were apparent. It was found that the celloidin technique produced more tissue shrinkage, otherwise the methods produced comparable results except that the staining quality and hence the photographic results were superior in the celloidin material. The atlas presented here consists of ten photographs with corresponding outline diagrams of the one normal, celloidin embedded and coronally sectioned brain. A Leitz Aristophot system was used to photograph the sections, using Kodak Plus-X pan sheet film, heavily orange filtered. The negatives were printed on high contrast Ilford F-4 paper. We have been conservative in nomenclature, contenting ourselves with bringing Goldby's (1941) treatment up to date. Where it was necessary to differ from Goldby we have usually accepted the usage of Rockel et al. (1972); exceptions are clearly indicated in the text. We have chosen to render this atlas in English, rather than employ a hybrid English-Latin neurological nomenclature. In doing this we have attempted to conform, where possible, to the standards laid down in the Nomina Anatomica (1966).
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The ten photographs were selected in order to point out the major features of the Trichosurus dorsal thalamus. The sections shown are not spaced at equal intervals but are irregularly spaced in accordance with the degree of change and the complexity of a given region. The levels of section are shown in Figure 1, which also gives an indication of the anteroposterior extent of selected thalamic nuclei. The notes and comments which follow compare our observations with those of other workers, in particular Goldby (1941) and Rockel et al. (1972). These comments are primarily restricted to matters of nomenclature and the 'lumping and splitting' of various nuclei and subnuclei, but they also point out differences between thalamus of Trichosurus and that of the American didelphids (as described by Bodian, 1939 and Oswaldo-Cruz & Rocha-Miranda, 1967, 1968). Detailed anatomical descriptions are provided only where previously undescribed regions are being considered or where difficulties arise in determining homologues between Trichosurus and Didelphis. Midline and intralaminar nuclei (Figs. 2-8) Though our general interpretation of these regions is in agreement with that of Goldby (1941), several points of divergence emerge when Trichosurus is compared with Didelphis. We include the region of the rhomboidal nucleus (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967, 1968) with the central nucleus because, like Goldby, we feel that the two regions are not sufficiently distinct to warrant separation in Trichosurus. Similarly, the reunient nucleus in Trichosurus includes the region described as the subparatenial nucleus in Didelphis. A separate centrolateral nucleus has not been recognized in Didelphis, this region apparently being considered a part of the paracentral nucleus (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967). I5-2
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Like Goldby, we feel that the two regions are cytoarchitecturally distinct and have therefore retained them as separate nuclei. Bodian, and Oswaldo-Cruz & RochaMiranda also describe, separately, a parafascicular and a posterolateral parafascicular nucleus. The latter appears to correspond to the parafascicular nucleus of Trichosurus while the former, on positional and cytoarchitectural criteria, may be equivalent to part of the intralaminar complex. In neither animal does the parafascicular (posterolateral parafascicular?) nucleus enlarge to form a distinct median central nucleus as it does in many eutherian mammals. Finally, in Trichosurus we do not distinguish a separate intermediodorsal nucleus as described in Didelphis. This region, comparatively very much smaller in Trichosurus than in Didelphis, corresponds to what we and Goldby include as the median seam of the paraventricular nucleus. Anterior nuclei (Figs. 2-5) This group of nuclei includes the anterodorsal, the interanterodorsal, the anteroventral and the anteromedial nuclei and is similarly organized in Trichosurus and Didelphis. Lateral nuclei (Figs. 4-11) The lateral nuclear complex of Trichosurus corresponds in most particulars with that described for Didelphis by both Bodian (1939) and Oswaldo-Cruz & RochaMiranda (1967, 1968) and differs, in our interpretation, from that proposed by Goldby (1941) for Trichosurus. Goldby divided the lateral tier into three major regions: an anterior 'Lateralis A', a ventral 'Lateralis B', and a posterior lateroposterior nucleus. Within 'Lateralis A' he recognized, but did not accord separate nuclear status to, a small group of cells which corresponds to our lateroanterior nucleus and, very probably, to the nucleus of the same name in Didelphis. The remainder of his 'Lateralis A' corresponds to our laterointermediate nucleus. Goldby's 'Lateralis B' was reassigned by Rockel et al. (1972) to the posterior nuclear complex (their nucleus Pob) as a result of their experimental findings. Accordingly, we have named this nucleus the posterior nucleus, wishing to note that only the name is changed; the position and nuclear boundaries being as Goldby described them. If homology of the laterointermediate and of the lateroposterior nuclei of Trichosurus and Didelphis is assumed, then these nuclei present internal differences in the two animals. The laterointermediate nucleus in Didelphis is divided into distinct dorsal and ventral regions by Oswaldo-Cruz & Rocha-Miranda (1967) but not by Bodian (1939). In Trichosurus the laterointermediate nucleus is cytoarchitecturally homogeneous. With the lateroposterior nucleus the reverse situation is present. In Didelphis no cytoarchitectural division into lateral and medial subnuclei has been described, whereas in Trichosurus such a division may be distinguished readily. The laterointermediate nucleus of these two marsupials is particularly difficult to place within the lateral nuclear complex of placental mammals. Oswaldo-Cruz & Rocha-Miranda (1967) remark that the marsupial laterointermediate nucleus may correspond to the laterodorsal nucleus of the cat. Retrograde degeneration studies of the thalamus after cortical ablations in both Trichosurus (Goldby, 1943) and Didelphis (Bodian, 1942; Diamond & Utley, 1963; Pubols, 1968) indicate a projection to the posterior parietal and peristriate cortical areas. In the macaque, however, the same experimental procedures indicate a laterodorsal nuclear projection to the basomedial temporal cortex (Locke & Kerr, 1973), a finding which would tend not to support the idea of homology between the eutherian laterodorsal and the metatherian laterointermediate nuclei. Further complicating the issue are our own
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(unpublished) findings, based upon the retrograde transport of horseradish peroxidase, which suggest that the peristriate and parietal cortices do not receive projections from the laterointermediate nucleus in Trichosurus. We are as yet unable to determine whether this nucleus projects to the basomedial cortex and are therefore unable to comment on the findings of Locke & Kerr. Medial nuclei Paratenial nucleus (Figs. 2-5) Though Goldby (1941) did not recognize any cytoarchitectural subdivisions in this nucleus, our material displays medial and lateral subdivisions. In this respect Trichosurus is similar to Didelphis (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967).
Mediodorsal nucleus (Figs. 5-7) Goldby (1941) recognized three subdivisions, basing his observations upon regional differences in myeloarchitecture and cell size. We do not consider these regional differences sufficiently reproducible from animal to animal to warrant separating them. Our interpretation is similar to that described by Bodian (1939) and OswaldoCruz & Rocha-Miranda (1967) in Didelphis. Ventral nuclei Ventroanterior nucleus (Figs. 4, 5) As with many eutherians (cat, Jasper & Ajmone-Marsan, 1954; squirrel monkey, Gergen & MacLean, 1962; macaque monkey, Olszewski, 1952, Walker, 1938), the ventroanterior nucleus is cytoarchitecturally distinct from the ventrolateral nucleus, a condition that is not as pronounced in the American opossum (Oswaldo-Cruz & Rocha-Miranda, 1967; Walsh & Ebner, 1973). Bodian's (1939) description of the opossum ventral nuclei is at variance with more recent treatments which tend to emphasize the similarities of this region in Didelphis with other mammals. We have not attempted to reconcile his interpretation with those of later workers. The cytoarchitecture of VA in Trichosurus appears to correspond closely to that described in the extreme anterior portion of the ventroanterior-ventrolateral complex (VAL) in the opossum (Oswaldo-Cruz & Rocha-Miranda, 1968). Of interest is the fact that the cortical projection of the ventroanterior nucleus in monkeys is to frontal and prefrontal regions (Carmel, 1970) while we have observed in Trichosurus that the cortical projection of this nucleus is primarily restricted to the parietal region (Haight & Neylon, 1977b). Ventrolateral nucleus (Figs. 4-6) Our ventrolateral nucleus corresponds to Goldby's ventrointermediate nucleus. Experimental evidence indicates that this region is similar to the ventrolateral nucleus in eutherian mammals, and it has been renamed accordingly (Haight & Neylon, 1977 c; Haight et al. 1976; Rockel et al. 1972). As noted above, the ventrolateral and ventroanterior nuclei in Didelphis are not clearly separable (Oswaldo-Cruz & RochaMiranda, 1967; Walsh & Ebner, 1973). Ventroposterior nucleus (Figs. 7-10) Goldby (1941) divided the ventroposterior complex into three cell groups; a dorsomedial group, which he thought might be equivalent to a 'submedius' nucleus;
J. R. HAIGHT AND L. NEYLON 240 a ventrolateral group; and, separating these two, a 'well defined condensation' or 'central core' of smaller cells. The ventroposterior nucleus, as defined in this paper and by Rockel et al. (1972), does not include Goldby's dorsomedial or 'submedius' division which, though not illustrated by him, probably corresponds to the ventromedial nucleus. The remaining 'central core' and ventrolateral parts of the complex correspond with the medial and lateral (VPM and VPL or trigeminal and lemniscal) divisions recognized in some eutherian mammals. This interpretation has been verified experimentally on the basis of VP's input (Rockel et al. 1972) and output connexions (Haight & Neylon, 1978; Haight et al. 1976). In Didelphis the ventroposterior complex is functionally divided into lemniscal and trigeminal zones (Pubols & Pubols, 1966; Sousa, Oswaldo-Cruz & Gattass, 1971; Walsh & Ebner, 1973) although a cytoarchitectural distinction is not obvious (Oswaldo-Cruz & Rocha-Miranda, 1967, 1968; Sousa et al. 1971). Hence, in this respect Trichosurus resembles certain specialized eutherians more than its generalized metatherian relative. The posteromedial subdivision of VP (our VPP) has not previously been described in Trichosurus although Rockel et al. (1972) include this region in the ventromedial nucleus (see their Fig. 4). On cytoarchitectural grounds this subnucleus is distinct from VM and is functionally associated with the VP complex (Haight & Neylon, 1978). VPP cells are large and of uniform size (see Table 2). They stain deeply and, between different individuals, exhibit considerable variation in packing density, ranging from a loose collection of a few cells visible in any one section to a distinct and well-formed subnucleus (Figs. 6, 7). In 21 % of the thalami examined VPP could not be distinguished (Haight & Neylon, 1977 a). Olszewski (1952) described a medial, small-celled or parvocellular subdivision of VPM (VPMpc) in the macaque. The similarly named region in the cat contains, in addition to small cells, many larger, deeply staining cells (Rinvik, 1968). The uniform large size and variable occurrence of VPP cells in Trichosurus distinguishes this subnucleus from VPMpc in the cat and monkey; however, the positional relationships of VPP and VPMpc are similar. No apparent equivalent of VPP is evident in Didelphis. Ventromedial nucleus (Figs. 5-9) Though not specifically mentioned by Goldby in the original description of the Trichosurus thalamus, the ventromedial nucleus, or a portion thereof, may have been included in his 'dorsomedial' or 'submedius' division of the ventroposterior complex. However, in a later paper Goldby (1943) separated the posterior portion of the anteromedial nucleus from the main body of that nucleus and gave it the name 'nucleus ventralis, pars medialis.' Our studies of the cortical projection of the ventromedial nucleds (Neylon & Haight, 1977) indicate that this region is not a part of VM and we have left it with the anteromedial nucleus. The ventromedial nuclei of Trichosurus and Didelphis are similar.
Posterior thalamus and metathalamus Posterior nucleus (Figs. 7-10) The posterior nucleus described here corresponds to Goldby's 'Lateralis B' nucleus, a nucleus regarded by Rockel et al. (1972) as being part of the posterior functional complex on the basis of its afferent connexions. In Trichosurus the nucleus is located between the lateral nuclear complex dorsally and the ventroposterior
Thalamus of Trichosurus
241
Table 2. A comparison of neuron size in VPP with neighbouring regions Region VPP VPM VPL VM
Neuron diameters Average diameter (#m) (range in,tm) 22-5 21-23 16-5 13-20 18-9 16-21 20-0 18-23
complex ventrally and is separated laterally from the medial geniculate nucleus by the medial lemniscus. The posterior nucleus of Didelphis is difficult to compare with that of Trichosurus. Oswaldo-Cruz & Rocha-Miranda (1967) describe a posterior nucleus which appears largely to correspond to the posterior Junctional complex in that animal (Mehler, 1969; Pubols & Pubols, 1966; Sousa et al. 1971). In contrast to Trichosurus, the Didelphis posterior nucleus is related anatomically to the medial geniculate nucleus, lying dorsal and lateral to the medial lemniscus. In the anatomical position of the Trichosurus posterior nucleus, Didelphus has a distinct cell group, 'Nucleus C' (Oswaldo-Cruz & Rocha-Miranda, 1967), which largely separates the posterior nucleus from the ventroposterior complex. The functional properties of cells in 'Nucleus C' suggest a possible association with the posterior functional complex (Sousa et al. 1971). From these data it would be tempting to homologize the opossum 'Nucleus C' with the possum posterior nucleus. However, this creates difficulties in comparing the large opossum posterior nucleus with similarly located structures in Trichosurus. Until further data are available, a meaningful comparison of this area in the two animals is not possible.
Suprageniculate nucleus (Figs. 8-11) This nucleus corresponds to that described by Goldby (1941) and to the suprageniculate component of the posterior complex (Pos) of Rockel et al. (1972). Portions of the Trichosurus suprageniculate nucleus may be included as part of the posterior nucleus in Didelphis.
Extrageniculate nucleus (Figs. 8-10) This region has not been previously described in Trichosurus. The nucleus is small and, except in well prepared and stained material, can be difficult to distinguish. The extrageniculate nucleus of EG is related to the anterior pole of the medial geniculate nucleus. Anteriorly, the nucleus appears to form a ventral extension of the lateroposterior nucleus between the medial lemniscus and the fibres of the external medullary lamina and optic tract. The rostral pole of the medial geniculate becomes encapsulated between the medial lemniscus and extrageniculate nucleus which then forms an indistinct, narrow crescent of cells over the lateral and ventral aspects of the principal division of the medial geniculate. Posteriorly, the ventral extremity of the crescent is continuous beneath the medial lemniscus and connects with the ventroposterior complex. The cells of the extrageniculate nucleus are of medium size and are highly variable in shape. Many are fusiform and are oriented parallel to the fibre tracts which partially surround the nucleus. Anteriorly, they are distinguished with difficulty from cells of the lateroposterior nucleus. Further, a distinction, based solely upon I6
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J. R. HAIGHT AND L. NEYLON 242 cytoarchitectural criteria, between the principal division of the medial geniculate nucleus and the extrageniculate nucleus can be difficult to make. However, the extrageniculate nucleus cells are usually less heavily stained than those of the medial geniculate and often a thin fibrous lamina can be distinguished separating the two nuclei. Though the afferent relationships of the extrageniculate nucleus have not been determined, the region is clearly distinguished by its projection to the superomarginal aspect of the parietal cortex, a feature which renders the extrageniculate nucleus quite distinct from its neighbouring thalamic nuclei (Haight & Neylon, unpublished observations).
Subparafascicular nucleus (Figs. 8-11) This nucleus presents some nomenclatural difficulties. The nucleus so described by Goldby (1941) corresponds to the nucleus of the same name in Didelphis (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967, 1968). However, a physiological study by Dennis & Kerr (1961) in Trichosurus found that the posterior portion of the subparafascicular nucleus received an anterolateral system input. They renamed this portion 'parageniculate nucleus'. Anatomical studies by Rockel et al. (1972) appeared to confirm these findings and these latter authors placed the 'parageniculate' with the posterior complex as the parageniculate component (Pop) of that functional grouping. The term 'parageniculate' is used by Ariens Kappers, Huber & Crosby (1936) to refer to the perigeniculate nucleus (Thuma, 1928) or pregeniculate nucleus (Rioch, 1929) in the cat, a region associated with the dorsal lateral geniculate nucleus. In view of this situation we feel that the name 'parageniculate' is best avoided and so we have retained Goldby's usage. Pretectal nucleus (Figs. 8-11) This region presents no interpretative problems, appearing similar in Didelphis and most other mammals. Medial geniculate nucleus (Figs. 10, 11) Apart from differences in terminology our description of the medial geniculate nucleus corresponds in essential detail to those of other authors for both Trichosurus (Goldby, 1941; Rockel et al. 1972) and Didelphis (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967). In agreement with Rockel et al. (1972) we have divided the medial geniculate into internal and principal subnuclei, following the description by Tarlov & Moore (1966) of this region in the rabbit. According to these latter authors their parcellation corresponds to the magnocellular and principal divisions of the cat medial geniculate (Rioch, 1929; Moore & Goldberg, 1963).
Lateral geniculate nuclei (Figs. 7-11) We can add little to the comprehensive description of the Trichosurus lateral geniculate presented by Hayhow (1967). In comparison with Didelphis it should be noted that Trichosurus does display a distinct cellular lamination of the dorsal lateral geniculate nucleus, a feature not present in Didelphis, but found in several other, but not all, diprotodontid marsupials (Johnson & Marsh, 1969).
Thalamus of Trichosurus
243
SUMMARY
In several respects the dorsal thalamus of Trichosurus presents a level of organizational complexity considerably in advance of that seen in Didelphis. In particular, such features as the lamination of the dorsal lateral geniculate, the distinct subdivisions of the ventroposterior and lateroposterior complexes, and the more pronounced separation of the ventroanterior from the ventrolateral nucleus, are similar to conditions found in many eutherians. On the other hand, some features which Trichosurus shares with Didelphis, such as the lack of a median central nucleus, and the well developed midline nuclei, are usually said to be indicative of a more 'primitive' level of neural organization. In most instances the thalamic nuclei in Trichosurus are easily homologized with those of Didelphis and other mammals. The difficult areas are the lateral and posterior groups of nuclei, regions which have generally been troublesome in most mammals thus far examined. What does become apparent after this examination of the Trichosurus thalamus is that this representative of the diprotodontid radiation has produced some neurological features which strikingly parallel those of certain advanced eutherians while retaining other features generally considered to be generalized and primitive. Within the metatheria Trichosurus represents a considerable advance over Didelphis. However, as will be seen in later papers in this series, there are other features, particularly those of thalamocortical fibre distribution, which serve to set Trichosurus quite markedly apart from both Didelphis and at least certain eutherian mammals (Haight & Neylon, 1977b, c, 1978).
This work was supported in part by the Australian Research Grants Committee, Grant D1-73/15220. We thank the Tasmanian National Parks and Wildlife Service for permission to take the possums we needed, and we also thank colleagues at the University of New South Wales and the Flinders University of South Australia for providing a selection of possums for comparison with the Tasmanian variety. To Professor George Martin and Dr Paula Wilson go particular thanks for their helpful comments on the manuscript. Finally, we wish to thank Miss Denise Wise for her photographic assistance and the many other colleagues whose comments and criticisms, both upon the study and the resultant manuscript, were of the utmost help. AD AM AV C CD
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ABBREVIATIONS LI Laterointermediate nucleus LP Lateroposterior nucleus LPL Lateral lateroposterior nucleus
Anterodorsal nucleus Anteromedial nucleus Anteroventral nucleus Central nucleus Caudate nucleus centrolateral nucleus cerebral peduncle Central tegmental field Epiphysis Extrageniculate nucleus external medullary lamina fornix Habenular nuclei Interoanterodorsal nucleus internal capsule Lateroanterior nucleus Lateral geniculate nucleus Dorsal lateral geniculate nucleus Ventral lateral geniculate nucleus
LPM MB MD MG
Medial lateroposterior nucleus
ot
optic tract
Mammillary body
Mediodorsal nucleus Medial geniculate nucleus MGi Internal division, medial geniculate nucleus MGp Principal division, medial geniculate nucleus medial lemniscus mI ms medullary stria mammillothalamic tract mt oc optic chiasma
PAG Periaquaductal grey matter PC Paracentral nucleus posterior commissure pc I6-2
244 PF PO PR PT PV rf RN RT RU SC SG
J. R. HAIGHT AND L. NEYLON
Parafascicular nucleus Posterior nucleus Pretectal nucleus Paratenial nucleus Paraventricular nucleus retroflex fasciculus Red nucleus Reticular nucleus Reunient nucleus Superior colliculus Suprageniculate nucleus
SPF Subparafascicular nucleus SR Subthalamic reticular formation (= Zona incerta) VA Ventroanterior nucleus VL Ventrolateral nucleus VM Ventromedial nucleus VP Ventroposterior nucleus (= Ventrobasal nucleus) VPL Lateral ventroposterior nucleus VPM Medial ventroposterior nucleus VPP Posteromedial ventroposterior nucleus REFERENCES
ARIENs KAPPERS, C. U., HUBER, G. C. & CROSBY, E. C. (1936). The Comparative Anatomy of the Nervous System of Vertebrates, Including Man, vol. ii, p. 1157. Reprinted by Hafner, New York, 1965. BODIAN, D. (1939). Studies on the diencephalon of the Virginia opossum. Part I. The nuclear pattern in the adult. Journal of Comparative Neurology 71, 259-324. BODIAN, D. (1942). Studies on the diencephalon of the Virginia opossum. Part III. The thalamo-cortical projection. Journal of Comparative Neurology 77, 525-575. CARMEL, P. W. (1970). Efferent projections of the ventral anterior nucleus of the thalamus in the monkey. American Journal of Anatomy 128, 159-184. DENNIS, B. J. & KERR, D. I. B. (1961). Somaesthetic pathways in the marsupial phalanger, Trichosurus vulpecula. Australian Journal of Experimnental Biology 39, 29-42. DIAMOND, I. T. & UTLEY, J. D. (1963). Thalamic retrograde degeneration study of sensory cortex in opossum. Journal of Comparative Neurology 120, 129-160. GERGEN, J. A. & MACLEAN, P. D. (1962). A stereotaxic atlas of the squirrel monkey's brain (Saimiri sciureus). U.S. Department of Health, Education and Welfare, Public Health Service Publication no. 933. GOLDBY, F. (1941). The normal histology of the thalamus in the phalanger, Trichosurus vulpecula. Journal of Anatomy 75, 197-224. GOLDBY, F. (1943). An experimental study of the thalamus in the phalanger, Trichosurus vulpecula. Journal of Anatomy 77, 195-224. HAIGHT, J. R. & NEYLON, L. (1977a). A variably present cell mass in the ventroposterior thalamic complex of the brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 124, 530. HAIGHT, J. R. & NEYLON, L. (1977b). Neocortical projections of the ventroanterior thalamic nucleus in the brush-tailed possum, Trichosurus vulpecula. Journal of Anatormy 124, 531. HAIGHT, J. R. & NEYLON, L. (1977 c). A craniocaudal gradient of representational overlap in the motorsomatic sensory neocortex of the brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 124, 531. HAIGHT, J. R. & NEYLON, L. (1978). The organization of neocortical projections from the ventroposterior thalamic complex in the marsupial brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 126, 458-484. HAIGHT, J. R., NEYLON, L. & WELLER, W. L. (1976). Horseradish peroxidase determination of thalamocortical projections in the brush-tailed possum, Trichosurus vulpecula. Journal ofAnatomy 121, 416-417. HAYHOW, W. R. (1967). The lateral geniculate nucleus of the marsupial phalanger, Trichosurus vulpecula. An experimental study of cytoarchitecture in relation to the intranuclear optic nerve projection fields. Journal of Comparative Neurology 131, 571-604. JASPER, H. H. & AJMONE-MARSAN, C. (1954). A Stereotaxic Atlas of the Diencephalon of the Cat. Ottawa: The National Research Council of Canada. JOHNSON, J. I. & MARSH, M. P. (1969). Laminated lateral geniculate in the nocturnal marsupial Petaurus breviceps (sugar glider). Brain Research 15, 250-254. LOCKE, S. & KERR, C. (1973). The projection of nucleus lateralis dorsalis of monkey to basomedial temporal cortex. Journal of Comparative Neurology 149, 29-42. MEHLER, W. R. (1969). Some neurological species differences - A posteriori. Annals of the New York Academy of Sciences 167, 424-468. MOORE, R. Y. & GOLDBERG, J. M. (1963). Ascending projections of the inferior colliculus in the cat. Journal of Comparative Neurology 121, 109-135. NEYLON, L. & HAIGHT, J. R. (1977). Neocortical projections of the ventromedial thalamic nucleus in the brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 124, 530. Nomina Anatomica (1966). 3rd ed. Amsterdam: Excerpta Medica Foundation. OLSZEWSKI, J. (1952). The Thalamus of the Macaca mulatta: An Atlas for Use with the Stereotaxic Instrument. Basel: S. Karger. OSWALDO-CRUZ, E. & ROCHA-MIRANDA, C. E. (1967). The diencephalon of the opossum in stereotaxic coordinates. I. The epithalamus and dorsal thalamus. Journal of Comparative Neurology 129, 1-38.
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245
OSWALDO-CRUZ, E. & RocHA-MIRANDA, C. E. (1968). The Brain ofthe Opossum (Didelphis marsupialis). A Cytoarchitectonic Atlas in Stereotaxic Coordinates. Instituto de biofisica, Universidade Federal do Rio de Janeiro. PUBOLS, B. H. (1968). Retrograde degeneration study of somatic sensory thalamo-cortical connections in brain of Virginia opossum. Brain Research 7, 232-251. PUBOLs, B. H. & PUBOLs, L. M. (1966). Somatic sensory representation in the thalamic ventrobasal complex of the Virginia opossum. Journal of Comparative Neurology 127, 19-34. RINVIK, E. (1968). A re-evaluation of the cytoarchitecture of the ventral nuclear complex of the cat's thalamus on the basis of corticothalamic connections. Brain Research 8, 237-254. RIOCH, D. McK. (1929). Studies on the diencephalon of carnivora. Part I. The nuclear configuration of the thalamus, epithalamus, and hypothalamus of the dog and cat. Journal of Comparative Neurology 49, 1-153. ROCKEL, A. J., HEATH, C. J. & JONES, E. G. (1972). Afferent connections to the diencephalon in the marsupial phalanger and the question of sensory convergence in the 'posterior group' of the thalamus. Journal of Comparative Neurology 145, 105-130. SOUSA, A. P. B., OSWALDO-CRUZ, E. & GATTASS, R. (1971). Somatotopic organization and response properties of neurons of the ventrobasal complex in the opossum. Journal of Comparative Neurology 142, 231-248. TARLOV, E. V. & MOORE, R. Y. (1966). The tecto-thalamic connections in the brain of the rabbit. Journal of Comparative Neurology 126, 403-422. THUMA, B. D. (1928). Studies on the diencephalon of the cat. I. The cytoarchitecture of the corpus geniculatum laterale. Journal of Comparative Neurology 46, 173-200. WALKER, A. E. (1938). The Primate Thalamus. Chicago: University of Chicago Press. WALSH, T. M. & EBNER, F. F. (1973). Distribution of cerebellar and somatic lemniscal projections in the ventral nuclear complex of the Virginia opossum. Journal of Comparative Neurology 147, 427-446.
225
With 11 figures Printed in Great Britain
An atlas of the dorsal thalamus of the marsupial brush-tailed possum, Trichosurus vulpecula J. R. HAIGHT AND L. NEYLON*
Department of Anatomy, University of Tasmania, Box 252C, GPO, Hobart, Tasmania 7001, Australia
(Accepted 7 March 1977) INTRODUCTION
For our work on thalamocortical relationships in Trichosurus we required detailed knowledge of the nuclear and cytoarchitectural organization of its dorsal thalamus, but we soon realized that a description adequate for our purpose did not exist. Goldby's (1941) account of the possum thalamus is an excellent general introduction, but has illustrative limitations and employs nomenclature which to some extent has been superseded. Rockel, Heath & Jones (1972) and Hayhow (1967) have described certain areas in some detail, but a comprehensive analysis is lacking. The Australian Trichosurus occupies an important position in comparative anatomy. A diprotodontid marsupial akin to the kangaroos, wallabies, wombats and the koala, this possum (or phalanger) is representative of the more advanced of the two major lines of Australian marsupial radiation. Within the metatherian subclass, Trichosurus is far removed from the stem marsupial line, of which living members of the American genus, Didelphis, are often taken as representative. As will be seen, the thalamus of the Australian brush-tailed possum differs in many respects from that of the American opossums as described by Bodian (1939) and Oswaldo-Cruz & Rocha-Miranda (1967, 1968). The atlas is not presented with stereotaxic coordinates. There are two reasons for this. First, Trichosurus exhibits considerable variation in body size. The Tasmanian possums used in this study are, with an average body weight of 3-2 kg, the largest representatives of their species. Possums inhabiting the warmer and drier areas of Australia tend to be much less massive, averaging 2 kg or less. These differences are reflected in skull and brain size (see Table 1). Brain weights of adult animals can range from 7-8 to 14'6 g. Second, there is inconsistency of internal organization within the possum thalamus (Haight & Neylon, 1977a); a significant minority (c. 35 %) of possums collected in Tasmania displayed an arrangement of thalamic nuclei sufficiently different from the norm to defeat any attempts at precise stereotaxic generalization. Such intraspecies variability makes a well illustrated atlas all the more necessary in order that those interested in working with this animal are aware of the 'normal' condition and can use the information to locate and identify the sometimes displaced and distorted nuclei. MATERIALS AND METHODS
The brains of three normal possums were used to compile this atlas. An additional 40 'experimental' thalami were referred to in order to confirm our assessments of * Present address: Department of Therapy, Western Australian Institute of Technology, Selby Street, Shenton Park, Western Australia 6008. IS
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Table 1. Comparison of body weights, brain weights and skull sizes in Trichosurus gathered from three areas of South Eastern Australia
Locality Adelaide, South Australia Sydney, New South Wales Hobart, Tasmania
Skull measurements , I Average bizygoAverage matic width basilar length mm (N) mm (N) 49-2 (14) 72-9 (14)
Average body weight kg (N) 1-6 (14)
Average brain weight g (N) 9-4 (14)
2-3 (20)
11-1 (20)
52-8 (9)
77-3 (9)
3-2 (56)
13 0 (23)
55-9 (12)
84-7 (12)
nuclear boundaries and configuration. All animals, normal and experimental, were captured in southern Tasmania between mid-1974 and mid-1976. Body weights ranged from 2-1 to 4 5 kg with a mean value of 3-2 kg. On average, males were 0 3 kg heavier than females. The normal possums were anaesthetized and perfused intracardially with 0-9 % saline solution followed by 10 % formol saline. In two cases the brains were embedded in celloidin and sectioned at 30 ,um, one in the coronal and the other in the sagittal plane. Alternate sections were stained for myelin using the Weil technique, and for cell bodies using warm aqueous thionin. Both series were mounted in Depex (Gurr). The remaining normal brain was embedded in egg yolk, frozen and sectioned coronally at 50 ,um, the sections being stained with aqueous thionin and mounted in Depex. Experimental animals were perfused with saline followed by a paraformaldehyde-glutaraldehyde mixture (Haight & Neylon, 1978). These thalami were sectioned, either in the coronal or sagittal plane at 40-60 ,tm, and certain sections stained with aqueous thionin while others were processed to demonstrate the retrograde transport of horseradish peroxidase from cortex to thalamus. These experimental thalami were also used to define nuclear boundaries where applicable. Thionin-stained sections prepared by the different methods were compared to ascertain whether significant differences in cell shape and staining properties were apparent. It was found that the celloidin technique produced more tissue shrinkage, otherwise the methods produced comparable results except that the staining quality and hence the photographic results were superior in the celloidin material. The atlas presented here consists of ten photographs with corresponding outline diagrams of the one normal, celloidin embedded and coronally sectioned brain. A Leitz Aristophot system was used to photograph the sections, using Kodak Plus-X pan sheet film, heavily orange filtered. The negatives were printed on high contrast Ilford F-4 paper. We have been conservative in nomenclature, contenting ourselves with bringing Goldby's (1941) treatment up to date. Where it was necessary to differ from Goldby we have usually accepted the usage of Rockel et al. (1972); exceptions are clearly indicated in the text. We have chosen to render this atlas in English, rather than employ a hybrid English-Latin neurological nomenclature. In doing this we have attempted to conform, where possible, to the standards laid down in the Nomina Anatomica (1966).
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The ten photographs were selected in order to point out the major features of the Trichosurus dorsal thalamus. The sections shown are not spaced at equal intervals but are irregularly spaced in accordance with the degree of change and the complexity of a given region. The levels of section are shown in Figure 1, which also gives an indication of the anteroposterior extent of selected thalamic nuclei. The notes and comments which follow compare our observations with those of other workers, in particular Goldby (1941) and Rockel et al. (1972). These comments are primarily restricted to matters of nomenclature and the 'lumping and splitting' of various nuclei and subnuclei, but they also point out differences between thalamus of Trichosurus and that of the American didelphids (as described by Bodian, 1939 and Oswaldo-Cruz & Rocha-Miranda, 1967, 1968). Detailed anatomical descriptions are provided only where previously undescribed regions are being considered or where difficulties arise in determining homologues between Trichosurus and Didelphis. Midline and intralaminar nuclei (Figs. 2-8) Though our general interpretation of these regions is in agreement with that of Goldby (1941), several points of divergence emerge when Trichosurus is compared with Didelphis. We include the region of the rhomboidal nucleus (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967, 1968) with the central nucleus because, like Goldby, we feel that the two regions are not sufficiently distinct to warrant separation in Trichosurus. Similarly, the reunient nucleus in Trichosurus includes the region described as the subparatenial nucleus in Didelphis. A separate centrolateral nucleus has not been recognized in Didelphis, this region apparently being considered a part of the paracentral nucleus (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967). I5-2
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Like Goldby, we feel that the two regions are cytoarchitecturally distinct and have therefore retained them as separate nuclei. Bodian, and Oswaldo-Cruz & RochaMiranda also describe, separately, a parafascicular and a posterolateral parafascicular nucleus. The latter appears to correspond to the parafascicular nucleus of Trichosurus while the former, on positional and cytoarchitectural criteria, may be equivalent to part of the intralaminar complex. In neither animal does the parafascicular (posterolateral parafascicular?) nucleus enlarge to form a distinct median central nucleus as it does in many eutherian mammals. Finally, in Trichosurus we do not distinguish a separate intermediodorsal nucleus as described in Didelphis. This region, comparatively very much smaller in Trichosurus than in Didelphis, corresponds to what we and Goldby include as the median seam of the paraventricular nucleus. Anterior nuclei (Figs. 2-5) This group of nuclei includes the anterodorsal, the interanterodorsal, the anteroventral and the anteromedial nuclei and is similarly organized in Trichosurus and Didelphis. Lateral nuclei (Figs. 4-11) The lateral nuclear complex of Trichosurus corresponds in most particulars with that described for Didelphis by both Bodian (1939) and Oswaldo-Cruz & RochaMiranda (1967, 1968) and differs, in our interpretation, from that proposed by Goldby (1941) for Trichosurus. Goldby divided the lateral tier into three major regions: an anterior 'Lateralis A', a ventral 'Lateralis B', and a posterior lateroposterior nucleus. Within 'Lateralis A' he recognized, but did not accord separate nuclear status to, a small group of cells which corresponds to our lateroanterior nucleus and, very probably, to the nucleus of the same name in Didelphis. The remainder of his 'Lateralis A' corresponds to our laterointermediate nucleus. Goldby's 'Lateralis B' was reassigned by Rockel et al. (1972) to the posterior nuclear complex (their nucleus Pob) as a result of their experimental findings. Accordingly, we have named this nucleus the posterior nucleus, wishing to note that only the name is changed; the position and nuclear boundaries being as Goldby described them. If homology of the laterointermediate and of the lateroposterior nuclei of Trichosurus and Didelphis is assumed, then these nuclei present internal differences in the two animals. The laterointermediate nucleus in Didelphis is divided into distinct dorsal and ventral regions by Oswaldo-Cruz & Rocha-Miranda (1967) but not by Bodian (1939). In Trichosurus the laterointermediate nucleus is cytoarchitecturally homogeneous. With the lateroposterior nucleus the reverse situation is present. In Didelphis no cytoarchitectural division into lateral and medial subnuclei has been described, whereas in Trichosurus such a division may be distinguished readily. The laterointermediate nucleus of these two marsupials is particularly difficult to place within the lateral nuclear complex of placental mammals. Oswaldo-Cruz & Rocha-Miranda (1967) remark that the marsupial laterointermediate nucleus may correspond to the laterodorsal nucleus of the cat. Retrograde degeneration studies of the thalamus after cortical ablations in both Trichosurus (Goldby, 1943) and Didelphis (Bodian, 1942; Diamond & Utley, 1963; Pubols, 1968) indicate a projection to the posterior parietal and peristriate cortical areas. In the macaque, however, the same experimental procedures indicate a laterodorsal nuclear projection to the basomedial temporal cortex (Locke & Kerr, 1973), a finding which would tend not to support the idea of homology between the eutherian laterodorsal and the metatherian laterointermediate nuclei. Further complicating the issue are our own
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(unpublished) findings, based upon the retrograde transport of horseradish peroxidase, which suggest that the peristriate and parietal cortices do not receive projections from the laterointermediate nucleus in Trichosurus. We are as yet unable to determine whether this nucleus projects to the basomedial cortex and are therefore unable to comment on the findings of Locke & Kerr. Medial nuclei Paratenial nucleus (Figs. 2-5) Though Goldby (1941) did not recognize any cytoarchitectural subdivisions in this nucleus, our material displays medial and lateral subdivisions. In this respect Trichosurus is similar to Didelphis (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967).
Mediodorsal nucleus (Figs. 5-7) Goldby (1941) recognized three subdivisions, basing his observations upon regional differences in myeloarchitecture and cell size. We do not consider these regional differences sufficiently reproducible from animal to animal to warrant separating them. Our interpretation is similar to that described by Bodian (1939) and OswaldoCruz & Rocha-Miranda (1967) in Didelphis. Ventral nuclei Ventroanterior nucleus (Figs. 4, 5) As with many eutherians (cat, Jasper & Ajmone-Marsan, 1954; squirrel monkey, Gergen & MacLean, 1962; macaque monkey, Olszewski, 1952, Walker, 1938), the ventroanterior nucleus is cytoarchitecturally distinct from the ventrolateral nucleus, a condition that is not as pronounced in the American opossum (Oswaldo-Cruz & Rocha-Miranda, 1967; Walsh & Ebner, 1973). Bodian's (1939) description of the opossum ventral nuclei is at variance with more recent treatments which tend to emphasize the similarities of this region in Didelphis with other mammals. We have not attempted to reconcile his interpretation with those of later workers. The cytoarchitecture of VA in Trichosurus appears to correspond closely to that described in the extreme anterior portion of the ventroanterior-ventrolateral complex (VAL) in the opossum (Oswaldo-Cruz & Rocha-Miranda, 1968). Of interest is the fact that the cortical projection of the ventroanterior nucleus in monkeys is to frontal and prefrontal regions (Carmel, 1970) while we have observed in Trichosurus that the cortical projection of this nucleus is primarily restricted to the parietal region (Haight & Neylon, 1977b). Ventrolateral nucleus (Figs. 4-6) Our ventrolateral nucleus corresponds to Goldby's ventrointermediate nucleus. Experimental evidence indicates that this region is similar to the ventrolateral nucleus in eutherian mammals, and it has been renamed accordingly (Haight & Neylon, 1977 c; Haight et al. 1976; Rockel et al. 1972). As noted above, the ventrolateral and ventroanterior nuclei in Didelphis are not clearly separable (Oswaldo-Cruz & RochaMiranda, 1967; Walsh & Ebner, 1973). Ventroposterior nucleus (Figs. 7-10) Goldby (1941) divided the ventroposterior complex into three cell groups; a dorsomedial group, which he thought might be equivalent to a 'submedius' nucleus;
J. R. HAIGHT AND L. NEYLON 240 a ventrolateral group; and, separating these two, a 'well defined condensation' or 'central core' of smaller cells. The ventroposterior nucleus, as defined in this paper and by Rockel et al. (1972), does not include Goldby's dorsomedial or 'submedius' division which, though not illustrated by him, probably corresponds to the ventromedial nucleus. The remaining 'central core' and ventrolateral parts of the complex correspond with the medial and lateral (VPM and VPL or trigeminal and lemniscal) divisions recognized in some eutherian mammals. This interpretation has been verified experimentally on the basis of VP's input (Rockel et al. 1972) and output connexions (Haight & Neylon, 1978; Haight et al. 1976). In Didelphis the ventroposterior complex is functionally divided into lemniscal and trigeminal zones (Pubols & Pubols, 1966; Sousa, Oswaldo-Cruz & Gattass, 1971; Walsh & Ebner, 1973) although a cytoarchitectural distinction is not obvious (Oswaldo-Cruz & Rocha-Miranda, 1967, 1968; Sousa et al. 1971). Hence, in this respect Trichosurus resembles certain specialized eutherians more than its generalized metatherian relative. The posteromedial subdivision of VP (our VPP) has not previously been described in Trichosurus although Rockel et al. (1972) include this region in the ventromedial nucleus (see their Fig. 4). On cytoarchitectural grounds this subnucleus is distinct from VM and is functionally associated with the VP complex (Haight & Neylon, 1978). VPP cells are large and of uniform size (see Table 2). They stain deeply and, between different individuals, exhibit considerable variation in packing density, ranging from a loose collection of a few cells visible in any one section to a distinct and well-formed subnucleus (Figs. 6, 7). In 21 % of the thalami examined VPP could not be distinguished (Haight & Neylon, 1977 a). Olszewski (1952) described a medial, small-celled or parvocellular subdivision of VPM (VPMpc) in the macaque. The similarly named region in the cat contains, in addition to small cells, many larger, deeply staining cells (Rinvik, 1968). The uniform large size and variable occurrence of VPP cells in Trichosurus distinguishes this subnucleus from VPMpc in the cat and monkey; however, the positional relationships of VPP and VPMpc are similar. No apparent equivalent of VPP is evident in Didelphis. Ventromedial nucleus (Figs. 5-9) Though not specifically mentioned by Goldby in the original description of the Trichosurus thalamus, the ventromedial nucleus, or a portion thereof, may have been included in his 'dorsomedial' or 'submedius' division of the ventroposterior complex. However, in a later paper Goldby (1943) separated the posterior portion of the anteromedial nucleus from the main body of that nucleus and gave it the name 'nucleus ventralis, pars medialis.' Our studies of the cortical projection of the ventromedial nucleds (Neylon & Haight, 1977) indicate that this region is not a part of VM and we have left it with the anteromedial nucleus. The ventromedial nuclei of Trichosurus and Didelphis are similar.
Posterior thalamus and metathalamus Posterior nucleus (Figs. 7-10) The posterior nucleus described here corresponds to Goldby's 'Lateralis B' nucleus, a nucleus regarded by Rockel et al. (1972) as being part of the posterior functional complex on the basis of its afferent connexions. In Trichosurus the nucleus is located between the lateral nuclear complex dorsally and the ventroposterior
Thalamus of Trichosurus
241
Table 2. A comparison of neuron size in VPP with neighbouring regions Region VPP VPM VPL VM
Neuron diameters Average diameter (#m) (range in,tm) 22-5 21-23 16-5 13-20 18-9 16-21 20-0 18-23
complex ventrally and is separated laterally from the medial geniculate nucleus by the medial lemniscus. The posterior nucleus of Didelphis is difficult to compare with that of Trichosurus. Oswaldo-Cruz & Rocha-Miranda (1967) describe a posterior nucleus which appears largely to correspond to the posterior Junctional complex in that animal (Mehler, 1969; Pubols & Pubols, 1966; Sousa et al. 1971). In contrast to Trichosurus, the Didelphis posterior nucleus is related anatomically to the medial geniculate nucleus, lying dorsal and lateral to the medial lemniscus. In the anatomical position of the Trichosurus posterior nucleus, Didelphus has a distinct cell group, 'Nucleus C' (Oswaldo-Cruz & Rocha-Miranda, 1967), which largely separates the posterior nucleus from the ventroposterior complex. The functional properties of cells in 'Nucleus C' suggest a possible association with the posterior functional complex (Sousa et al. 1971). From these data it would be tempting to homologize the opossum 'Nucleus C' with the possum posterior nucleus. However, this creates difficulties in comparing the large opossum posterior nucleus with similarly located structures in Trichosurus. Until further data are available, a meaningful comparison of this area in the two animals is not possible.
Suprageniculate nucleus (Figs. 8-11) This nucleus corresponds to that described by Goldby (1941) and to the suprageniculate component of the posterior complex (Pos) of Rockel et al. (1972). Portions of the Trichosurus suprageniculate nucleus may be included as part of the posterior nucleus in Didelphis.
Extrageniculate nucleus (Figs. 8-10) This region has not been previously described in Trichosurus. The nucleus is small and, except in well prepared and stained material, can be difficult to distinguish. The extrageniculate nucleus of EG is related to the anterior pole of the medial geniculate nucleus. Anteriorly, the nucleus appears to form a ventral extension of the lateroposterior nucleus between the medial lemniscus and the fibres of the external medullary lamina and optic tract. The rostral pole of the medial geniculate becomes encapsulated between the medial lemniscus and extrageniculate nucleus which then forms an indistinct, narrow crescent of cells over the lateral and ventral aspects of the principal division of the medial geniculate. Posteriorly, the ventral extremity of the crescent is continuous beneath the medial lemniscus and connects with the ventroposterior complex. The cells of the extrageniculate nucleus are of medium size and are highly variable in shape. Many are fusiform and are oriented parallel to the fibre tracts which partially surround the nucleus. Anteriorly, they are distinguished with difficulty from cells of the lateroposterior nucleus. Further, a distinction, based solely upon I6
A NA 126
J. R. HAIGHT AND L. NEYLON 242 cytoarchitectural criteria, between the principal division of the medial geniculate nucleus and the extrageniculate nucleus can be difficult to make. However, the extrageniculate nucleus cells are usually less heavily stained than those of the medial geniculate and often a thin fibrous lamina can be distinguished separating the two nuclei. Though the afferent relationships of the extrageniculate nucleus have not been determined, the region is clearly distinguished by its projection to the superomarginal aspect of the parietal cortex, a feature which renders the extrageniculate nucleus quite distinct from its neighbouring thalamic nuclei (Haight & Neylon, unpublished observations).
Subparafascicular nucleus (Figs. 8-11) This nucleus presents some nomenclatural difficulties. The nucleus so described by Goldby (1941) corresponds to the nucleus of the same name in Didelphis (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967, 1968). However, a physiological study by Dennis & Kerr (1961) in Trichosurus found that the posterior portion of the subparafascicular nucleus received an anterolateral system input. They renamed this portion 'parageniculate nucleus'. Anatomical studies by Rockel et al. (1972) appeared to confirm these findings and these latter authors placed the 'parageniculate' with the posterior complex as the parageniculate component (Pop) of that functional grouping. The term 'parageniculate' is used by Ariens Kappers, Huber & Crosby (1936) to refer to the perigeniculate nucleus (Thuma, 1928) or pregeniculate nucleus (Rioch, 1929) in the cat, a region associated with the dorsal lateral geniculate nucleus. In view of this situation we feel that the name 'parageniculate' is best avoided and so we have retained Goldby's usage. Pretectal nucleus (Figs. 8-11) This region presents no interpretative problems, appearing similar in Didelphis and most other mammals. Medial geniculate nucleus (Figs. 10, 11) Apart from differences in terminology our description of the medial geniculate nucleus corresponds in essential detail to those of other authors for both Trichosurus (Goldby, 1941; Rockel et al. 1972) and Didelphis (Bodian, 1939; Oswaldo-Cruz & Rocha-Miranda, 1967). In agreement with Rockel et al. (1972) we have divided the medial geniculate into internal and principal subnuclei, following the description by Tarlov & Moore (1966) of this region in the rabbit. According to these latter authors their parcellation corresponds to the magnocellular and principal divisions of the cat medial geniculate (Rioch, 1929; Moore & Goldberg, 1963).
Lateral geniculate nuclei (Figs. 7-11) We can add little to the comprehensive description of the Trichosurus lateral geniculate presented by Hayhow (1967). In comparison with Didelphis it should be noted that Trichosurus does display a distinct cellular lamination of the dorsal lateral geniculate nucleus, a feature not present in Didelphis, but found in several other, but not all, diprotodontid marsupials (Johnson & Marsh, 1969).
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SUMMARY
In several respects the dorsal thalamus of Trichosurus presents a level of organizational complexity considerably in advance of that seen in Didelphis. In particular, such features as the lamination of the dorsal lateral geniculate, the distinct subdivisions of the ventroposterior and lateroposterior complexes, and the more pronounced separation of the ventroanterior from the ventrolateral nucleus, are similar to conditions found in many eutherians. On the other hand, some features which Trichosurus shares with Didelphis, such as the lack of a median central nucleus, and the well developed midline nuclei, are usually said to be indicative of a more 'primitive' level of neural organization. In most instances the thalamic nuclei in Trichosurus are easily homologized with those of Didelphis and other mammals. The difficult areas are the lateral and posterior groups of nuclei, regions which have generally been troublesome in most mammals thus far examined. What does become apparent after this examination of the Trichosurus thalamus is that this representative of the diprotodontid radiation has produced some neurological features which strikingly parallel those of certain advanced eutherians while retaining other features generally considered to be generalized and primitive. Within the metatheria Trichosurus represents a considerable advance over Didelphis. However, as will be seen in later papers in this series, there are other features, particularly those of thalamocortical fibre distribution, which serve to set Trichosurus quite markedly apart from both Didelphis and at least certain eutherian mammals (Haight & Neylon, 1977b, c, 1978).
This work was supported in part by the Australian Research Grants Committee, Grant D1-73/15220. We thank the Tasmanian National Parks and Wildlife Service for permission to take the possums we needed, and we also thank colleagues at the University of New South Wales and the Flinders University of South Australia for providing a selection of possums for comparison with the Tasmanian variety. To Professor George Martin and Dr Paula Wilson go particular thanks for their helpful comments on the manuscript. Finally, we wish to thank Miss Denise Wise for her photographic assistance and the many other colleagues whose comments and criticisms, both upon the study and the resultant manuscript, were of the utmost help. AD AM AV C CD
CL Cp CTF E
EG eml fx HB IAD ic LA LG
LGd LGv
ABBREVIATIONS LI Laterointermediate nucleus LP Lateroposterior nucleus LPL Lateral lateroposterior nucleus
Anterodorsal nucleus Anteromedial nucleus Anteroventral nucleus Central nucleus Caudate nucleus centrolateral nucleus cerebral peduncle Central tegmental field Epiphysis Extrageniculate nucleus external medullary lamina fornix Habenular nuclei Interoanterodorsal nucleus internal capsule Lateroanterior nucleus Lateral geniculate nucleus Dorsal lateral geniculate nucleus Ventral lateral geniculate nucleus
LPM MB MD MG
Medial lateroposterior nucleus
ot
optic tract
Mammillary body
Mediodorsal nucleus Medial geniculate nucleus MGi Internal division, medial geniculate nucleus MGp Principal division, medial geniculate nucleus medial lemniscus mI ms medullary stria mammillothalamic tract mt oc optic chiasma
PAG Periaquaductal grey matter PC Paracentral nucleus posterior commissure pc I6-2
244 PF PO PR PT PV rf RN RT RU SC SG
J. R. HAIGHT AND L. NEYLON
Parafascicular nucleus Posterior nucleus Pretectal nucleus Paratenial nucleus Paraventricular nucleus retroflex fasciculus Red nucleus Reticular nucleus Reunient nucleus Superior colliculus Suprageniculate nucleus
SPF Subparafascicular nucleus SR Subthalamic reticular formation (= Zona incerta) VA Ventroanterior nucleus VL Ventrolateral nucleus VM Ventromedial nucleus VP Ventroposterior nucleus (= Ventrobasal nucleus) VPL Lateral ventroposterior nucleus VPM Medial ventroposterior nucleus VPP Posteromedial ventroposterior nucleus REFERENCES
ARIENs KAPPERS, C. U., HUBER, G. C. & CROSBY, E. C. (1936). The Comparative Anatomy of the Nervous System of Vertebrates, Including Man, vol. ii, p. 1157. Reprinted by Hafner, New York, 1965. BODIAN, D. (1939). Studies on the diencephalon of the Virginia opossum. Part I. The nuclear pattern in the adult. Journal of Comparative Neurology 71, 259-324. BODIAN, D. (1942). Studies on the diencephalon of the Virginia opossum. Part III. The thalamo-cortical projection. Journal of Comparative Neurology 77, 525-575. CARMEL, P. W. (1970). Efferent projections of the ventral anterior nucleus of the thalamus in the monkey. American Journal of Anatomy 128, 159-184. DENNIS, B. J. & KERR, D. I. B. (1961). Somaesthetic pathways in the marsupial phalanger, Trichosurus vulpecula. Australian Journal of Experimnental Biology 39, 29-42. DIAMOND, I. T. & UTLEY, J. D. (1963). Thalamic retrograde degeneration study of sensory cortex in opossum. Journal of Comparative Neurology 120, 129-160. GERGEN, J. A. & MACLEAN, P. D. (1962). A stereotaxic atlas of the squirrel monkey's brain (Saimiri sciureus). U.S. Department of Health, Education and Welfare, Public Health Service Publication no. 933. GOLDBY, F. (1941). The normal histology of the thalamus in the phalanger, Trichosurus vulpecula. Journal of Anatomy 75, 197-224. GOLDBY, F. (1943). An experimental study of the thalamus in the phalanger, Trichosurus vulpecula. Journal of Anatomy 77, 195-224. HAIGHT, J. R. & NEYLON, L. (1977a). A variably present cell mass in the ventroposterior thalamic complex of the brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 124, 530. HAIGHT, J. R. & NEYLON, L. (1977b). Neocortical projections of the ventroanterior thalamic nucleus in the brush-tailed possum, Trichosurus vulpecula. Journal of Anatormy 124, 531. HAIGHT, J. R. & NEYLON, L. (1977 c). A craniocaudal gradient of representational overlap in the motorsomatic sensory neocortex of the brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 124, 531. HAIGHT, J. R. & NEYLON, L. (1978). The organization of neocortical projections from the ventroposterior thalamic complex in the marsupial brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 126, 458-484. HAIGHT, J. R., NEYLON, L. & WELLER, W. L. (1976). Horseradish peroxidase determination of thalamocortical projections in the brush-tailed possum, Trichosurus vulpecula. Journal ofAnatomy 121, 416-417. HAYHOW, W. R. (1967). The lateral geniculate nucleus of the marsupial phalanger, Trichosurus vulpecula. An experimental study of cytoarchitecture in relation to the intranuclear optic nerve projection fields. Journal of Comparative Neurology 131, 571-604. JASPER, H. H. & AJMONE-MARSAN, C. (1954). A Stereotaxic Atlas of the Diencephalon of the Cat. Ottawa: The National Research Council of Canada. JOHNSON, J. I. & MARSH, M. P. (1969). Laminated lateral geniculate in the nocturnal marsupial Petaurus breviceps (sugar glider). Brain Research 15, 250-254. LOCKE, S. & KERR, C. (1973). The projection of nucleus lateralis dorsalis of monkey to basomedial temporal cortex. Journal of Comparative Neurology 149, 29-42. MEHLER, W. R. (1969). Some neurological species differences - A posteriori. Annals of the New York Academy of Sciences 167, 424-468. MOORE, R. Y. & GOLDBERG, J. M. (1963). Ascending projections of the inferior colliculus in the cat. Journal of Comparative Neurology 121, 109-135. NEYLON, L. & HAIGHT, J. R. (1977). Neocortical projections of the ventromedial thalamic nucleus in the brush-tailed possum, Trichosurus vulpecula. Journal of Anatomy 124, 530. Nomina Anatomica (1966). 3rd ed. Amsterdam: Excerpta Medica Foundation. OLSZEWSKI, J. (1952). The Thalamus of the Macaca mulatta: An Atlas for Use with the Stereotaxic Instrument. Basel: S. Karger. OSWALDO-CRUZ, E. & ROCHA-MIRANDA, C. E. (1967). The diencephalon of the opossum in stereotaxic coordinates. I. The epithalamus and dorsal thalamus. Journal of Comparative Neurology 129, 1-38.
Thalamus of Trichosurus
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OSWALDO-CRUZ, E. & RocHA-MIRANDA, C. E. (1968). The Brain ofthe Opossum (Didelphis marsupialis). A Cytoarchitectonic Atlas in Stereotaxic Coordinates. Instituto de biofisica, Universidade Federal do Rio de Janeiro. PUBOLS, B. H. (1968). Retrograde degeneration study of somatic sensory thalamo-cortical connections in brain of Virginia opossum. Brain Research 7, 232-251. PUBOLs, B. H. & PUBOLs, L. M. (1966). Somatic sensory representation in the thalamic ventrobasal complex of the Virginia opossum. Journal of Comparative Neurology 127, 19-34. RINVIK, E. (1968). A re-evaluation of the cytoarchitecture of the ventral nuclear complex of the cat's thalamus on the basis of corticothalamic connections. Brain Research 8, 237-254. RIOCH, D. McK. (1929). Studies on the diencephalon of carnivora. Part I. The nuclear configuration of the thalamus, epithalamus, and hypothalamus of the dog and cat. Journal of Comparative Neurology 49, 1-153. ROCKEL, A. J., HEATH, C. J. & JONES, E. G. (1972). Afferent connections to the diencephalon in the marsupial phalanger and the question of sensory convergence in the 'posterior group' of the thalamus. Journal of Comparative Neurology 145, 105-130. SOUSA, A. P. B., OSWALDO-CRUZ, E. & GATTASS, R. (1971). Somatotopic organization and response properties of neurons of the ventrobasal complex in the opossum. Journal of Comparative Neurology 142, 231-248. TARLOV, E. V. & MOORE, R. Y. (1966). The tecto-thalamic connections in the brain of the rabbit. Journal of Comparative Neurology 126, 403-422. THUMA, B. D. (1928). Studies on the diencephalon of the cat. I. The cytoarchitecture of the corpus geniculatum laterale. Journal of Comparative Neurology 46, 173-200. WALKER, A. E. (1938). The Primate Thalamus. Chicago: University of Chicago Press. WALSH, T. M. & EBNER, F. F. (1973). Distribution of cerebellar and somatic lemniscal projections in the ventral nuclear complex of the Virginia opossum. Journal of Comparative Neurology 147, 427-446.
