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1% Showed Wide Receptive Fields, Or Bilat- Eral Representation Somatotopic Organization and Response Properties of Neurons of the Ventrobasal Complex in the Opossum ' AGLAI P. B. SOUSA,Z E. OSWALDO-CRUZ AND R. GATTASS 2 Departamento de Neurobiologia, Institvto de Bioflsica, 458 av. Pasteur, Rio de Janeiro, Brad ABSTRACT Thalamic responses to somatic stimulation were studied in 47 specimens of the South American opossum, D. marsupialis aurita. Topographic representation of the body surface in the ventrobasal complex was determined by recording unit cluster responses to natural stimulation in sodium pentobarbital anesthetised animals. The pattern of representation observed was similar to that reported in the North American subspecies and comparable to the findings in eutherian mammals. The analysis of single units recorded with extra-cellular microelectrodes showed that the great majority of neurons are place and modality specific. A predominance of skin (vs. deep) sensibility was observed. Units activated by displacement of hairs and vibrissae displayed receptive fields similar to those reported in higher mammals, Of the units isolated within the anatomical bound- aries of the ventrobasal complex only 1% showed wide receptive fields, or bilat- eral representation. None of the units could be activated by auditory stimulation. Neurons displaying wide, discontinuous or bilateral receptive fields showing auditory-somatic convergence were isolated in nucleus paraf ascicularis, subpara- fascicularis and in the Posterior group Using anatomical techniques it has been nervation density are related to a larger shown, in a wide variety of mammals, that voIume of thalamic tissue. components of the ventrobasal complex Single unit recording from this region in (xVB), as defined by Rose and Mount- cats showed that the neurons receiving castle ('52) are the main site of termina- lemniscal projections are place and modal- tion of the medial lemniscus. Recent ana- ity specific (Rose and Mountcastle, '54). tomical literature related to this problem Poggio and Mountcastle ('63) demon- was reviewed by Bowsher ('65). strated, by recording more than 1,000 units After the introduction of electrophysio- from the xVB in chronically denervated logical recording methods, a precise organi- monkeys, that this restricted input is not zation of the somatic sensory projections due to the use of anesthetic agents. within the anatomical boundaries of this In eutherian mammals results differing from this pattern have been occasionally nucleus was demonstrated in several spe- reported. Besides cortico-dependent neu- cies (rat: Angel, '64; Davidson, '65; Em- rons the ventrobasal complex has been mers, '65; rabbit: Rose and Mountcastle, shown to include elements that survive de- '52; Mountcastle et al., '52; raccoon: cortication (Clark and Powell, '53; Bava Welker and Johnson, '65; sheep: Cabral and Johnson, '71; rhesus monkey: Mount- et al., '66). They possibly represent the in- terneurons described in the posterolateral castle and Henneman, '52; cynomdogus xVB by Andersen et al. ('64). monkey : Albe-Fessard and Bowsher, '65; spider monkey: Pubols, '68). It was shown 1 This investigation was supported by Public Health Service Research grant NB 04651, from the National that the body surface is represented in a Institute of Neurological Diseases and Stroke; BNDE Contract FUNTEC-74 and Conselho de Pesquisas da circumscribed region within the ventro- U.F.R.J. basal complex. In this representation pe- ZFellow from the Conselho Nacional de Pesquisas. 3 Senior Researcher (Pesquisador Conferencista) ripheral regions displaying a greater in- Conselho Nacional de Pesquisas. J. COMP. NEUR., 142: 231-248. 23 1 232 A. P. B. SOUSA, E. OSWALDOCRUZ AND R. GATTASS By determining the site of termination neuroanatomical investigations (for a com- of the spinothalamic tract, it was shown plete review see Oswaldo-Cruz and Rocha- that the ventrobasal complex is not the Miranda, '68). The morphological features only region receiving somatic projections. of the opossum thalamus, which have been The small calibre fibers of this tract were described by various authors (Bodian, shown to project to a wider area, which '39; Diamond and Utley, '63; Oswaldo- includes the caudal pole of the ventrobasal Cruz and Rocha-Miranda, '67a,b, '68), are complex, the posterior group (Po, as de- similar to those of higher mammals. fined by Rose and Woolsey, '58), the para- Recording from single units in the xVB fascicular-center median region, as well of the North American subspecies, Erick- as some of the intralaminar nuclei (Mehler son et al. ('64) reported a large percentage et al., '60). of units displaying wide receptive fields Single unit analysis of the Po region and convergence of sensory modalities. in the cat (Poggio and Mountcastle, '60; This result would support the idea that the Whitlock and Perl, '59; '61) shows that the metatheria display a primitive form of functional properties of its component thalamic organization, intermediate be- cells are different from those reported in tween the reptilian and the higher mam- the ventrobasal complex. The projections malian pattern. On the other hand, using to this region are attributed to the antero- the same species but recording unit cluster lateral spinal tract. A large percentage of responses to tactile stimulation, Pubols its component cells display not only wide and Pubols ('66) reported a precise somato- receptive fields, often bilateral, but also topical organization within the boundaries convergence of different sensory modal- of the xVB, similar in all respects to the ities. results obtained in eutherian mammals. Similar properties and functional organi- In view of the conflicting results ob- zation were found in the cortical sensory tained in the study of the opossum thala- areas; SI displaying properties akin to mus, the following work was carried out to those of the ventrobasal complex (Mount- clarify the points in variance. castle et al., '57; Mountcastle and Powell, The functional organization of the xVB '59; Powell and Mountcastle, '59), while was studied in a South American sub- SII can be related to the properties dis- species (D. marsupialis aurita Wied, 1826). played by Po (Andersson, '62; Carreras and In this species the cytoarchitectonic organi- Andersson, '63; Berman, '61a,b). All of zation of the central nervous system has the above results were obtained in various been shown to be identical to that of the species of eutherian mammals. North American variety by detailed ana- The functional properties displayed by tomical and statistical studies (Oswaldo- these divisions of the somatic sensory Cruz and Rocha-Miranda, '67a,b, '68). mechanisms conducted by ( 1) the dorsal Our description of the ventrobasal com- column-medial lemniscus and by (2) the plex closely corresponds with Bodian's ('39) anterolateral pathway have been corre- nucleus ventralis pars principalis, except lated by Rose and Mountcastle ('59) with for the possible inclusion of part of our respectively, ( 1) the epicritic and (2) pro- nucleus ventralis thalami lateralis and topathic concepts expressed by Head et nucleus C (see Oswaldo-Cruz and Rocha- al. ('20). Miranda, '67a,b, '68). This complex, ovoid In view of the proposed theories regard- in shape, extends from A 5.50 to A 3.17. ing the evolution of the sensory systems The rostro-caudal axis of this nucleus is and that of the thalamus (Bishop, '59; Dia- ventrally tilted in respect to the Horsley- mond and Chow, '62), it would be of Clarke basal plane. In the medio-lateral interest to extend these studies to primitive direction it attains a maximum width of mammals, representatives of the meta- 2.2 mm at its mid-portion; the dorso-ven- theria group. tral extent reaching its maximum of The common opossum (Didelphis mar- 1.5 mm at the same level. supialis, Linnaeus, 1758), being a species The medial border of this complex is of wide ecological distribution in the con- with nuclei ventralis thalami medialis ex- tinent, has been the subject of numerous cept at its caudal tip, where nuclei subparu- VENTROBASAL COMPLEX OF THE OPOSSUM 233 fascicularis and posterioris thalami re- filled with warm Ringer or mineral oil. The place the latter. The ventro and lateral dura was incised and, in all animals used borders are given by the well developed for microelectrode recording, the cortical lamina medullaris externa, except at pos- gray overlaying the thalamic region under- terior planes where nucleus posterioris going exploration was removed by sub-pial thalami is found capping the caudal pole suction. of the xVB. Dorsally, in its rostral pole, Penetrations were oriented according to the complex is related with nuclei intra- the stereotaxic atlas developed in this lab- laminaris, nucleus lateralis thalami inter- oratory for both the North and South medius and nucleus ventralis thalami Eat- eralis. At a caudal level nucleus C makes American subspecies ( Oswaldo-Cruz and its appearance as the dorsal border reach- Rocha-Miranda, '68). ing the caudal pole of the complex. In four animals the dorsal column and/ The rostral limit of this complex is diffi- or dorsolateral quadrant were sectioned at cult to determine in anatomical grounds, high cervical level. The pia-arachnoid for it gradually merges with nuclei ven- membrane was dissected and the lesion tralis thalami lateralis. accomplished by means of a razor blade fragment, the extent of the lesion being MATERIAL AND METHODS later determined by microscopic inspec- Two experimental series are included in tions of paraffin embedded, Nissl stained the present work. In the first group of 19 frontal sections. animals, unit cluster activity was recorded Recording methods. Unit cluster re- in order to establish the topography of sponses were recorded using steel needles projections of the body surface in the xVB. prepared from dental broaches, approxi- A second group, comprising 28 animals, mately 300 in diameter, showing a grad- was used to study the functional charac- ual taper towards the tip. The electrodes teristics of single units in the xVB and in were varnish-insulated except at the tip, neighboring structures. Included in this where a region of approximately 150- group are four animals in which lesions in 250 was left exposed.
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