Thalamic Input to Representations of the Teeth,Tongue, and Face in Somatosensory Area 3b of Macaque Monkeys

Representations of the parts of the oral cavity and face in somatosensory area 3b of macaque monkeys were identified with microelectrode recordings and injected with different neuroanatomical tracers to reveal patterns of thalamic projections to tongue, teeth, and other representations in primary somatosensory cortex. The locations of injection sites and resulting labeled neurons were further determined by relating sections processed to reveal tracers to those processed for myeloarchitecture in the cortex and multiple architectural stains in the thalamus. The ventroposterior medial subnucleus (VPM) for touch was identified as separate from the ventroposterior medial parvicellular nucleus (VPMpc) for taste by differential expression of several types of proteins. Our results revealed somatotopically matched projections from VPM to the part of 3b representing intra‐oral structures and the face. Retrogradely labeled cells resulting from injections in area 3b were also found in other thalamic nuclei including: anterior pulvinar (Pa), ventroposterior inferior (VPI), ventroposterior superior (VPS), ventroposterior lateral (VPL), ventral lateral (VL), center median (CM), central lateral (CL), and medial dorsal (MD). None of our injections, including those into the representation of the tongue, labeled neurons in VPMpc, the thalamic taste nucleus. Thus, area 3b does not appear to be involved in processing taste information from the thalamus. This result stands in contrast to those reported for New World monkeys. J. Comp. Neurol. 521:3954–3971, 2013. © 2013 Wiley Periodicals, Inc.     

Thalamic connections of three representations of the body surface in somatosensory cortex of gray squirrels

The anatomical tracer, wheat germ agglutinin, was used to determine the connections of electrophysiologically identified locations in three architectonically distinct representations of the body surface in the somatosensory cortex of gray squirrels. Injections in the first somatosensory area, S-I, revealed reciprocal connections with the ventroposterior nucleus (VP), a portion of the thalamus just dorsomedial to VP, the posterior medial nucleus, Pom, and sometimes the ventroposterior inferior nucleus (VPI). As expected, injections in the representation of the face in S-I resulted in label in ventroposterior medial (VPM), the medial subnucleus of VP, whereas injections in the representation of the body labeled ventroposterior lateral (VPL), the lateral subnucleus of VP. Furthermore, there was evidence from connections that the caudal face and head are represented dorsolaterally in VPM, and the forelimb is represented centrally and medially in VPL. The results also support the conclusion that a representation paralleling that in VP exists in Pom, so that the ventrolateral part of Pom represents the face and the dorsomedial part of Pom is devoted to the body. Because connections with VPI were not consistently revealed, the possibility exists that only some parts or functional modules of S-I are interconnected with VPI. Two separate small representations of the body surface adjoin the caudoventral border of S-I. Both resemble the second somatosensory area, S-II, enough to be identified as S-II in the absence of evidence for the other. We term the more dorsal of the two fields S-II because it was previously defined as S-II in squirrels (Nelson et al., '79), and because it more closely resembles the S-II identified in most other mammals. We refer to the other field as the parietal ventral area, PV (Krubitzer et al, '86). Injections in S-II revealed reciprocal connections with VP, Pom, and a thalamic region lateral and caudal to Pom and dorsal to VP, the posterior lateral nucleus, Pol. Whereas major interconnections between S-II and VPI have been reported for cats, raccoons, and monkeys, no such interconnections were found for S-II in squirrels. The parietal ventral area, PV, was found to have prominent reciprocal interconnections with VP, VPI, and the internal (magnocellular) division of the medial geniculate complex (MGi). The pattern of connections conforms to the established somatotopic organization of VP and suggests a crude parallel somatotopic organization in VPI. Less prominent interconnections were with Pol.(ABSTRACT TRUNCATED AT 400 WORDS)     

Intratrigeminal and thalamic projections of nucleus caudalis in the squirrel monkey (Saimiri sciureus): a degeneration and autoradiographic study.

In order to test the hypothesis that thalamic efferents of trigeminal nucleus caudalis (NC) are the cranial analogue of the spinothalamic system, lesion and autoradiographic studies were carried out in the squirrel monkey, and the terminal projection fields in thalamus were noted. Results showed that NC, including lateral reticular formation (LRF), projects to contralateral VPM, the VPM-VPL border and medial VPL, and a region dorsal to ventroposterior nucleus (VP) proper which contains cells larger than those in VPM yet which stain as darkly as VPL neurons; this latter zone of termination may be homologous with VPL_o (Vim) in other species, which is that area receiving lemniscal and cerebellar afferents (Mehler, '71; Walsh and Ebner, '73; Boivie, '74). In addition, a small projection is noted in an area intercalated between dorsomedial MG, limitans nucleus and posterior VP which closely agrees with the medial division of Posterior nucleus (Po) described in rhesus and squirrel monkey (Burton and Jones, '76). No terminations were observed in the gustatory nucleus medial to VPM. Bilateral, terminal projection fields were observed in posterior mediodorsal nucleus (MD), and a paralaminar area (PL) which lies in the ventrolateral strip of MD and is particularly prominent in primates; other bilateral fields were noted in CL, particularly the more medial segment of the nucleus. A sparse projection was noted in contralateral CM. Ipsilateral, intratrigeminal connections between NC and main sensory nucleus (MSV) also were observed. We conclude that, in the squirrel monkey, NC efferents, probably including LRF, may be considered analagous to the spinothalamic system by virtue of terminations in older medial and newer ventroposterior thalamus. Terminations in posterior MD may be specific to Primates. Moreover, projections to an area just dorsal to VP proper in squirrel monkey may be included within the broader definition of a neo-spinothalamic area as reflected in spinothalamic tract projections to the ventrolateral complex in cat (Boivie, '71b; Jones and Burton, '74). The small NC projection to a part of Po is consistent with spinothalamic terminations to a “posterior” thalamic area in other primates (Mehler, '69), and with the suggestion that medial Po transmits pain information (Burton and Jones, '76).     

Connections between area 3b of the somatosensory cortex and subdivisions of the ventroposterior nuclear complex and the anterior pulvinar nucleus in squirrel monkeys.

The goal of this study was to determine whether somatosensory thalamic nuclei other than the ventroposterior nucleus proper (VP) have connections with area 3b of the postcentral cortex in squirrel monkeys. Small injections of the anatomical tracers wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) or 3H-proline were placed in electrophysiologically identified representations of body parts. The results indicate that, besides the well-established somatotopically organized connections with VP, area 3b has connections with three other nuclei of the somatosensory thalamus: the ventroposterior superior nucleus (VPS ["shell" of VP]), the ventroposterior inferior nucleus (VPI), and the anterior pulvinar nucleus (Pa). Injections confined to area 3b or involving adjacent parts of area 3a or area 1 indicate that connections between VPS, VPI, and Pa and the postcentral cortex are somatotopically organized. In VPS, connections related to the hand were found medially, and connections related to the foot were lateral. In VPI, connections with the cortical representations of the mouth, hand, and foot were successively more lateral. In Pa, connections related to the mouth, hand, and foot were successively more ventral, lateral, and caudal, and the trunk region was caudomedial. The findings suggest that VPI contains a representation of all parts of the body, including the face. The connections of Pa with the primary somatosensory cortex, area 3b, the location of Pa relative to the ventroposterior nucleus, and the high degree of topographic order in the connections of Pa with the postcentral cortex suggest that Pa is an integral part of the somatosensory thalamus in monkeys and is homologous to the medial nucleus of the posterior group (Pom) in other mammals. Overall, the results contribute to the growing evidence that individual somatosensory cortical areas in monkeys receive inputs from multiple thalamic sources, and that a single thalamic nucleus has several cortical targets.     

Cortical and thalamic connections of the representations of the teeth and tongue in somatosensory cortex of new world monkeys

Connections of representations of the teeth and tongue in primary somatosensory cortex (area 3b) and adjoining cortex were revealed in owl, squirrel, and marmoset monkeys with injections of fluorescent tracers. Injection sites were identified by microelectrode recordings from neurons responsive to touch on the teeth or tongue. Patterns of cortical label were related to myeloarchitecture in sections cut parallel to the surface of flattened cortex, and to coronal sections of the thalamus processed for cytochrome oxidase (CO). Cortical sections revealed a caudorostral series of myelin dense ovals (O1-O4) in area 3b that represent the periodontal receptors of the contralateral teeth, the contralateral tongue, the ipsilateral teeth, and the ipsilateral tongue. The ventroposterior medial subnucleus, VPM, and the ventroposterior medial parvicellular nucleus for taste, VPMpc, were identified in the thalamic sections. Injections placed in the O1 oval representing teeth labeled neurons in VPM, while injections in O2 representing the tongue labeled neurons in both VPMpc and VPM. These injections also labeled adjacent part of areas 3a and 1, and locations in the lateral sulcus and frontal lobe. Callosally, connections of the ovals were most dense with corresponding ovals. Injections in the area 1 representation of the tongue labeled neurons in VPMpc and VPM, and ipsilateral area 3b ovals, area 3a, opercular cortex, and cortex in the lateral sulcus. Contralaterally, labeled neurons were mostly in area 1. The results implicate portions of areas 3b, 3a, and 1 in the processing of tactile information from the teeth and tongue, and possibly taste information from the tongue.     

Myelin stains reveal an anatomical framework for the representation of the digits in somatosensory area 3b of macaque monkeys

Brain sections cut parallel to the cortical surface revealed myelin-light septa that isolated representations of the digits and parts of the face, teeth, and tongue in area 3b of adult and infant macaque monkeys. The widths of the bands of cortex representing individual digits, as measured by the distances between isolating septa, were proportionally similar in infant (2-4 week) and adult monkeys. However, the bands for digits 1-3 were somewhat narrower in infant than adult monkeys. There was little variation in absolute widths across individuals in the infant or adult groups, or between left and right hemispheres of the same group. Widths for digits 1-4 progressively decreased. The results suggest that these isomorphs of digits emerge in prenatal or early postnatal development and typical variations in postnatal hand use have little impact on subsequent development. As the hand representation in somatosensory cortex of monkeys may be significantly altered after the partial loss of peripheral nerve inputs, the physiological representation is not completely constrained by the isolating septa. Instead, the septa may serve as a persistent marker of normal organization in studies of cortical reorganization.     

Connections of the fronto-parietal operculum and the postcentral gyrus with the posterior ventral thalamic nucleus, especially its medial nucleus, in monkeys

In 22 crab-eating monkeys (Macaca irus), either lesions or HRP injections were made in the frontol parietal operculum and, for the purpose of contrast, in the postcentral gyrus to observe their fiber connectionl with the posterior ventral nucleus (VP). The exposed opercular part, reported to consist of areas 3b, 1, and 2 showed scanty fiber connections with VP. The buried parietal operculum had connections with the media (VPM) and lateral (VPL) nuclei of VP, corresponding to the second somatic sensory cortex (SII). This cortica area was connected, in VPM, to its ventromedial part, while the base of the postcentral gyrus, the ordinary face area of SI, was connected to its lateral-most part. This suggests that the ventromedial part of VPM is more intimately related to SII, and its lateral-most part to SI. In contrast, the SI and SII areas of VPL overlapped more extensively with each other. The cortical area which received fibers from the parvocellular part of VPM (VPMpc) lay in the frontal operculum, especially in its buried part. This area extended caudally beyond the precentral dimple and included areas 1 and 2 of the buried frontal operculum, indicating that its posterior extent was wider than the pure taste cortical area. Spinothalamic terminations in VPL and the PO nuclear group were discussed in relation to cortical connections of these thalamic nuclei. It was suggested that spinothalamic input could be relayed to both postcentral and opercular cortices. The relation of the spinothalamic input to the PO group appeared to be minor.     

Bilateral effects of spinal overhemisections on the development of the somatosensory system in rats

Connections of the forepaw regions of somatosensory cortex (S1) were determined in rats reared to maturity after spinal cord overhemisections at cervical level C3 on postnatal day 3. Overhemisections cut all ascending and descending pathways and intervening gray on one side of the spinal cord and the pathways of the dorsal funiculus contralaterally. Bilateral lesions of the dorsal columns reduced the size of the brainstem nuclei by 41%, and the ventroposterior lateral subnucleus (VPL) of the thalamus by 20%. Bilateral lesions also prevented the emergence of the normal cytochrome oxidase barrel pattern in forepaw and hindpaw regions of S1. Injections of wheat germ agglutinin conjugated to horseradish peroxidase were placed in the forepaw region of granular S1 and surrounding dysgranular S1 contralateral to the hemisection. The VPL nucleus was densely labeled, whereas the adjoining ventroposterior medial subnucleus, VPM, representing the head, was unlabeled. Thus, there was no evidence of abnormal connections of VPM to forepaw cortex. Foci of transported label in the ipsilateral hemisphere appeared to be in normal locations and of normal extents, but connections in the opposite hemisphere were broadly and nearly uniformly distributed in sensorimotor cortex in a pattern similar to that in postnatal rats. Rats with incomplete lesions that spared the dorsal column pathway on the left side but not the right demonstrated surprisingly normal distributions of callosal connections in the nondeprived right hemisphere, even though the injected left hemisphere was deprived. Thus, the development of the normal pattern of callosal connections depends on dorsal column input and not on normal interhemsipheric interactions.     

Thalamic projections to the second and fourth somesthetic areas in the anterior ectosylvian gyrus of the cat

The topical organization of thalamic projections to the second and fourth somesthetic areas in the anterior ectosylvian gyrus of the cat has been studied using the technique of retrograde axonal transport of horseradish peroxidase. The projections of the posterolateral and posteromedial ventral nuclei (VPL, VPM) to the second somesthetic area (SII) are organized somatotopically. The posterior portion of SII (hindlimb area) receives fibers mainly from the dorsolateral part of VPL, the middle portion of SII (forelimb area) from the ventromedial part of VPL, and the anterior portion of SII (face area) from VPM. These topical projections are more loosely organized and less densely arranged than those to the first somesthetic area. The SII receives a few fibers from the medial geniculate nucleus, particularly its magnocellular and dorsal principal parts, and from the suprageniculate nucleus. The posterior part of SII lying near the secondary auditory area receives many fibers from the medial geniculate and suprageniculate nuclei, and only a few fibers from the lateral central and paracentral nuclei. The fourth somesthetic area (SIV), located in the dorsal bank of the anterior ectosylvian sulcus, receives fibers mainly from the dorsal principal and magnocellular parts of the medial geniculate nucleus, and from the suprageniculate nucleus. The SIV receives a fair number of fibers from VPL and VPM roughly in a somatotopical manner. The posterior portion of SIV receives fibers chiefly from the dorsolateral part of VPL, the middle portion of SIV from the ventromedial part of VPL, and the anterior portion from VPM. In addition, SIV receives a few fibers from the lateral central, paracentral, ventral lateral and ventral medial nuclei. The SIV, together with the most posterior part of SII, forms an auditory area, receiving many fibers from the medial geniculate and suprageniculate nuclei, and a few fibers from the intralaminar nuclei.     

The somatotopic organization of the ventroposterior thalamus of the squirrel monkey, Saimiri sciureus

Multiunit microelectrode mapping techniques were used to investigate the organization of the somatosensory thalamus in squirrel monkeys. Receptive fields and response characteristics were determined for closely spaced recording sites along arrays of electrode penetrations that passed through the ventral thalamus dorsoventrally, rostrocaudally, or lateromedially. The results were related to thalamic architecture and led to the following conclusions: (1) A large, single, systematic representation of the body surface occupied most or all of the ventroposterior nucleus, VP. The nucleus was further defined by a distinct cytoarchitectonic appearance, produced by densely packed, deeply stained neurons. (2) Recording sequences in VP were characterized by (a) abrupt shifts in receptive field locations over short recording distances indicating that the electrode had crossed discontinuities or folds in the representation, (b) long sequences of overlapping receptive fields indicating regions of continuous representation and the maintenance of adjacency in the map, and (c) similar receptive field locations for sites along the trajectory of a penetration indicating regions of isorepresentation. Major somatotopic discontinuities were associated with crossing narrow cell-poor laminae that partially divided VP into subnuclei related to the hand, foot, trunk, and tail in lateral VP and the face in medial VP. Somatotopic discontinuities occurred for electrode penetrations in all three planes, but discontinuities were greater and more frequent for lateromedial electrode penetrations. Lines of isorepresentation and gradual change were most extensive in the rostrocaudal and dorsoventral planes. We hypothesize that the disruptions, regions of isorepresentation, and regions of gradual change result from the thickening, splitting, and folding of a two-dimensional representation of the skin surface to occupy a three-dimensional volume. (3) The magnifications of various skin surfaces in VP were variable so that some skin surfaces, especially the tips of the digits, occupied relatively large portions of the nucleus, while other skin surfaces such as the trunk activated little tissue. It appeared that regions of isorepresentation varied in extent according to magnification factor and position in the map. (4) Within VP, neurons could be classified as slowly adapting or rapidly adapting to maintained skin indentation. Each type of neuron formed small groups or clusters in the nucleus so that several successive recording sites typically encountered one type before a sequence of the other type was observed.(ABSTRACT TRUNCATED AT 400 WORDS)     

Mapping the effects of motor cortex stimulation on somatosensory relay neurons in the rat thalamus: Direct responses and afferent modulation

Single unit recordings were used to map the spatial distribution of motor (MI) cortical influences on thalamic somatosensory relay nuclei in the rat. A total of 215 microelectrode penetrations were made to record single neurons in tracks through the medial and lateral ventroposterior (VPM and VPL), ventrolateral (VL), reticular (nRt), and posterior (Po) thalamic nuclei. Single units were classified according to their: 1) location within the nuclei, 2) receptive fields, and 3) response to standardized microstimulation in deep layers of the forepaw-forelimb areas of MI cortex. For mapping purposes, only short latency (1-7 msec) excitatory neuronal responses to the MI cortex stimulation were considered. Percentages of recorded thalamic neurons responsive to the MI stimulation varied considerably across nuclei: VL: 42.6%, nRt: 23.0%, VPL: 15.7%, VPM: 9.3%, and Po: 3.9%. Within the VPL, most responsive neurons were found in "border" regions, i.e., areas adjacent to the VL, and (to a lesser extent) the nRt and Po thalamic nuclei. The same parameters of MI cortical stimulation were used in studies of corticofugal modulation of afferent transmission through the VPL thalamus. A condition-test (C-T) paradigm was implemented in which the cortical stimulation (C) was delivered at a range of time intervals before test (T) mechanical vibratory stimulation was applied to digit No. 4 of the contralateral forepaw. The time course of MI cortical effects was analyzed by measuring the averaged evoked unit responses of the thalamic neurons to the T stimuli, and plotting them as a function of C-T intervals from 5-50 msec. Of the 30 VPL neurons tested during MI stimulation, the average response to T stimulation was decreased a mean 43%, with the suppression peaking at about 30 msec after the C stimulus. This suppression was more pronounced in the VPL border areas (-52% in areas adjacent to VL and nRt) than in the VPL center (-25%).     

Central projections from the skin of the hand in squirrel monkeys.

Central termination patterns of afferents from the hands of squirrel monkeys were studied after subdermal injections of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) or cholera toxin subunit B conjugated to HRP (BHRP). WGA-HRP more effectively labeled axons terminating in the superficial dorsal horn of the spinal cord, while BHRP more effectively labeled axons terminating in the deeper layers. Injections of both tracers, when restricted to parts of glabrous digits, palm, or dorsal hand, revealed somatotopic patterns in the spinal cord and pars rotunda of the cuneate nucleus that were, in some respects, similar and, in other respects, quite different from those previously reported for macaque monkey (Florence et al., J. Comp. Neurol. 286:48-70, '89). As in macaques, injections in digits 1-5 produced a rostrocaudal sequence of foci of terminations in the cervical spinal cord. However, inputs from the palm were located medial to those from the digits, whereas the palm is represented lateral to the digits in macaque monkeys. Since inputs from the palm is also medial in the dorsal horn in cats (Nyberg and Blomqvist, J. Comp. Neurol. 242:28-39, '85), the condition in squirrel monkeys may be similar to the generalized state. In the cuneate nucleus, single injections in the hand produced dense label in the pars rotunda, and sparse label in the rostral and caudal poles. As in macaque monkeys, inputs from specific parts of the hand related to rostrocaudal clusters of cells that are cytochrome oxidase dense. The representation of the digits differed from macaques in that the digits were represented dorsal to the palm, rather that ventral to the palm as in macaques. Again, comparisons with cats suggest that squirrel monkeys have the more generalized pattern. Finally, inputs from the hair, dorsal surfaces of the digits terminated on the same clusters as the inputs from the glabrous, ventral surfaces, apparently overlapping somewhat. The proximity of these terminations from dorsal and ventral surfaces of the digits may be related to observations that cortical representations of the glabrous surfaces of digits become responsive to dorsal surfaces of the same digits when inputs from glabrous skin are chronically deactivated (e.g., Merzenich et al., Neuroscience 3:33-55, '83).     

Representation of face and intra-oral structures in area 3b of macaque monkey somatosensory cortex

Details of the representation of body regions innervated by the trigeminal nerve were elucidated in monkey cerebral cortex. Microelectrode recording was used to generate somatosensory maps in the posterior bank of the central sulcus and on the exposed cortical surface lateral to the lateral tip of the central sulcus in Macaca nemestrina. The area innervated by the contralateral trigeminal nerve is represented in an 8-mm mediolateral extent of area 3b lateral to the representation of the hand. Lateral to this, still within area 3b, there is an expanded representation of ipsilateral intra-oral structures measuring 6 mm in mediolateral extent. Both representations fill area 3b anteroposteriorly. The ipsilateral representation forms approximately 40% of the trigeminal representation, consistent with the amount of the ventroposterior medial (VPM) thalamic nucleus devoted to representation of ipsilateral intra-oral structures. Comparison of the present results with maps of the face representation in other species of monkey shows a consistent somatotopy of the face between species; size variations are mainly related to the enlarged ipsi- and contralateral representations of the cheek pouches in macaques. The general somatotopy of the trigeminal representation in monkeys is consistent with that in other mammalian species. © 1996 Wiley-Liss, Inc.     

The lateral cervical nucleus in the cat: anatomic organization of cervicothalamic neurons.

The morphology of the lateral cervical nucleus (LCN) and the organization of the cervicothalamic projection neurons were studied in cats which had received thalamic injections of horseradish peroxidase (HRP). The boundaries of the LCN were defined following very large thalamic (HRP injections. Roughly 92-97% of LCN cells project contralaterally to thalamus; an additional 1.5% project ipsillaterally. Computer-assisted measurements of perikaryal areas demonstrated that there are two sizes of LCN cells, large (175-900 micrometer 2) and small (less than 175 micrometer 2); the small cells are localized in the medial third of the LCN. LCN cells which are not labeled after large thalamic HRP injections are predomininantly small, medially-located neurons. Small HRP injections into physiologically identified regions of ventroposterior thalamus demonstrated that cervicothalamic neurons are organized in a topography consistent with that observed physiologically in the LCN (Craig and Tapper, '78). Dorsolateral LCN cells are retrogradely labeled from nucleus ventroposterolateralis, pars lateralis (VPL1), ventromedial LCN cells are labeled from pars medialis (VPL m), and a few medial cells are labeled from nucleus ventroposteromedialis (VPM). A few cells in the medial portion of the LCN are also labeled from each part of ventroposterior thalamus. Some interspersion was observed even in the cases with the most well-restricted labeling. We conclude that the LCN maintains a basic somatotographic organization with an inherent variability, certain aspects of which are consistently demonstrable both physiologically and anatomically. Evidence was also obtained suggestive of a rostrocaudal inversion in the cervicothalamic projection. The cervicothalamic projection, the differentiation of the medial LCN subpopulation, and the possible redefinition of the LCN are discussed in light of these results.     

Thalamic projections from lateral cervical nucleus in monkey. A degeneration study

The projection from the lateral cervical nucleus (LCN) to the thalamus has been investigated in macaque monkeys. After electrolytic lesions of the LCN, the degeneration was studied in sections impregnated by the Wiitanen method. The cervicothalamic fibers cross the midline at their level of origin and ascend to the thalamus in the medial lemniscus. A small ipsilateral projection may also exist. The tract terminates in the posteromedial (POm) and ventralis posterolateralis (VPL) nuclei. Termination in the POm is indicated by the presence of a small number of thin preterminal fibers. In the VPL the cervicothalamic fibers are unevenly distributed, forming patches of moderately dense preterminal networks, mainly in the medial two-thirds of the nucleus. Rostrocaudally the termination is restricted to areas corresponding to Olszewski's VPLc. Compared to cat, the cervicothalamic projection to the VPL in the monkey appears considerably smaller. It is also much smaller than the spinothalamic projection to the VPL in the monkey. The results neither confirm nor exclude a small projection to the nucleus ventralis posteromedialis (VPM) from the lateral cervical nucleus.     

Structural plasticity of GABAergic and glutamatergic networks in the motor thalamus of parkinsonian monkeys

In the primate thalamus, the parvocellular ventral anterior nucleus (VApc) and the centromedian nucleus (CM) receive GABAergic projections from the internal globus pallidus (GPi) and glutamatergic inputs from motor cortices. In this study, we used electron microscopy to assess potential structural changes in GABAergic and glutamatergic microcircuits in the VApc and CM of MPTP-treated parkinsonian monkeys. The intensity of immunostaining for GABAergic markers in VApc and CM did not differ between control and parkinsonian monkeys. In the electron microscope, three major types of terminals were identified in both nuclei: (a) vesicular glutamate transporter 1 (vGluT1)-positive terminals forming asymmetric synapses (type As), which originate from the cerebral cortex, (b) GABAergic terminals forming single symmetric synapses (type S1), which likely arise from the reticular nucleus and GABAergic interneurons, and (c) GABAergic terminals forming multiple symmetric synapses (type S2), which originate from GPi. The density of As terminals outnumbered that of S1 and S2 terminals in VApc and CM of control and parkinsonian animals. No significant change was found in the abundance and synaptic connectivity of S1 and S2 terminals in VApc or CM of MPTP-treated monkeys, while the prevalence of “As” terminals in VApc of parkinsonian monkeys was 51.4% lower than in controls. The cross-sectional area of vGluT1-positive boutons in both VApc and CM of parkinsonian monkeys was significantly larger than in controls, but their pattern of innervation of thalamic cells was not altered. Our findings suggest that the corticothalamic system undergoes significant synaptic remodeling in the parkinsonian state.     

Differential synaptic plasticity of the corticostriatal and thalamostriatal systems in an MPTP-treated monkey model of parkinsonism

Two cardinal features of Parkinson's disease (PD) pathophysiology are a loss of glutamatergic synapses paradoxically accompanied by an increased glutamatergic transmission to the striatum. The exact substrate of this increased glutamatergic drive remains unclear. The striatum receives glutamatergic inputs from the thalamus and the cerebral cortex. Using vesicular glutamate transporters (vGluTs) 1 and 2 as markers of the corticostriatal and thalamostriatal afferents, respectively, we examined changes in the synaptology and relative prevalence of striatal glutamatergic inputs in methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated monkeys using electron microscopic immunoperoxidase and confocal immunofluorescence methods. Our findings demonstrate that the prevalence of vGluT1-containing terminals is significantly increased in the striatum of MPTP-treated monkeys (51.9 ± 3.5% to 66.5 ± 3.4% total glutamatergic boutons), without any significant change in the pattern of synaptic connectivity; more than 95% of vGluT1-immunolabeled terminals formed axo-spinous synapses in both conditions. In contrast, the prevalence of vGluT2-immunoreactive terminals did not change after MPTP treatment (21.7 ± 1.3% vs. 21.6 ± 1.2% total glutamatergic boutons). However, a substantial increase in the ratio of axo-spinous to axo-dendritic synapses formed by vGluT2-immunoreactive terminals was found in the pre-caudate and post-putamen striatal regions of MPTP-treated monkeys, suggesting a certain degree of synaptic reorganization of the thalamostriatal system in parkinsonism. About 20% of putative glutamatergic terminals did not show immunoreactivity in striatal tissue immunostained for both vGluT1 and vGluT2, suggesting the expression of another vGluT in these boutons. These findings provide striking evidence that suggests a differential degree of plasticity of the corticostriatal and thalamostriatal system in PD.     

Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque

The thalamocortical relations of the somatic fields in and around the lateral sulcus of the macaque were studied following cortical injections of tritated amino acids and horseradish peroxidase (HRP). Special attention was paid to the second somatosensory area (S2), the connections of which were also studied by means of thalamic isotope injections and retrograde degeneration. S2 was shown to receive its major thalamic input from the ventroposterior inferior thalamic nucleus (VPI) and not, as previously reported, from the caudal division of the ventroposterior lateral nucleus (VPLc). Following small injections of isotope or HRP into the hand representation of S2, only VPI was labeled. Larger injections, which included the representations of more body parts, led to heavy label in VPI, with scattered label in VPLc, the central lateral nucleus (CL), and the posterior nucleus (Po). In addition, small isotope injections into VPLc did not result in label in S2 unless VPI was also involved in the injection site, and ablations of S2 led to cell loss in VPI. Comparison of injections involving different body parts in S2 suggested a somatotopic arrangement within VPI such that the trunk and lower limb representations are located posterolaterally and the hand and arm representations anteromedially. The location of the thalamic representations of the head, face, and intraoral structures that project to S2 may be in the ventroposterior medial nucleus (VPM). The granular (Ig) and dysgranular (Id) fields of the insula and the retroinsular field (Ri) each receive inputs from a variety of nuclei located at the posteroventral border of the thalamus. Ig receives its heaviest input from the suprageniculate-limitans complex (SG-Li), with additional inputs from Po, the magnocellular division of the medial geniculate n. (MGmc), VPI, and the medial pulvinar (Pulm). Id receives its heaviest input from the basal ventromedial n. (VMb), with additional inputs from VPI, Po, SG-Li, MGmc, and Pulm. Ri receives its heaviest input from Po, with additional input from SG-Li, MGmc, Pulm, and perhaps VPI. Area 7b receives its input from Pulm, the oral division of the pulvinar, the lateral posterior n., the medial dorsal n., and the caudal division of the ventrolateral n. These results indicate that the somatic cortical fields, except for those comprising the first somatosensory area, each receive inputs from an array of thalamic nuclei, rather than just one, and that individual thalamic somatosensory relay nuclei each project to more than one cortical field.     

Synaptic arrangements in the ventral posterolateral nucleus of the squirrel

Because murine rodents have no complex synaptic arrangements in the ventral posterolateral nucleus (VPL), we sought to determine if the lack of complexity was a characteristic common to all rodents. We studied the synaptology of VPL in the fox squirrel, Sciurus niger, using electron microscopy. We found vesicle-containing dendrites and complex synaptic arrangements in the squirrel VPL. Therefore, the relative simplicity of the rat and mouse VPL is not a general feature of the rodent somatosensory thalamus.