Thalamic projections to areas 3a, 3b,and 4 in the sensorimotor cortex of the mature and infant macaque monkey

Area 3a in the macaque monkey, located in the fundus of the central sulcus, separates motor and somatosensory cortical areas 4 and 3b. The known connections of areas 4 and 3b differ substantially, as does the information which they receive, process, and transfer to other parts of the central nervous system. In this analysis the thalamic projections to each of these three cortical fields were examined and compared by using retrogradely transported fluorescent dyes (Fast Blue, Diamidino Yellow, Rhodamine and Green latex microspheres) as neuron labels. Coincident labeling of projections to 2–3 cortical sites in each monkey allowed the direct comparison of the soma distributions within the thalamic space of the different neuron populations projecting to areas 3a, 3b, and 4, as well as to boundary zones between these cortical fields. The soma distribution ofthalamic neurons projecting to a small circumscribed zone (diameter = 0.5–1.0 mm) strictly within cortical area 3a (in region of hand representation) filled out a “territory” traversing the dorsal half of the cytoarchitectonically defined thalamic nucleus, VPLc (abbreviations as in Olszewski [1952] The Thalamus of the Macaca mulatta. Basel: Karger). This elongate, rather cylindrical, territory extended caudally into the anterior pulvinar nucleus, but not forward into VPLo. The rostrocaudal extent of the thalamic territory defining the soma distribution of neurons projecting to small zones of cortical area 3b was similar, but typically extended into the ventral part of VPLc, filling out a medially concavo-convex laminar space. Two such territories projecting to adjacent zones of areas 3a and 3b, respectively, overlapped and shared thalamic space, but not thalamic neurons. Contrasting with the 3a and 3b thalamic territories, the soma distribution of thalamic neurons projecting to a circumscribed zone in the nearby motor cortex (area 4) did not penetrate into VPLc, but instead filled out a mediolaterally flattened territory extending from rostral VLo, VLm, VPLo to caudal and dorsal VLc, LP, and Pulo. These territories skirted around VPLc. All three cortical areas (4, 3a, and 3b) also received input from distinctive clusters of cells in the intralaminar Cn.Md. It is inferred that, in combination, the thalamic territories in areas 3a, 3b, and 4 (and also area 1 and 2), which would be coactive during the execution of a manual task, constituted a lamellar space extending from VLo rostrally to Pul.o caudally. How Pul.o neuron populations relate to the more rostral populations within the same thalamic territory projecting to a localized cortical zone remains uncertain. Within the medially located territories the distribution of the neuron population in Pul.o was spatially continuous with the more rostral thalamic cells projecting to the same localized cortex, but in lateral thalamic territories these 2 populations were usually spatially discontinous. In the newborn macaque an orderly change in the territorial projections to localized zones in area 4, 3a, and 3b was also demonstable. However, thalamic nuclear projections were more expansive than in the mature animal. As well as the VPLc input, a third of the thalamic input to area 3a was now from VLo, VPLo, and VLm. Area 4 also had a significant input from VPLc, an input not observed in the mature macaque. © 1993 Wiley-Liss, Inc.     

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.     

Regional distribution of cholecystokinin receptors in primate cerebral cortex determined by in vitro receptor autoradiography

Cholecystokinin (CCK) is a putative peptide neurotransmitter present in high concentration in the cerebral cortex. By using techniques of in vitro receptor autoradiography, CCK binding sites in primate cortex were labeled with 125I-Bolton-Hunter-labeled CCK-33 (the 33-amino-acid C-terminal peptide) and 3H-CCK-8 (the C-terminal octapeptide). Biochemical studies performed on homogenized and slide-mounted tissue sections showed that the two ligands labeled a high-affinity, apparently single, saturable site. Autoradiography revealed that binding sites labeled by both ligands were anatomically indistinguishable and were distributed in two basic patterns. A faint and diffuse label characterized portions of medial prefrontal cortex, premotor and motor cortices, the superior parietal lobule, and the temporal pole. In other cortical areas the pattern of binding was layer-specific; i.e., binding sites were concentrated within particular cortical layers and were superimposed upon the background of diffuse label. Layer-specific label was found in the prefrontal cortex, anterior and posterior cingulate gyrus, somatosensory cortex, inferior parietal lobule, retrosplenial cortex, insula, temporal lobe cortices, and in the primary visual and adjacent visual association cortices. The areal and laminar localization of layer-specific CCK binding sites consistently coincided with the cortical projections of thalamic nuclei. In prefrontal cortex, CCK binding sites were present in layers III and IV, precisely paralleling the terminal fields of thalamocortical projections from the mediodorsal and medial pulvinar nucleus of the thalamus. In somatosensory cortex, the pattern of CCK binding in layer IV coincided with thalamic inputs arising from the ventrobasal complex, while in the posterior cingulate gyrus, insular cortex, and retrosplenial cortex, layer IV and lower III binding mirrored the laminar distribution of cortical afferents of the medial pulvinar. CCK binding in layers IVa, IVc alpha, IVc beta, and VI of primary visual cortex corresponded to the terminal field disposition of lateral geniculate neurons, whereas in adjacent visual association cortex, binding in layers III, IV, and VI faithfully followed the cortical distribution of projections from the inferior and lateral divisions of the pulvinar nucleus of the thalamus. We interpret the diffusely labeled binding sites in primate cortex as being associated with the intrinsic system of CCK-containing interneurons that are distributed throughout all layers and areas of the cortex. The stratified binding sites, however, appear to be associated with specific extrinsic peptidergic projections.(ABSTRACT TRUNCATED AT 400 WORDS)     

Posterior parietal cortex projections to the ventral lateral and some association thalamic nuclei in Macaca mulatta

The study focused on projections from the posterior parietal cortex (PPC) to the ventral lateral thalamic nucleus (VL) and three thalamic association nuclei, mediodorsal (MD), lateral posterior (LP) and pulvinar. For light microscopic analysis small biotinylated dextran amine (BDA) or biocytin injections were placed in midrostral and dorsal portions of the inferior parietal lobule (IPL), respectively. The distribution of anterograde and retrograde labeling was charted, and representative axons and terminal fields were reconstructed in the sagittal plane to examine their features. Two types of fibers were identified--those of thin diameter forming diffuse terminal fields with small boutons, and thick fibers forming focal terminal fields with large boutons. Area PFG injection of BDA resulted in labeling of both types of fibers in LP, MD, and pulvinar, whereas only fibers of the first type were found in VL. Biocytin injection in area Opt resulted in preferential labeling of large fibers terminating in LP and pulvinar. Further electron microscopic analysis of labeled boutons in VL and LP, following a large wheat germ agglutinin conjugated horseradish peroxidase injection in the middle of IPL, confirmed the existence of small and large corticothalamic boutons and their different termination sites: the small boutons formed synapses on distal dendrites while the large boutons were found close to somata of thalamocortical projection neurons, on the dendrites of local circuit neurons and in complex synaptic arrangements, such as glomeruli. The results demonstrate that projections from small loci of the PPC to functionally and connectionally different thalamic nuclei differ anatomically, implying a different functional impact on these diverse targets.     

Intracellular staining of physiologically identified neurons and axons in the somatosensory thalamus of the cat

Neurons and axons responding to somesthetic stimulation in the thalamic ventrobasal complex (VB) were characterized electrophysiologically by intracellular recording and then individually injected with horseradish peroxidase. Two types of thalamocortical relay neuron were identified, primarily on the basis of dendritic morphology and axon diameter. Types with cutaneous or deep receptive fields were found in each class. Neither type had collateral axons in VB but each gave branches to the thalamic reticular nucleus (RTN). Small putative interneurons in VB and RTN neurons with somatosensory receptive fields were also injected. The RTN neurons had profusely branched widely ramifying axons in VB and adjoining nuclei. Injected medial lemniscal axons in VB had a range of receptive field properties and conduction velocities and ended in elongated anteroposterior domains with one or more dense concentrations of terminal boutons of varying size and with varying numbers of boutons.     

Corticopulvinar connections of areas V5, V4, and V3 in the macaque monkey: a dual model of retinal and cortical topographies

The connection zones of cortical areas V3, V4, and V5 (MT) with the thalamic pulvinar nucleus in the macaque monkey were identified. A combination of single- and dual-tracer techniques was used to study their topography and to establish whether these zones occupy separate or overlapping pulvinar territories. In each case, the retinotopic distribution of tracer in the pulvinar was charted by reference to its parallel distribution within the maps of cortical areas V1 and V2. Each of the areas V3, V4, and V5 were found to connect with both the 1 degrees and the 2 degrees maps located within the inferior and lateral pulvinar nuclei and to respect the previously identified topographies of these maps. However, V5 connects to a narrow zone lining the rostrolateral margin of the lateral and inferior pulvinar and V4 to a broader zone within the body of these two nuclei, which is adjacent to but separate from the V5 zone; the V3 zone overlaps both. Focal injections into cortex produce columns of pulvinar label whose trajectory defines a line of isorepresentation. The lines of isorepresentation in the 1 degrees and 2 degrees maps are approximately linear and parallel and adopt a rostrolateral to caudomedial axis; in the 1 degrees map, this axis is roughly perpendicular to the facet of the inferior pulvinar that lies adjacent to the lateral geniculate nucleus. The connections of V5 and V4 can be modelled as successive zones along the axis of isorepresentation, with registered visual topographies. The scheme is extended by existing reports that inferotemporal cortex connects to the caudomedial pole of this axis-reflecting an occipitotemporal cortical gradient, in that V1 and other prestriate areas, e.g., V3, connect to the opposite pole. Thus a simple model of the mapped volume in the pulvinar arises, in which a unidimensional cortical topography is represented orthogonally to retinal topography. Adjoining this volume medially, within the inferior and medial pulvinar, is a second, heavier zone of V5 connectivity, which is poorly topographic. Both the medial and the rostrolateral zones of V5 connectivity may overlap with previously identified regions of tectal input to the pulvinar.     

Organization of the Visual Sector of the Thalamic Reticular Nucleus in Galago

Projections to and from the visual sector of the thalamic reticular nucleus were studied in the prosimian primate genus Galago by anterograde and retrograde transport of WGA-HRP injected into the dorsal lateral geniculate nucleus (GLd), pulvinar nucleus, and their cortical targets. Contrary to the idea that thalamic connections with the reticular nucleus are not delimited sharply between nuclei associated with the same modality, our results show a distinct laminar segregation of the projections from the GLd and pulvinar nuclei. The GLd is connected reciprocally with the lateral {frsol|2/3} of the caudal part of the reticular nucleus, and the striate cortex sends projections to the same lateral tier. Both sets of projections are organized topographically, lines of projection taking the form of slender elongated strips that run from caudo-dorsal to rostro-ventral within the nucleus. The pulvinar nucleus, which projects to several areas of the temporal, parietal, and occipital lobes, including the striate cortex, is connected reciprocally with the medial {frsol|1/3} of the caudal part of the reticular nucleus. Every injection into the pulvinar nucleus labelled a wide area of the medial tier, with no indication of visuotopic organization. The projections from the middle temporal area, one of the principal targets of the pulvinar nucleus, also terminate only in the medial tier of the visual sector. And we would expect that, in general, a thalamic nucleus and its cortical target would project to the same part of the reticular nucleus. The case of the striate area is an exception but only in the sense that it projects to the pulvinar nucleus as well as GLd. Thus an injection into a single locus in area 17 produces two parallel strips in the visual sector of the reticular nucleus, but both are in the lateral tier. We propose that each strip arises from a separate population of cells with cortical layer VI, one with an allegiance to the GLd and the other to the pulvinar nucleus.     

Place of the thalamus in the network of interconnections between the association and limbic cortices in the monkey

Anatomophysiological criteria underlying the definition of associative cortex as well as limbic cortex include some imprecise data. The original notion of "cortical association spheres" (Flechsig) with no connections with the thalamus has rightly been abandoned, and that of the macroscopic "large limbic lobe" (Broca) fails to stand up to histologic or hodologic findings. However, the concept of cortical areas implicated specifically in multiple sensorial integration, sensory-motor coupling and control of behavior lasts due to necessity. In the monkey, the posterior parietal cortex of area 7 (PG area), the cortex of the upper slope of the superior temporal sulcus (STS) and the prefrontal cortex anterior to the sulcus arcuatus exchange direct corticocortical connections, receive afferents from sensory cortex and are not connected to specific thalamic relays. The term "associative" in its widest sense applies more particularly therefore to these cortical areas organized in networks. On the internal surface of the hemisphere, the cingular gyrus, retrosplenial cortex and parahippocampic gyrus (TF and TH areas) which occupy the major part of the limbic lobe, participate in the formation of this network and exchange direct cortico-cortical connections with the associative cortex defined above. The use of anterograde (labelled aminoacids) and retrograde (peroxidases) markers and of fluorescent dyes, allowing double retrograde labelling, demonstrates that the median pulvinar nucleus is connected with the knots of the associative cortical network. This thalamic nucleus, of a relatively increased size from phylogenetic evolution, is therefore excluded from the classification opposing specific and diffuse projection nuclei. In contrast to the thalamic reticular nucleus, which lacks cortical projections, and to the nuclei of the internal medullary band, which have the striatum as main target, the median pulvinar is a thalamic structure connected directly and specifically with each of the cortical areas, lesions of which result in negligence behavior.     

Anatomical evidence for medial pulvinar connections with the posterior cingulate cortex, the retrosplenial area, and the posterior parahippocampal gyrus in monkeys

Reciprocal connections between the medial pulvinar and the limbic neocortex in monkeys were demonstrated by means of tritiated amino acid injections in the medial pulvinar and the cingulate cortex, and HRP injections in the medial pulvinar. It appears that the medial nucleus of the pulvinar sends projection fibres to the posterior cingulate gyrus (area 23), the retrosplenial area, and the posterior parahippocampal gyrus (areas TH and TF). The labeled terminals were concentrated in two bands, one in the deeper part of layer III and in layer IV, and the other in layer I. These projections were observed to be reciprocal, and the cortical afferent fibers to the medial pulvinar were found to originate from the deep layers of the cortex. The medial nucleus of the pulvinar was already known to be connected with the prefrontal cortex and with the inferior parietal lobule. Since this nucleus is now demonstrated to be connected with the posterior limbic neocortex, it is envisaged as being the thalamic counterpart of a cortical triad (prefrontal, parietal, and limbic) involved in modulating directed attention.     

The morphology and distribution of striate cortex terminals in the inferior and lateral subdivisions of the Macaca monkey pulvinar.

The origin of the various types of axon terminals in Macaca pulvinar remains uncertain because of the contradictory results obtained in EM degeneration studies. We have used EM-autoradiography to determine the morphology of terminals in the inferior and lateral pulvinar which originate from neurons in visual cortex. After injections of H3 proline into area 17, both the small diameter (RS) and the large diameter (RL) terminals containing round vesicles and making asymmetric contacts are labeled in the two pulvinar subdivisions. Labeled and unlabeled terminals are intermixed within the pulvinar focus which suggests that the dendrites of the same pulvinar neuron receive overlapping inputs from several cortical areas. Because only 5% of the pulvinar terminals are RLs (Ogren and Hendrickson, '79), and this small number of RLs originates from at least two visual cortical areas plus the superior colliculus (Partlow et al., '77), superior colliculus input to inferior pulvinar is small compared to the combined RS and RL cortical input. Together the findings from this study and the preceding paper (Ogren and Henderickson, '79), show that while pulvinar is typical of other thalamic nuclei in the structure of its neurons and synapses, it differs in that the input from subcortical structures is minimal. It is suggested that inferior and lateral pulvinar function principally as integrators of visula cortical information.     

Bottlebrush dendritic endings and large dendritic fields: motion-detecting neurons in the mammalian tectum

The widefield vertical neurons of the lower stratum griseum superficiale (SGS3) and upper stratum opticum (SO) of the superior colliculus provide an extrageniculate route for visual information to reach the pulvinar. Previous physiological studies indicate that SGS3/SO neurons have large receptive fields and respond to small moving stimuli. We sought to better characterize the dendritic morphology of SGS3/SO neurons with intracellular filling in slice preparations of the ground squirrel superior colliculus. We found that dendrites of widefield vertical cells end in monostratified arrays of spiny terminal specializations called "bottlebrush" dendritic endings. Two major subtypes of neurons are described. Type I neurons have somata restricted to the SGS3 and bottlebrush endings in the most superficial sublayer of the SGS. Type II neurons are found at the base of the SGS and in the upper SO, and have bottlebrush endings arrayed within the middle sublayers of the SGS. Bottlebrush endings may sample and integrate laminated afferents to the superior colliculus, and cellular subtypes may underlie multiple information streams within the tectopulvinar pathway. A similar dendritic morphology and projection pattern can be found in cells of the avian optic tectum that project upon the nucleus rotundus, a thalamic nucleus homologous to the mammalian caudal/inferior pulvinar. Because motion processing is a dominant feature of the avian tectorotundal pathway, the current results suggest that both dendritic morphology and motion processing are conserved features of widefield vertical cells in the tectopulvinar pathway of vertebrates.     

Reevaluation of the primary motor cortex connections with the thalamus in primates

Six injections (approximately 1 mm in diameter) of biotinylated dextran amine (BDA) were placed in different locations of the primary motor cortex of the rhesus monkey. Anterograde and retrograde labeling patterns in the thalamus were charted and individual labeled axons traced in continuous serial sections. Both anterograde and retrograde labeling in the thalamus was extensive, spanning several millimeters mediolaterally and including ventral lateral, ventral anterior, centromedian, and centrolateral nuclei. Paracentral, mediodorsal, lateral posterior, and medial pulvinar nuclei were also labeled. Two basic types of corticothalamic axons were identified: small to medium-width, type 1 axons that formed large terminal fields with small boutons, and thick, type 2 axons that formed small terminal fields with large boutons. Within each group, subtypes were identified based on specific features of the axons and terminals: two subtypes of type 1 axons and four subtypes of type 2 axons. The results revealed multiple modes of corticothalamic connectivity: sparsely distributed type 1 axons, dense plexuses of type 1 axons, type 2 axon terminal fields either singly or in clusters, and mixed plexuses of type 1 and type 2 axons. Only some cells in the plexuses were retrogradely labeled; some plexuses did not contain any labeled neurons, and many retrogradely labeled neurons were in the regions devoid of anterograde labeling. These connectivity patterns differed between thalamic nuclei. The results revealed much more complex relationships between M1 and thalamus than were previously thought to exist. It is suggested that this connectivity is neither of exclusively a feedback nature nor perfectly reciprocal but is subserved by a multitude of channels, most likely originating from different populations of cortical neurons, and feeding into a variety of functionally different neuronal networks, with each processing specific information.     

Bilateral thalamic damage,cortical hypometabolism and behavioural disturbances

Thalamic damage could be responsible for reduced metabolism in anterior cortical areas. In order to investigate an anatomical lesion and impairment of regional blood flow (rCBF) in distant cortical areas, we studied by magnetic resonance imaging (MRI) and single photon emission computed tomography (SPECT) a patient with bilateral thalamic infarction, who presented with sudden consciousness impairment, drowsiness, gaze paralysis, dysphagia and bilateral Babinski sign. Three weeks later the neurological symptoms disappeared, but a severe mental deterioration was evident MRI showed thalamic bilateral damage of posterior and medial areas, involving part of the pulvinar, more evident for the right thalamus. A ^99mTc-HMPAO SPECT showed a decrease of rCBF over frontal and parietal regions, more evident for the right hemisphere. Six months later a severe memory impairment was still evident and MRI and SPECT picture were unchanged. The persistent memory defect could be related to a loss of cortical activation following the thalamic damage. The absence of primary lesions of cortical regions on CT scan and MRI and the neuroanatomical considerations on the diffuse projections running from medial nuclei and pulvinar to large parts of anterior neocortex supported this hypothesis.     

Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey

The efferent projections of the deep cerebellar nuclei were studied and their fiber trajectories and thalamic termination zones described. The thalamic termination zones for the dentate, interposed and fastigial nuclei are identical and coincide with the cytoarchitectonically unique cell-sparse region of the ventral lateral complex. This region includes nuclei VPLo, VLc, VLps, X and extensions of these between the cell clusters of nucleus VLo. The inputs from dentate and interpositus are contralateral, dense, and their termination patterns extend continuously throughout all nuclear components of the cell-sparse zone. Interdigitation of these two inputs within the cell-sparse region is directly demonstrated. The fastigial input is more restricted but bilateral. Each of the deep cerebellar nuclei also projects to the central lateral nucleus of the intralaminar complex. The strong interconnection of the cell-sparse zone with cortical area 4 is confirmed. The patterns of retrogradely labeled thalamocortical cells and of anterogradely labeled corticothalamic terminations following cortical injections of horseradish peroxidase and of tritiated amino acids, extend continuously through the VPLo-VLc region and its extensions, but do not invade the posteriorly situated VPLc nucleus. Thalamic inputs from the dorsal column nuclei terminate independently within the morphologically distinct VPLc nucleus adjacent to the cell-sparse cerebellar terminal zone. The dorsal column-lemniscal terminations do not overlap the cerebellar terminations. The clear segregation of the two sets of terminations is demonstrated directly using an anterograde double labeling method. Spinothalamic terminations end in VPLc but extend into the cerebellar terminal zone. Another ascending input, from the vestibular nuclei, is also shown to terminate within the cell-sparse zone. Comparison with other studies implies that cerebellar, pallidal and substantia nigral inputs do not converge in the monkey thalamus and that the nuclei in which they terminate project to different cortical areas. The relation of these and of sensory influences ascending to motor cortex from the periphery are discussed.     

Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions

In this study and its companion, the cortical and subcortical connections of the medial belt region of the marmoset monkey auditory cortex were compared with the core region. The main objective was to document anatomical features that account for functional differences observed between areas. Injections of retrograde and bi-directional anatomical tracers targeted two core areas (A1 and R), and two medial belt areas (rostromedial [RM] and caudomedial [CM]). Topographically distinct patterns of connections were revealed among subdivisions of the medial geniculate complex (MGC) and multisensory thalamic nuclei, including the suprageniculate (Sg), limitans (Lim), medial pulvinar (PM), and posterior nucleus (Po). The dominant thalamic projection to the CM was the anterior dorsal division (MGad) of the MGC, whereas the posterior dorsal division (MGpd) targeted RM. CM also had substantial input from multisensory nuclei, especially the magnocellular division (MGm) of the MGC. RM had weak multisensory connections. Corticotectal projections of both RM and CM targeted the dorsomedial quadrant of the inferior colliculus, whereas the CM projection also included a pericentral extension around the ventromedial and lateral portion of the central nucleus. Areas A1 and R were characterized by focal topographic connections within the ventral division (MGv) of the MGC, reflecting the tonotopic organization of both core areas. The results indicate that parallel subcortical pathways target the core and medial belt regions and that RM and CM represent functionally distinct areas within the medial belt auditory cortex.     

Corticothalamic connections of the posterior parietal cortex in the rhesus monkey

Corticothalamic connections of posterior parietal regions were studied in the rhesus monkey by using the autoradiographic technique. Our observations indicate that the rostral superior parietal lobule (SPL) is connected with the ventroposterolateral (VPL) thalamic nucleus. In addition, whereas the rostral SPL is connected with the ventrolateral (VL) and lateral posterior (LP) thalamic nuclei, the rostral IPL has connections with the ventroposteroinferior (VPI), ventroposteromedial parvicellular (VPMpc), and suprageniculate (SG) nuclei as well as the VL nucleus. The caudal SPL and the midportion of IPL show projections mainly to the lateral posterior (LP) and oral pulvinar (PO) nuclei, respectively. These areas also have minor projections to the medial pulvinar (PM) nucleus. Finally, the medial SPL and the caudal IPL project heavily to the PM nucleus, dorsally and ventrally, respectively. In addition, the medial SPL has some connections with the LP nucleus, whereas the caudal IPL has projections to the lateral dorsal (LD) nucleus. Furthermore, the caudal and medial SPL and the caudal IPL regions have additional projections to the reticular and intralaminar nuclei-the caudal SPL predominantly to the reticular, and the caudal IPL mainly to the intralaminar nuclei. These results indicate that the rostral-to-caudal flow of cortical connectivity within the superior and inferior parietal lobules is paralleled by a rostral-to-caudal progression of thalamic connectivity. That is, rostral parietal association cortices project primarily to modality-specific thalamic nuclei, whereas more caudal regions project most strongly to associative thalamic nuclei.     

The Organization of Projections from Subdivisions of the Auditory Cortex and Thalamus to the Auditory Sector of the Thalamic Reticular Nucleus in Galago

Anterograde and retrograde transport techniques were used to study the connexions between different subdivisions of the auditory cortex and thalamus with the thalamic reticular nucleus in the prosimian, Galago. In particular, the goal was to determine whether the primary auditory nucleus, GMv, and its cortical target, area I of the auditory cortex (A I), project to a different region of the auditory sector of the reticular nucleus from the secondary auditory nuclei, GMmc and Po and their cortical targets outside A I. The results show that the projections to and from the auditory sector are indeed segregated: injections of wheatgerm agglutinin-conjugated horseradish peroxidase into either GMmc or Po labelled cells and terminals along the medial, lateral and ventral borders of the auditory sector, forming a U-shaped pattern. Projections from area II of the auditory cortex produced almost an identical pattern of the terminal labelling in the auditory sector. In contrast, injections into GMv-labelled cells and terminals in the centre region of the auditory sector, in the 'interior' of the U-shaped region. Projections from A I were distributed to both the U-shaped border region and the central core of the auditory sector probably because A I received projections from GMmc, Po and GMv. The significance of these results depends on a comparison between the auditory and visual sectors of the reticular nucleus. Both sectors are divided into tiers or subsectors-one related to the primary relay nucleus, i.e. GLd or GMv, and the other related to the secondary relay nuclei, i.e. pulvinar nucleus, GMmc, Po, etc.     

Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus

Thalamic connections of the insula in the rhesus monkey were studied with axonal transport methods. Tritiated amino acid injections limited to the insula revealed autoradiographic label in the principal and parvicellular components of the ventroposterior medial nucleus, the ventroposterior inferior nucleus, the oral and medial pulvinar nuclei, the nucleus reuniens, the parvicellular and magnocellular components of the medial dorsal nucleus, the centromedian-parafasicularis nuclei, and the reticular nucleus. In additional animals, tritiated amino acids and horseradish perioxidase injections were made within different regions of the insula. Although the injection sites in these additional cases may have included minor extensions into claustrum and adjacent structures, several tentative conclusions emerged with respect to the antero-posterior gradient in insulothalamic connectivity. The anterior insula appears to have a more extensive relationship with the ventroposterior medial complex, the medial dorsal nucleus, the centromedian-parafasicularis nuclei and with some midline nuclei. In contrast, the posterior insula is more extensively connected with the ventroposterior inferior nucleus, the oral and medial pulvinar nuclei, and the suprageniculate nucleus. The patterns of insulothalamic connections support conclusions derived from observations on the cortical connectivity of the primate insular cortex indicating that the anterior insula is related to olfactory, gustatory, and viscero-autonomic behavior, whereas the posterior insula is related to auditory-somesthetic-skeletomotor function (Mesulam and Mufson, '82b). The medial pulvinar nucleus has extensive connections with many paralimbic cortical regions including the insula as well as with high order polymodal association cortex. These findings suggest that the medial pulvinar may provide a region for the convergence of multisensory association input with limbic information.     

The primate mediodorsal (MD) nucleus and its projection to the frontal lobe

The frontal lobe projections of the mediodorsal (MD) nucleus of the thalamus were examined in rhesus monkey by transport of retrograde markers injected into one of nine cytoarchitectonic regions (Walker's areas 6, 8A, 9, 10, 11, 12, 13, 46, and Brodmann's area 4) located in the rostral third of the cerebrum. Each area of prefrontal, premotor, or motor cortex injected was found to receive a topographically unique thalamic input from clusters of cells in specific subdivisions within MD. All of the prefrontal areas examined also receive topographically organized inputs from other thalamic nuclei including, most prominently, the ventral anterior (VA) and medial pulvinar nuclei. Conversely, and in agreement with previous findings, MD projects to areas of the frontal lobe beyond the traditional borders of prefrontal cortex, such as the anterior cingulate and supplementary motor cortex. The topography of thalamocortical neurons revealed in coronal sections through VA, MD, and pulvinar is circumferential. In the medial part of MD, for example, thalamocortical neurons shift from a dorsal to a ventral position for cortical targets lying medial to lateral along the ventral surface of the lobe; neurons in the lateral MD move from a ventral to a dorsal position, for cortical areas situated lateral to medial on the convexity of the hemisphere. The aggregate evidence for topographic specificity is supported further by experiments in which different fluorescent dyes were placed in multiple areas of the frontal lobe in each of three cases. The results show that very few, if any, thalamic neurons project to more than one area of cortex. The widespread cortical targets of MD neurons together with evidence for multiple thalamic inputs to prefrontal areas support a revision of the classical hodological definition of prefrontal cortex as the exclusive cortical recipient of MD projections. Rather, the prefrontal cortex is defined by multiple specific relationships with the thalamus.     

Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus).

The afferent thalamic connections to cortical fields important for control of head movement in space were analysed by intracortical retrograde tracer injections. The proprioceptive/vestibular area 3aV, the neck-trunk region of area 3a, receives two thirds of its thalamic projections from the oral and superior ventroposterior nucleus (VPO/VPS), which is considered as the proprioceptive relay of the ventroposterior complex (Kaas et al., J. Comp. Neurol. 226:211-240, 1984). The parieto-insular vestibular cortex (PIVC, area retroinsularis, Ri) receives its main thalamic input from posterior parts of the ventroposterior complex and from the medial pulvinar. Anatomical evidence is presented that the posterior region of the ventroposterior complex is a special compartment within this principal somatosensory relay complex. The parietotemporal association area T3, mainly involved in visual-optokinetic signal processing, receives a substantial input from the medial, the lateral, and the inferior pulvinar. Dual tracer experiments revealed that about 5% of the thalamic neurons projecting to 3aV were spatially intermingled with neurons projecting to areas PIVC or T3. This spatial intermingling was distributed over small but numerous, circumscribed thalamic regions, called "common patches," which were found mainly in the intralaminar nuclei, the posterior group of thalamic nuclei, and the caudal parts of the ventroposterior complex. The "common patches" may indicate a functional coupling of area 3aV with the PIVC or area T3 on the thalamic level. In control experiments thalamic projections to the granular insula Ig and the anterior part of area 7, two cerebral structures connected with the vestibular cortical areas, were studied. Some overlap in the thalamic relay structures projecting to these areas with those projecting to the vestibular cortices was found. A quantitative evaluation of thalamic regions projecting to different cortical structures was performed by constructing so-called "thalamograms." A scheme was developed that describes the afferent thalamic connections by which vestibular, visual-optokinetic, and proprioceptive signals reach the vestibular cortical areas PIVC and 3aV.