A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey

Rezak, Michael; Benevento, L.A.

doi:10.1016/0006-8993(79)90260-9

Cited by 135 publications

(67 citation statements)

References 47 publications

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“…The pulvinar is known to send projections to both primary (V1) and secondary visual cortices (35,36). These projections led Rezak and Benevento (36) to conclude that the inputs from pulvinar are likely to influence the response properties of V1 neurons.…”

Section: Discussionmentioning

confidence: 99%

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

Viaene

Petrof

Sherman

2011

Proc. Natl. Acad. Sci. U.S.A.

147

133

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Primary somatosensory cortex (S1) receives two distinct classes of thalamocortical input via the lemniscal and paralemniscal pathways, the former via ventral posterior medial nucleus (VPM), and the latter, from the posterior medial nucleus (POm). These projections have been described as parallel thalamocortical pathways. Although the VPM thalamocortical projection has been studied in depth, several details of the POm projection to S1 are unknown. We studied the synaptic properties and anatomical features in the mouse of the projection from POm to all layers of S1 and to layer 4 of secondary somatosensory cortex (S2). Neurons in S1 responded to stimulation of POm with what has been termed Class 2 properties (paired-pulse facilitation, small initial excitatory postsynaptic potentials (EPSPs), a graded activation profile, and a metabotropic receptor component; thought to be modulatory), whereas neurons in layer 4 of S2 responded with Class 1A properties (paired-pulse depression, large initial EPSPs, an all-or-none activation profile, and no metabotropic receptor component, thought to be a main information input). Also, labeling from POm produced small boutons in S1, whereas both small and large boutons were found in S2. Our data suggest that the lemniscal and paralemniscal projections should not be thought of as parallel information pathways to S1 and that the paralemniscal projection may instead provide modulatory inputs to S1. driver | modulator | glutamatergic | barrel cortex | synapse P rimary somatosensory (also barrel or S1) cortex in rodents receives two distinct types of input from thalamus that are thought to convey different types of sensory information (1, 2). The lemniscal projection is relayed through the ventral posterior medial nucleus (VPM), whereas the paralemniscal projection is routed through posterior medial nucleus (POm) (3, 4). These projections are not only separated in thalamus, but remain largely segregated across cortical layers and in barrels and septa (3-8).The synaptic properties of the VPM or lemniscal projection to S1 have been described (9-12). VPM inputs to layer 4 and the subgranular layers have Class 1* (or driver) properties, suggesting that they are main information routes, whereas the projections to layers 2/3 have predominantly Class 2 properties, suggesting a modulatory rather than information-bearing function. If the paralemniscal projection to S1 is a parallel information route (3, 4), the prediction is that the synaptic properties of this pathway should be largely or exclusively Class 1A (for detailed explanation of classification terms, see refs. 11-13). POm is known to provide Class 1A input to layer 4 of secondary somatosensory cortex (S2) (10), but the POm projection to S1 has yet to be described. We thus studied the properties of the POm thalamocortical projection and found that the POm projection to S1 is entirely Class 2 in nature, suggesting that it provides modulatory inputs to S1 rather than functioning as a parallel information pathway. ResultsGlutamate Uncaging...

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Section: Discussionmentioning

confidence: 99%

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

Viaene

Petrof

Sherman

2011

Proc. Natl. Acad. Sci. U.S.A.

147

133

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“…This would be consistent with the pulvinar lying near the bottom of the hierarchy and providing ascending projections to the extrastriate cortex. Interestingly, however, the pulvinar projection to VI terminates mainly in superficial layers, even though the reciprocal pathway originates from layer 5, just as for extrastriate areas (Rezak and Benevento, 1979). Thus, there is no clear basis for placing the pulvinar in a specific hierarchical relationship relative to VI.…”

Section: Subcortical Projectionsmentioning

confidence: 97%

Distributed Hierarchical Processing in the Primate Cerebral Cortex

Felleman¹,

1991

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In recent years, many new cortical areas have been identified in the macaque monkey. The number of identified connections between areas has increased even more dramatically. We report here on (1) a summary of the layout of cortical areas associated with vision and with other modalities, (2) a computerized database for storing and representing large amounts of information on connectivity patterns, and (3) the application of these data to the analysis of hierarchical organization of the cerebral cortex. Our analysis concentrates on the visual system, which includes 25 neocortical areas that are predominantly or exclusively visual in function, plus an additional 7 areas that we regard as visual-association areas on the basis of their extensive visual inputs. A total of 305 connections among these 32 visual and visual-association areas have been reported. This represents 31 % of the possible number of pathways if each area were connected with all others. The actual degree of connectivity is likely to be closer to 40%. The great majority of pathways involve reciprocal connections between areas. There are also extensive connections with cortical areas outside the visual system proper, including the somatosensory cortex, as well as neocortical, transitional, and archicortical regions in the temporal and frontal lobes. In the somatosensory/motor system, there are 62 identified pathways linking 13 cortical areas, suggesting an overall connectivity of about 40%. Based on the laminar patterns of connections between areas, we propose a hierarchy of visual areas and of somatosensory/motor areas that is more comprehensive than those suggested in other recent studies. The current version of the visual hierarchy includes 10 levels of cortical processing. Altogether, it contains 14 levels if one includes the retina and lateral geniculate nucleus at the bottom as well as the entorhinal cortex and hippocampus at the top. Within this hierarchy, there are multiple, intertwined processing streams, which, at a low level, are related to the compartmental organization of areas VI and V2 and, at a high level, are related to the distinction between processing centers in the temporal and parietal lobes. However, there are some pathways and relationships (about 10% of the total) whose descriptions do not fit cleanly into this hierarchical scheme for one reason or another. In most instances, though, it is unclear whether these represent genuine exceptions to a strict hierarchy rather than inaccuracies or uncertainties in the reported assignment.During the past decade, there has been an explosion of information about the organization and connectivity of sensory and motor areas in the mammalian cerebral cortex. Many laboratories have concentrated their efforts on the visual cortex of macaque monkeys, whose superb visual capacities in many ways rival those of humans. In this article, we survey recent progress in charting the layout of different cortical areas in the macaque and in analyzing the hierarchical relationships among these areas, part...

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“…The fact that EphA3 is expressed by presumptive extrastriate but not striate cortex at E65 suggests that hierarchical distinctions emerge early among visual subregions. Indeed, such early molecular distinctions are mirrored in the fact that layer IV cells of the striate and extrastriate cortex in primates, but not in most other species, eventually receive exclusive inputs from the spulvinar and lateral geniculate nuclei, respectively, of the thalamus (Benevento and Rezak, 1976;Hendrickson et al, 1978;Rezak and Benevento, 1979;Levitt et al, 1995). This is why the difference in distribution of EphA3 and EphA6 might not be expected in other species, where the projections of visual thalamic nuclei overlap.…”

Section: Areal Distributionmentioning

confidence: 92%

Molecular Evidence for the Early Specification of Presumptive Functional Domains in the Embryonic Primate Cerebral Cortex

1999

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To identify molecules that may play a role in the initiation of cerebral cortical area formation, we examined the expression of the Eph receptors and their ligands, the ephrins, during primate corticogenesis. We selected the macaque monkey neocortex because of its clear areal subdivisions, large surface area, protracted development (gestation ϭ 165 d), and similarity to the human brain. In situ hybridizations, performed at early [embryonic day 65 (E65)], middle (E80), and late (E95) stages of cortical development, revealed that EphA system family members are expressed in distinct gradients and laminar and areal domains in the embryonic neocortex. Indeed, several regionally restricted molecular patterns are already apparent within the cortical plate at E65, before the formation of thalamocortical connections, suggesting that the initial expression of some EphA system members is regulated by programs intrinsic to cortical cells. For example, EphA3, EphA6, and EphA7 are all selectively expressed within the presumptive visual cortex. However, although EphA6 and EphA7 are present throughout this region, EphA3 is only expressed in the prospective extrastriate cortex, suggesting that cortical cells harbor functional biases that may influence the formation of appropriate synaptic connections. Although several patterns of early gene expression are stable (e.g., EphA3, EphA4, and EphA6), others change as development proceeds (e.g., EphA5, EphA7, ephrin-A2, ephrin-A3, and ephrin-A5), perhaps responding to extrinsic cues. Thus, at E95, after connections between the cortical plate and thalamus have formed, receptor subtypes EphA3, EphA5, EphA6, and EphA7 and the ligand ephrin-A5 are expressed in posterior regions, whereas EphA4 and ephrin-A2 and ephrin-A3 are either uniformly distributed or anteriorly biased. Taken together, our results demonstrate molecular distinctions among cells of the embryonic primate neocortex, revealing hitherto unrecognized compartmentalization early in corticogenesis.

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A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey

Cited by 135 publications

References 47 publications

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

Properties of the thalamic projection from the posterior medial nucleus to primary and secondary somatosensory cortices in the mouse

Distributed Hierarchical Processing in the Primate Cerebral Cortex

Molecular Evidence for the Early Specification of Presumptive Functional Domains in the Embryonic Primate Cerebral Cortex

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