Thalamo‐cortical connections of areas 3a and M1 in marmoset monkeys

The present investigation is part of a broader effort to examine cortical areas that contribute to manual dexterity, reaching, and grasping. In this study we examine the thalamic connections of electrophysiologically defined regions in area 3a and architectonically defined primary motor cortex (M1). Our studies demonstrate that area 3a receives input from nuclei associated with the somatosensory system: the superior, inferior, and lateral divisions of the ventral posterior complex (VPs, VPi, and VPl, respectively). Surprisingly, area 3a receives the majority of its input from thalamic nuclei associated with the motor system, posterior division of the ventral lateral nucleus of the thalamus (VL), the mediodorsal nucleus (MD), and intralaminar nuclei including the central lateral nucleus (CL) and the centre median nucleus (CM). In addition, sparse but consistent projections to area 3a are from the anterior pulvinar (Pla). Projections from the thalamus to the cortex immediately rostral to area 3a, in the architectonically defined M1, are predominantly from VL, VA, CL, and MD. There is a conspicuous absence of inputs from the nuclei associated with processing somatic inputs (VP complex). Our results indicate that area 3a is much like a motor area, in part because of its substantial connections with motor nuclei of the thalamus and motor areas of the neocortex (Huffman et al. [2000] Soc. Neurosci. Abstr. 25:1116). The indirect input from the cerebellum and basal ganglia via the ventral lateral nucleus of the thalamus supports its role in proprioception. Furthermore, the presence of input from somatosensory thalamic nuclei suggests that it plays an important role in somatosensory and motor integration. J. Comp. Neurol. 435:291–310, 2001. © 2001 Wiley‐Liss, Inc.

[1]  J. Kaas,et al.  Representation of the body surface in somatic koniocortex in the prosimian Galago , 1980, The Journal of comparative neurology.

[2]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[3]  H. Ku¨nzle Thalamic projections from the precentral motor cortex inMacaca fascicularis , 1976, Brain Research.

[4]  C. Darian‐Smith,et al.  Thalamic projections to areas 3a, 3b, and 4 in the sensorimotor cortex of the mature and infant macaque monkey , 1993, The Journal of comparative neurology.

[5]  Gerald M. Edelman,et al.  Dynamic aspects of neocortical function , 1984 .

[6]  J. Kaas,et al.  Studies on the evolution of multiple somatosensory representations in primates: The organization of anterior parietal cortex in the new world callitrichid, Saguinus , 1986, The Journal of comparative neurology.

[7]  Jun Tanji,et al.  Activity of neurons in cortical area 3a during maintenance of steady postures by the monkey , 1975, Brain Research.

[8]  M. Carpenter,et al.  Projections of the globus pallidus and adjacent structures: An autoradiographic study in the monkey , 1976, The Journal of comparative neurology.

[9]  H. Künzle Thalamic projections from the precentral motor cortex in Macaca fascicularis. , 1976, Brain research.

[10]  David P. Friedman,et al.  Thalamic basis of place- and modality-specific columns in monkey somatosensory cortex: a correlative anatomical and physiological study. , 1982, Journal of neurophysiology.

[11]  L Krubitzer,et al.  Area 3a: topographic organization and cortical connections in marmoset monkeys. , 2001, Cerebral cortex.

[12]  André Parent,et al.  Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by flourescence retrograde labeling method , 1982, Brain Research.

[13]  A M Dale,et al.  Segregation of somatosensory activation in the human rolandic cortex using fMRI. , 2000, Journal of neurophysiology.

[14]  R. Andersen,et al.  Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex. , 1998, Journal of neurophysiology.

[15]  K. Nakano,et al.  An autoradiographic study of cortical projections from motor thalamic nuclei in the macaque monkey , 1992, Neuroscience Research.

[16]  Garrett E. Alexander Basal ganglia , 1998 .

[17]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[18]  J. C. Houk,et al.  A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS , 1984, Brain Research.

[19]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  E. Welker,et al.  Dual morphology and topography of the corticothalamic terminals originating from the primary, supplementary motor, and dorsal premotor cortical areas in Macaque monkeys , 1998, The Journal of comparative neurology.

[21]  J. Kaas,et al.  Thalamic connections of the primary motor cortex (M1) of owl monkeys , 1994, The Journal of comparative neurology.

[22]  C. G. Phillips,et al.  Inputs from low threshold muscle and cutaneous afferents of hand and forearm to areas 3a and 3b of baboon's cerebral cortex. , 1976, The Journal of physiology.

[23]  E. G. Jones,et al.  A new parcellation of the human thalamus on the basis of histochemical staining , 1989, Brain Research Reviews.

[24]  W. T. Thach,et al.  Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey , 1983, Brain Research Reviews.

[25]  J. Kaas,et al.  Connections of the ventroposterior nucleus of the thalamus with the body surface representations in cortical areas 3b and 1 of the cynomolgus macaque, (Macaca fascicularis) , 1981, The Journal of comparative neurology.

[26]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[27]  L A Krubitzer,et al.  The somatosensory thalamus of monkeys: Cortical connections and a redefinition of nuclei in marmosets , 1992, The Journal of comparative neurology.

[28]  B L Whitsel,et al.  Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site. , 1996, Journal of neurophysiology.

[29]  J. Kaas,et al.  Architectonic subdivisions of the motor thalamus of owl monkeys: Nissl, acetylcholinesterase, and cytochrome oxidase patterns , 1994, The Journal of comparative neurology.

[30]  V. Mountcastle,et al.  The representation of tactile sensibility in the thalamus of the monkey , 1952, The Journal of comparative neurology.

[31]  C. Darian‐Smith,et al.  Thalamic projections to sensorimotor cortex in the macaque monkey: Use of multiple retrograde fluorescent tracers , 1990, The Journal of comparative neurology.

[32]  S P Wise,et al.  Neuronal responses in sensorimotor cortex to ramp displacements and maintained positions imposed on hindlimb of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[33]  C. G. Phillips,et al.  Projection from low‐threshold muscle afferents of hand and forearm to area 3a of baboon's cortex , 1971, The Journal of physiology.

[34]  David P. Friedman,et al.  Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. , 1982, Journal of neurophysiology.

[35]  J. Kaas,et al.  Corticocortical and collateral thalamocortical connections of postcentral somatosensory cortical areas in squirrel monkeys: a double-labeling study with radiolabeled wheatgerm agglutinin and wheatgerm agglutinin conjugated to horseradish peroxidase. , 1985, Somatosensory research.

[36]  S. Landgren,et al.  Projection to cerebral cortex of Group I muscle afferents from the cat's hind limb , 1969, The Journal of physiology.

[37]  V. Mountcastle The visual functions of the parietal lobe , 1984, Behavioural Brain Research.

[38]  E. Rausell,et al.  Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  J. Kaas,et al.  Thalamic projections from electrophysiologically defined sites of body surface representations in areas 3b and 1 of somatosensory cortex of Cebus monkeys. , 1986, Somatosensory research.

[40]  J. B. Preston,et al.  Responses of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon. , 1976, Journal of neurophysiology.

[41]  J. Kaas,et al.  Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys , 1985, The Journal of comparative neurology.

[42]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[43]  P. Strick Anatomical analysis of ventrolateral thalamic input to primate motor cortex. , 1976, Journal of neurophysiology.

[44]  R. Porter,et al.  What is area 3a? , 1980, Brain Research Reviews.

[45]  G. Rizzolatti,et al.  Thalamic input to inferior area 6 and area 4 in the macaque monkey , 1989, The Journal of comparative neurology.

[46]  M. Sur,et al.  Representations of the body surface in postcentral parietal cortex of Macaca fascicularis , 1980, The Journal of comparative neurology.

[47]  J. Kaas,et al.  Regional segregation of neurons responding to quickly adapting, slowly adapting, deep and pacinian receptors within thalamic ventroposterior lateral and ventroposterior inferior nuclei in the squirrel monkey (Saimiri sciureus) , 1981, Neuroscience.

[48]  H. Gould,et al.  Connections between area 3b of the somatosensory cortex and subdivisions of the ventroposterior nuclear complex and the anterior pulvinar nucleus in squirrel monkeys , 1990, The Journal of comparative neurology.

[49]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[50]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[51]  P. Strick Multiple sources of thalamic input to the primate motor cortex , 1975, Brain Research.

[52]  U. Büttner,et al.  Vestibular projections to the monkey thalamus: An autoradiographic study , 1979, Brain Research.

[53]  M. Wong-Riley,et al.  Quantitative light and electron microscopic analysis of cytochrome oxidase‐rich zones in the striate cortex of the squirrel monkey , 1984, The Journal of comparative neurology.

[54]  J. Kaas,et al.  The somatotopic organization of the ventroposterior thalamus of the squirrel monkey, Saimiri sciureus , 1984, The Journal of comparative neurology.

[55]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[56]  S. Landgren,et al.  The projection of group I muscle afferents from the hindlimb to the contralateral thalamus of the cat. , 1970, Acta physiologica Scandinavica.

[57]  E. Jones Chapter I - The thalamus of primates , 1998 .

[58]  B L Whitsel,et al.  Body representation in ventrobasal thalamus of macaque: a single-unit analysis. , 1977, Journal of neurophysiology.

[59]  David P. Friedman,et al.  Thalamic input to areas 3a and 2 in monkeys. , 1981, Journal of neurophysiology.

[60]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[61]  O J Grüsser,et al.  Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus) , 1992, The Journal of comparative neurology.

[62]  E. G. Jones,et al.  Differential thalamic relationships of sensory‐motor and parietal cortical fields in monkeys , 1979, The Journal of comparative neurology.

[63]  H Asanuma,et al.  Activities of neurons in area 3a of the cerebral cortex during voluntary movements in the monkey. , 1974, Brain research.

[64]  O. Oscarsson,et al.  Short‐latency projections to the cat cerebral cortex from skin and muscle afferents in the contralateral forelimb , 1966, The Journal of physiology.

[65]  PL Strick,et al.  The origin of thalamic inputs to the "hand" representation in the primary motor cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  B. Whitsel,et al.  Thalamic projections to S‐I in macaque monkey , 1978, The Journal of comparative neurology.

[67]  S P Wise,et al.  Submodality distribution in sensorimotor cortex of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[68]  J. Johnson Comparative Development of Somatic Sensory Cortex , 1990 .

[69]  M. Carpenter,et al.  Organization of pallidothalamic projections in the rhesus monkey , 1973, The Journal of comparative neurology.

[70]  O. Grüsser,et al.  Cortico‐cortical connections and cytoarchitectonics of the primate vestibular cortex: A study in squirrel monkeys (Saimiri sciureus) , 1992, The Journal of comparative neurology.