Few intrinsic connections cross the hand‐face border of area 3b of New World monkeys

After long‐standing loss of afferents from the hand, the hand representation in area 3b of the somatosensory cortex of monkeys becomes responsive to touch on the face. Because the reactivation of deprived hand cortex by the face inputs could depend on axonal connections across the hand‐face border, we determined the extent of such connections in New World marmosets, owl monkeys, and squirrel monkeys. Small injections of anatomic tracers were placed in the hand or the face representations after these representations were identified by microelectrode recordings. The positions of retrogradely labeled neurons were plotted in processed brain sections cut parallel to the brain surface, and their locations were related to anatomic isomorphs of the hand and face representations revealed in adjacent brain sections stained for myelin. In these sections, the hand‐face border was clearly visualized as a myelin‐poor septum. The intrinsic connections of area 3b labeled by injections in either the hand or face representations were almost completely confined to their respective representation, and very few neurons projected across the border. In addition, neurons in the somatosensory thalamus labeled by injections in either face or hand representations were confined to either VPM, representing the face, or the hand subnucleus of VPL. Thus the reactivation of hand cortex by face stimulation does not depend on a previously existing network of intrinsic cortical connections across the hand‐face border, or mismatched thalamocortical projections. J. Comp. Neurol. 454:310–319, 2002. © 2002 Wiley‐Liss, Inc.

[1]  Neeraj Jain,et al.  Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys , 2001, The Journal of comparative neurology.

[2]  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.

[3]  Iwona Stepniewska,et al.  Somatosensory input to the ventrolateral thalamic region in the macaque monkey: A potential substrate for parkinsonian tremor , 2003, The Journal of comparative neurology.

[4]  J. Kaas,et al.  Subdivisions of the visual system labeled with the Cat-301 antibody in tree shrews , 1994, Visual Neuroscience.

[5]  J. Kaas,et al.  A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations. , 1998, Cerebral cortex.

[6]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[7]  J. Kaas,et al.  Functional reorganization in adult monkey thalamus after peripheral nerve injury , 1991, Neuroreport.

[8]  J. Kaas,et al.  Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. , 1998, Science.

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

[10]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[11]  M Sur,et al.  The arbors of axons terminating in middle cortical layers of somatosensory area 3b in owl monkeys. , 1989, Somatosensory & motor research.

[12]  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.

[13]  E G Jones,et al.  Extent of intracortical arborization of thalamocortical axons as a determinant of representational plasticity in monkey somatic sensory cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[15]  S. Hockfield,et al.  A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[16]  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.

[17]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[18]  E G Jones,et al.  Hand/Face Border as a Limiting Boundary in the Body Representation in Monkey Somatosensory Cortex , 1997, The Journal of Neuroscience.

[19]  Jon H. Kaas,et al.  Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury , 1997, Nature.

[20]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  J. Kaas,et al.  Pattern of peripheral deafferentation predicts reorganizational limits in adult primate somatosensory cortex. , 1994, Somatosensory & motor research.

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

[23]  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.

[24]  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.

[25]  J. Kaas,et al.  Connections of areas 3b and 1 of the parietal somatosensory strip with the ventroposterior nucleus in the owl monkey (Aotus trivirgatus) , 1979, The Journal of comparative neurology.

[26]  P. Manger,et al.  Extensive Divergence and Convergence in the Thalamocortical Projection to Monkey Somatosensory Cortex , 1998, The Journal of Neuroscience.

[27]  C. Gilbert,et al.  Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  Mriganka Sur,et al.  Morphology of single intracellularly stained axons terminating in area 3b of macaque monkeys , 1990, The Journal of comparative neurology.

[29]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[30]  J. Kaas,et al.  Limits on plasticity in somatosensory cortex of adult rats: hindlimb cortex is not reactivated after dorsal column section. , 1995, Journal of neurophysiology.

[31]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[32]  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.

[33]  Jon H. Kaas,et al.  Reorganization of sensory and motor systems in adult mammals after injury , 2001 .

[34]  D. J. Felleman,et al.  Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys , 1983, Neuroscience.

[35]  P. Manger,et al.  Plasticity of the somatosensory cortical map in macaque monkeys after chronic partial amputation of a digit , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[37]  J. Kaas,et al.  Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[39]  J. Crabtree,et al.  Monoclonal antibody Cat-301 selectively identifies a subset of nuclei in the cat's somatosensory thalamus , 1993, Journal of neurocytology.

[40]  J. Kaas,et al.  Growth of new brainstem connections in adult monkeys with massive sensory loss. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.