Cortical connections to single digit representations in area 3b of somatosensory cortex in squirrel monkeys and prosimian galagos

The ventral posterior nucleus of thalamus sends highly segregated inputs into each digit representation in area 3b of primary somatosensory cortex. However, the spatial organization of the connections that link digit representations of areas 3b with other somatosensory areas is less understood. Here we examined the cortical inputs to individual digit representations of area 3b in four squirrel monkeys and one prosimian galago. Retrograde tracers were injected into neurophysiologically defined representations of individual digits of area 3b. Cortical tissues were cut parallel to the surface in some cases and showed that feedback projections to individual digits overlapped extensively in the hand representations of areas 3b, 1, and parietal ventral (PV) and second somatosensory (S2) areas. Other regions with overlapping populations of labeled cells included area 3a and primary motor cortex (M1). The results were confirmed in other cases in which the cortical tissues were cut in the coronal plane. The same cases also showed that cells were primarily labeled in the infragranular and supragranular layers. Thus, feedback projections to individual digit representations in area 3b mainly originate from multiple digits and other portions of hand representations of areas 3b, 1, PV, and S2. This organization is in stark contrast to the segregated thalamocortical inputs, which originate in single digit representations and terminate in the matching digit representation in the cortex. The organization of feedback connections could provide a substrate for the integration of information across the representations of adjacent digits in area 3b. J. Comp. Neurol. 521:3768–3790, 2013. © 2013 Wiley Periodicals, Inc.

[1]  J. Kaas,et al.  Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys , 1987, The Journal of comparative neurology.

[2]  J. Kaas,et al.  Architectonic Subdivisions of Neocortex in the Galago (Otolemur garnetti) , 2010, Anatomical record.

[3]  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.

[4]  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.

[5]  J. Kaas,et al.  Consistent features of the representation of the hand in area 3b of macaque monkeys. , 1987, Somatosensory research.

[6]  J. Kaas,et al.  The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex , 1979, The Journal of comparative neurology.

[7]  J. Kaas,et al.  Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: Comparisons with other primates , 1982, The Journal of comparative neurology.

[8]  Mriganka Sur,et al.  Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1 , 1985, Brain Research.

[9]  Jon H Kaas,et al.  Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch) , 2004, The Journal of comparative neurology.

[10]  J. Kaas,et al.  Myelin stains reveal an anatomical framework for the representation of the digits in somatosensory area 3b of macaque monkeys , 2004, The Journal of comparative neurology.

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

[12]  D. Rasmusson,et al.  Interactions between inputs from adjacent digits in somatosensory thalamus and cortex of the raccoon , 2003, Experimental Brain Research.

[13]  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.

[14]  Leah Krubitzer,et al.  The organization and connections of anterior and posterior parietal cortex in titi monkeys: do New World monkeys have an area 2? , 2005, Cerebral cortex.

[15]  E. G. Jones,et al.  Lamination and differential distribution of thalamic afferents within the sensory‐motor cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[16]  D. Pandya,et al.  Cortico‐cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey , 1978, The Journal of comparative neurology.

[17]  J. H. Kaas,et al.  Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1 , 1990, Brain Research.

[18]  J. Kaas,et al.  Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. , 2009, Cerebral cortex.

[19]  S. Nelson,et al.  Dynamics of neuronal processing in rat somatosensory cortex , 1999, Trends in Neurosciences.

[20]  J. Kaas,et al.  Central projections from the skin of the hand in squirrel monkeys , 1991, The Journal of comparative neurology.

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

[22]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[23]  Anna W Roe,et al.  Responses of areas 3b and 1 in anesthetized squirrel monkeys to single- and dual-site stimulation of the digits. , 2008, Journal of neurophysiology.

[24]  Melanie R. Bernard,et al.  Response properties of neurons in primary somatosensory cortex of owl monkeys reflect widespread spatiotemporal integration. , 2010, Journal of neurophysiology.

[25]  H. Burton,et al.  Vibrotactile stimulus order effects in somatosensory cortical areas of rhesus monkeys. , 1998, Somatosensory & motor research.

[26]  Anna W Roe,et al.  Intrinsic horizontal connections process global tactile features in the primary somatosensory cortex: Neuroanatomical evidence , 2013, The Journal of comparative neurology.

[27]  Pramodsingh H Thakur,et al.  Second-order receptive fields reveal multidigit interactions in area 3b of the macaque monkey. , 2012, Journal of neurophysiology.

[28]  K. Sathian,et al.  Altered responses to cutaneous stimuli in the second somatosensory cortex following lesions of the postcentral gyrus in infant and juvenile macaques , 1990, The Journal of comparative neurology.

[29]  Melanie R. Bernard,et al.  Widespread spatial integration in primary somatosensory cortex , 2008, Proceedings of the National Academy of Sciences.

[30]  Hubert Preissl,et al.  The right hand knows what the left hand is feeling , 2005, Experimental Brain Research.

[31]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  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.

[33]  J. DiCarlo,et al.  Structure of Receptive Fields in Area 3b of Primary Somatosensory Cortex in the Alert Monkey , 1998, The Journal of Neuroscience.

[34]  T. Brushart,et al.  Somatotopy of digital nerve projections to the cuneate nucleus in the monkey. , 1989, Somatosensory & motor research.

[35]  K. Rockland,et al.  Giant Neurons in the Macaque Pulvinar: A Distinct Relay Subpopulation , 2007, Frontiers in neuroanatomy.

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

[37]  D J Felleman,et al.  Somatotopic organization of the lateral sulcus of owl monkeys: Area 3b, s‐II, and a ventral somatosensory area , 1989, The Journal of comparative neurology.

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

[39]  E. G. Jones,et al.  Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Iwona Stepniewska,et al.  Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys. , 2011, Cerebral cortex.

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

[42]  Greg C. Champney,et al.  Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex , 2006, Experimental Brain Research.

[43]  H. Burton,et al.  Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates , 1976, The Journal of comparative neurology.

[44]  David P. Friedman,et al.  Representation pattern in the second somatic sensory area of the monkey cerebral cortex , 1980, The Journal of comparative neurology.

[45]  M. Sur,et al.  Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains , 1996, Journal of Neuroscience Methods.

[46]  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.

[47]  E G Jones,et al.  Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  J. Kaas,et al.  Reorganization of Somatosensory Cortex After Nerve and Spinal Cord Injury. , 1998, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[49]  Jon H Kaas,et al.  Evolution of somatosensory and motor cortex in primates. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[50]  S. Shimegi,et al.  Physiological and Anatomical Organization of Multiwhisker Response Interactions in the Barrel Cortex of Rats , 2000, The Journal of Neuroscience.

[51]  PL Strick,et al.  Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Hui-Xin Qi,et al.  Cell‐poor septa separate representations of digits in the ventroposterior nucleus of the thalamus in monkeys and prosimian galagos , 2011, The Journal of comparative neurology.

[53]  Neeraj Jain,et al.  Few intrinsic connections cross the hand‐face border of area 3b of New World monkeys , 2002, The Journal of comparative neurology.

[54]  L. Krubitzer,et al.  Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: Evidence for SII and PV , 2000, The Journal of comparative neurology.

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

[56]  G. T. Coleman,et al.  Functional characteristics of the parallel SI- and SII-projecting neurons of the thalamic ventral posterior nucleus in the marmoset. , 2001, Journal of neurophysiology.

[57]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[58]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. , 1969, Brain : a journal of neurology.

[59]  E. G. Jones The Ventral Nuclei , 1985 .

[60]  J. Kaas,et al.  Ablations of areas 3b (SI proper) and 3a of somatosensory cortex in marmosets deactivate the second and parietal ventral somatosensory areas. , 1990, Somatosensory & motor research.

[61]  M. Stryker,et al.  Anesthetic state does not affect the map of the hand representation within area 3b somatosensory cortex in owl monkey , 1987, The Journal of comparative neurology.

[62]  Melanie R. Bernard,et al.  Effects of spatiotemporal stimulus properties on spike timing correlations in owl monkey primary somatosensory cortex. , 2012, Journal of neurophysiology.

[63]  L. Heimer,et al.  In vivo anterograde and retrograde axonal trnasport of the fluoresecent rhodamine-dextran-amine, Fluor-Ruby, within the CNS , 1990, Brain Research.

[64]  J. Kaas The functional organization of somatosensory cortex in primates. , 1993, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[65]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. 3. Thalamic connexions. , 1970, Brain : a journal of neurology.

[66]  J. Kaas,et al.  The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys , 1986, The Journal of comparative neurology.

[67]  Takeshi Kaneko,et al.  Complementary distribution of vesicular glutamate transporters in the central nervous system , 2002, Neuroscience Research.

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

[69]  J. Kaas,et al.  Somatotopic organization of inputs from the hand to the spinal gray and cuneate nucleus of monkeys with observations on the cuneate nucleus of humans , 1989, The Journal of comparative neurology.

[70]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[71]  Jon H Kaas,et al.  Somatosensory cortex of prosimian Galagos: Physiological recording, cytoarchitecture, and corticocortical connections of anterior parietal cortex and cortex of the lateral sulcus , 2003, The Journal of comparative neurology.

[72]  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.

[73]  Jamie L. Reed,et al.  Spatiotemporal Properties of Neuron Response Suppression in Owl Monkey Primary Somatosensory Cortex When Stimuli Are Presented to Both Hands , 2011, The Journal of Neuroscience.

[74]  H. Sato,et al.  Temporal Characteristics of Response Integration Evoked by Multiple Whisker Stimulations in the Barrel Cortex of Rats , 1999, The Journal of Neuroscience.

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

[76]  Mark Tommerdahl,et al.  Ipsilateral Input Modifies the Primary Somatosensory Cortex Response to Contralateral Skin Flutter , 2006, The Journal of Neuroscience.

[77]  David C Lyon,et al.  Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus) , 2002, The Journal of comparative neurology.

[78]  K. Kultas‐Ilinsky,et al.  Reevaluation of the primary motor cortex connections with the thalamus in primates , 2003, The Journal of comparative neurology.

[79]  J. Kaas,et al.  Double representation of the body surface within cytoarchitectonic area 3b and 1 in “SI” in the owl monkey (aotus trivirgatus) , 1978, The Journal of comparative neurology.

[80]  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.

[81]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[82]  R. Lemon,et al.  Direct and indirect corticospinal control of arm and hand motoneurons in the squirrel monkey (Saimiri sciureus). , 1997, Journal of neurophysiology.

[83]  David P. Friedman,et al.  Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch , 1986, The Journal of comparative neurology.

[84]  David P. Friedman,et al.  Physiological evidence for serial processing in somatosensory cortex. , 1987, Science.

[85]  Troy A. Hackett,et al.  Regional and laminar distribution of the vesicular glutamate transporter, VGluT2, in the macaque monkey auditory cortex , 2009, Journal of Chemical Neuroanatomy.

[86]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[87]  Mara Fabri,et al.  Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys , 1995, The Journal of comparative neurology.

[88]  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.

[89]  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.

[90]  Leah Krubitzer,et al.  Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys , 2003, The Journal of comparative neurology.

[91]  M. Sur Receptive fields of neurons in areas 3b and 1 of somatosensory cortex in monkeys , 1980, Brain Research.

[92]  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.

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

[94]  J. Kaas,et al.  Interhemispheric connections of cortical sensory areas in tree shrews , 1985, The Journal of comparative neurology.

[95]  Iwona Stepniewska,et al.  Thalamocortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in New World monkeys. , 2010, Cerebral cortex.

[96]  J. Wall,et al.  Evidence for Brainstem and Supra-Brainstem Contributions to Rapid Cortical Plasticity in Adult Monkeys , 1999, The Journal of Neuroscience.