Somatosensory Cortex of Macaque Monkeys is Designed for Opposable Thumb

The evolution of opposable thumb has enabled fine grasping ability and precision grip, which led to the capacity for fine manipulation of objects and refined tool use. Since tactile inputs to an opposable thumb are often spatially and temporally out of synch with inputs from the fingers, we hypothesized that inputs from the opposable thumb would be processed in an independent module in the primary somatosensory cortex (area 3b). Here we show that in area 3b of macaque monkeys, most neurons in the thumb representation do not respond to tactile stimulation of other digits and receive few intrinsic cortical inputs from other digits. However, neurons in the representations of other digits respond to touch on any of the four digits and are significantly more interconnected in the cortex. The thumb inputs are thus processed in an independent module, whereas there is significantly more inter-digital information exchange between the other digits. This cortical organization reflects behavioral use of the hand with an opposable thumb.

[1]  Jon H. Kaas,et al.  Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys , 2013, Behavioural Brain Research.

[2]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[3]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

[4]  S. Levay,et al.  The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  E Burdet,et al.  Somatotopic Mapping of the Developing Sensorimotor Cortex in the Preterm Human Brain , 2018, Cerebral cortex.

[6]  C. Leonard,et al.  Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions. , 1992, Somatosensory & motor research.

[7]  The Journal of Comparative Neurology , 1899, The American Naturalist.

[8]  Jon H. Kaas,et al.  Large-Scale Reorganization in the Somatosensory Cortex and Thalamus after Sensory Loss in Macaque Monkeys , 2008, The Journal of Neuroscience.

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

[10]  C. Sherwood,et al.  Comparative analysis of Meissner's corpuscles in the fingertips of primates , 2015, Journal of anatomy.

[11]  F. Ebner,et al.  Effect of Enriched Environment Rearing on Impairments in Cortical Excitability and Plasticity after Prenatal Alcohol Exposure , 1999, The Journal of Neuroscience.

[12]  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.

[13]  J. Kaas,et al.  Responsiveness and somatotopic organization of anterior parietal field 3b and adjoining cortex in newborn and infant monkeys. , 1988, Somatosensory & motor research.

[14]  D. Fragaszy,et al.  Prehension in Cebus and Saimiri: I. Grip type and hand preference , 1988, American Journal of Primatology.

[15]  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.

[16]  A. Reiner,et al.  Pathway tracing using biotinylated dextran amines , 2000, Journal of Neuroscience Methods.

[17]  Niranjan Kambi,et al.  Large-Scale Expansion of the Face Representation in Somatosensory Areas of the Lateral Sulcus after Spinal Cord Injuries in Monkeys , 2009, The Journal of Neuroscience.

[18]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[19]  Variation in form of the pyramidal tract and its relationship to digital dexterity. , 1975, Brain, behavior and evolution.

[20]  K. Sathian,et al.  Tactile spatial acuity at the human fingertip and lip , 1996, Neurology.

[21]  D. Hubel,et al.  Extent of recovery from the effects of visual deprivation in kittens. , 1965, Journal of neurophysiology.

[22]  M. Weliky,et al.  Functional mapping of horizontal connections in developing ferret visual cortex: experiments and modeling , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  J. Diedrichsen,et al.  Hand use predicts the structure of representations in sensorimotor cortex , 2015, Nature Neuroscience.

[24]  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.

[25]  N. Jain,et al.  Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries , 2015, The Journal of Neuroscience.

[26]  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.

[27]  Niranjan Kambi,et al.  Reorganization of the Primary Motor Cortex of Adult Macaque Monkeys after Sensory Loss Resulting from Partial Spinal Cord Injuries , 2011, The Journal of Neuroscience.

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

[29]  Jerald D. Kralik,et al.  Chronic, multisite, multielectrode recordings in macaque monkeys , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[31]  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.

[32]  J. Gore,et al.  The Relationship of Anatomical and Functional Connectivity to Resting-State Connectivity in Primate Somatosensory Cortex , 2013, Neuron.

[33]  M W Marzke,et al.  Precision grips, hand morphology, and tools. , 1997, American journal of physical anthropology.

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

[35]  J. Kaas,et al.  The Organization of the Somatosensory System in Primates , 2001 .

[36]  Anna W. Roe,et al.  The Functional Architecture of Area V2 in the Macaque Monkey , 1997 .

[37]  J. Kaas,et al.  GAP-43 expression in the medulla of macaque monkeys: changes during postnatal development and the effects of early median nerve repair. , 1995, Brain research. Developmental brain research.

[38]  N. Jain,et al.  Two whisker motor areas in the rat cortex: Evidence from thalamocortical connections , 2014, The Journal of comparative neurology.

[39]  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.

[40]  M. Sur,et al.  Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex , 2000, Neuron.

[41]  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.

[42]  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.

[43]  A. Grinvald,et al.  The Cortical Representation of the Hand in Macaque and Human Area S-I: High Resolution Optical Imaging , 2001, The Journal of Neuroscience.

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

[45]  M. Graziano,et al.  Diversity of grip in Macaca mulatta , 2009, Experimental Brain Research.

[46]  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.

[47]  Niranjan Kambi,et al.  Large-scale reorganization of the somatosensory cortex following spinal cord injuries is due to brainstem plasticity , 2014, Nature Communications.

[48]  E. Jones Distribution patterns of individual medial lemniscal axons in the ventrobasal complex of the monkey thalamus , 1983, The Journal of comparative neurology.

[49]  Chia-Chi Liao,et al.  Cortical connections to single digit representations in area 3b of somatosensory cortex in squirrel monkeys and prosimian galagos , 2013, The Journal of comparative neurology.

[50]  C. Schroeder,et al.  Interactions within the Hand Representation in Primary Somatosensory Cortex of Primates , 2010, The Journal of Neuroscience.

[51]  Neeraj Jain,et al.  Cortical and thalamic connections of the representations of the teeth and tongue in somatosensory cortex of new world monkeys , 2007, The Journal of comparative neurology.

[52]  Finn A. GENnS Distribution of Acetyl Cholinesterase in the Hippocampal Region of the Guinea Pig , 1972 .

[53]  H. Killackey,et al.  Patterning of local intracortical projections within the vibrissae representation of rat primary somatosensory cortex , 1995, The Journal of comparative neurology.

[54]  N. Jain,et al.  Ipsilateral cortical inputs to the rostral and caudal motor areas in rats , 2016, The Journal of comparative neurology.

[55]  J. Napier The prehensile movements of the human hand. , 1956, The Journal of bone and joint surgery. British volume.

[56]  J. Kaas,et al.  Magnification, receptive-field area, and "hypercolumn" size in areas 3b and 1 of somatosensory cortex in owl monkeys. , 1980, Journal of neurophysiology.

[57]  J. Horton,et al.  Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. , 1984, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.