Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys.

Recordings from the representations of the glabrous digits in area 3b of the somatosensory cortex of owl and macaque monkeys revealed two types of neurons. Rapidly adapting (RA) neurons responded only at the onset and offset of a 1-s skin indentation. Slowly adapting (SA) neurons also responded to stimulus onset and offset but, in addition, they responded throughout the 1-s skin indentation. RA neurons were found in all cortical layers while SA neurons were found only in the middle cortical layers. In electrode penetrations perpendicular to the layers, some penetrations encountered only RA neurons (RA penetrations), while other penetrations first encountered RA neurons, then SA neurons, and finally RA neurons again (SA penetrations). When closely spaced electrode penetrations were made throughout the representation of a single digit, it was apparent that RA and SA penetrations were not randomly distributed. The distribution suggested the existence of separate clusters or bands of SA and RA neurons in the middle layers of cortex. The predominant orientation of the SA and RA regions was rostrocaudally along the lengths of the digit representations. The SA and RA bands varied in width, had no systematic position in the representation of individual digits, and often crossed from the representation of one digit to another. Because of overlapping receptive fields for neurons in adjoining bands, the SA and RA bands appeared to represent the digits separately. This would allow all skin surfaces for each digit to be subserved by both types of neurons.

[1]  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.

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

[3]  J Hyvärinen,et al.  Receptive field integration and submodality convergence in the hand area of the post‐central gyrus of the alert monkey. , 1978, The Journal of physiology.

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

[5]  V. Mountcastle.  Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[6]  D. Hubel,et al.  Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor , 1974, The Journal of comparative neurology.

[7]  J. Kaas,et al.  Representations of the body surface in areas 3b and 1 of postcentral parietal cortex of cebus monkeys , 1983, Brain Research.

[8]  David P. Friedman,et al.  Focal projection of electrophysiologically defined groupings of thalamic cells on the monkey somatic sensory cortex , 1980, Brain Research.

[9]  V. Mountcastle,et al.  Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. , 1959, Bulletin of the Johns Hopkins Hospital.

[10]  V. Mountcastle,et al.  The problem of sensing and the neural coding of sensory events , 1967 .

[11]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[12]  Mountcastle Vb,et al.  Central nervous mechanisms subserving position sense and kinesthesis. , 1959 .

[13]  M. Descheˆnes,et al.  Geometry and orientation of thalamocortical arborizations in the cat somatosensory cortex as revealed by computer reconstruction , 1982, Brain Research.

[14]  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.

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

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

[17]  J Hyvärinen,et al.  Influence of attentive behavior on neuronal responses to vibration in primary somatosensory cortex of the monkey. , 1980, Journal of neurophysiology.

[18]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[19]  J. Chubbuck.  Small motion biological stimulator , 1966 .

[20]  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.

[21]  M. Deschenes,et al.  Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat , 1981, The Journal of comparative neurology.

[22]  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.

[23]  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.

[24]  B. Whitsel,et al.  Anterior parietal cortical topographic organization in macaque monkey: a reevaluation. , 1982, Journal of neurophysiology.

[25]  E. Jones,et al.  Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  F. O. Schmitt,et al.  The Organization of the Cerebral Cortex. , 1982 .

[27]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[28]  V. Mountcastle,et al.  Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. , 1959, Bulletin of the Johns Hopkins Hospital.

[29]  R. Dykes,et al.  The organization of two cutaneous submodalities in the forearm region of area 3b of cat somatosensory cortex , 1983, The Journal of comparative neurology.

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

[31]  J. Kaas,et al.  Modular segregation of functional cell classes within the postcentral somatosensory cortex of monkeys. , 1981, Science.

[32]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[33]  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.

[34]  R. Dykes,et al.  Organization of primary somatosensory cortex in the cat. , 1980, Journal of neurophysiology.

[35]  M Sugitani,et al.  Touching textured surfaces: cells in somatosensory cortex respond both to finger movement and to surface features. , 1982, Science.

[36]  B L Whitsel,et al.  Representation of head and face in postcentral gyrus of the macaque. , 1975, Journal of neurophysiology.

[37]  K. Andres,et al.  Morphology of cutaneous receptors. , 1982, Annual review of neuroscience.