Spatial and Temporal Structure of Receptive Fields in Primate Somatosensory Area 3b: Effects of Stimulus Scanning Direction and Orientation

This is the third in a series of studies of the neural representation of tactile spatial form in somatosensory cortical area 3b of the alert monkey. We previously studied the spatial structure of >350 fingerpad receptive fields (RFs) with random-dot patterns scanned in one direction (DiCarlo et al., 1998) and at varying velocities (DiCarlo and Johnson, 1999). Those studies showed that area 3b RFs have a wide range of spatial structures that are virtually unaffected by changes in scanning velocity. In this study, 62 area 3b neurons were studied with three to eight scanning directions (58 with four or more directions). The data from all three studies are described accurately by an RF model with three components: (1) a single, central excitatory region of short duration, (2) one or more inhibitory regions, also of short duration, that are adjacent to and nearly synchronous with the excitation, and (3) a region of inhibition that overlaps the excitation partially or totally and is temporally delayed with respect to the first two components. The mean correlation between the observed RFs and the RFs predicted by this three-component model was 0.81. The three-component RFs also predicted orientation sensitivity and preferred orientation to a scanned bar accurately. The orientation sensitivity was determined most strongly by the intensity of the coincident RF inhibition in relation to the excitation. Both orientation sensitivity and this ratio were stronger in the supragranular and infragranular layers than in layer IV.

[1]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[2]  J. DiCarlo,et al.  Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey , 1999, The Journal of Neuroscience.

[3]  I N Bankman,et al.  Neural image transformation in the somatosensory system of the monkey: comparison of neurophysiological observations with responses in a neural network model. , 1990, Cold Spring Harbor symposia on quantitative biology.

[4]  R. Romo,et al.  Representation of moving tactile stimuli in the somatic sensory cortex of awake monkeys. , 1995, Journal of neurophysiology.

[5]  S. Andersson Intracellular Postsynaptic Potentials in the Somatosensory Cortex of the Cat , 1965, Nature.

[6]  Y. Iwamura,et al.  Regional diversity in excitatory and inhibitory receptive-field organization of cat thalamic ventrobasal neurons. , 1974, Journal of neurophysiology.

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

[8]  W. Spencer,et al.  Cutaneous masking. II. Geometry of excitatory andinhibitory receptive fields of single units in somatosensory cortex of the cat. , 1979, Journal of neurophysiology.

[9]  V. Mountcastle,et al.  Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey , 1991, Journal of Neuroscience Methods.

[10]  E. P. Gardner,et al.  A quantitative analysis of responses of direction-sensitive neurons in somatosensory cortex of awake monkeys. , 1980, Journal of neurophysiology.

[11]  William H. Press,et al.  Book-Review - Numerical Recipes in Pascal - the Art of Scientific Computing , 1989 .

[12]  W. Spencer,et al.  Temporal and spatial parameters of excitation and afferent inhibition in cuneothalamic relay neurons. , 1977, Journal of neurophysiology.

[13]  J Hyvärinen,et al.  Movement‐sensitive and direction and orientation‐selective cutaneous receptive fields in the hand area of the post‐central gyrus in monkeys. , 1978, The Journal of physiology.

[14]  S S Hsiao,et al.  Spatial pattern representation and transformation in monkey somatosensory cortex. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Steven S. Hsiao,et al.  Neural mechanisms of tactile form recognition , 1995 .

[16]  J. Eccles,et al.  The ventro‐basal complex of the thalamus: types of cells, their responses and their functional organization , 1964, The Journal of physiology.

[17]  Mountcastle Vb,et al.  The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. , 1959 .

[18]  William H. Press,et al.  Numerical Recipes in FORTRAN - The Art of Scientific Computing, 2nd Edition , 1987 .

[19]  Kenneth O. Johnson,et al.  A rotating drum stimulator for scanning embossed patterns and textures across the skin , 1988, Journal of Neuroscience Methods.

[20]  G M Innocenti,et al.  Response patterns of somatosensory cortical neurones to peripheral stimuli. An intracellular study. , 1972, Archives italiennes de biologie.

[21]  E P Gardner,et al.  Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys. , 1986, Journal of neurophysiology.

[22]  R. Dykes,et al.  Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. , 1984, Journal of neurophysiology.

[23]  T P POWELL,et al.  The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. , 1959, Bulletin of the Johns Hopkins Hospital.

[24]  E P Gardner,et al.  Temporal integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. , 1980, Journal of neurophysiology.

[25]  L. Pubols,et al.  Orientation detectors in the primary somatosensory neocortex of the raccoon , 1977, Brain Research.

[26]  A. Towe,et al.  Postsynaptic potential patterns evoked upon cells in sensorimotor cortex of cat by stimulation at the periphery. , 1968, Experimental neurology.

[27]  E. P. Gardner,et al.  Neuronal mechanisms underlying direction sensitivity of somatosensory cortical neurons in awake monkeys. , 1980, Journal of neurophysiology.

[28]  J. Eccles,et al.  MECHANISMS OF SYNAPTIC TRANSMISSION IN THE CUNEATE NUCLEUS. , 1964, Journal of neurophysiology.

[29]  John W. Lane,et al.  Marking microelectrode penetrations with fluorescent dyes , 1996, Journal of Neuroscience Methods.

[30]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

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

[32]  W. Spencer,et al.  Spatial and temporal features of afferent inhibition of thalamocortical relay cells. , 1979, Journal of neurophysiology.

[33]  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.

[34]  E P Gardner,et al.  Spatial integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. , 1980, Journal of Neurophysiology.

[35]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[36]  K. Mardia Statistics of Directional Data , 1972 .