Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task.

1. Adult owl monkeys were trained to detect differences in the frequency of a tactile flutter-vibration stimulus above a 20-Hz standard. All stimuli were delivered to a constant skin site restricted to a small part of a segment of one finger. The frequency-difference discrimination performance of all but one of these monkeys improved progressively with training. 2. The distributed responses of cortical neurons ("maps") of the hand surfaces were defined in detail in somatosensory cortical area 3b. Representations of trained hands were compared with those of the opposite, untrained hand, and to the area 3b representations of hands in a second set of monkeys that were stimulated tactually in the same manner while these monkeys were attending to auditory stimuli (passive stimulation controls). 3. The cortical representations of the trained hands were substantially more complex in topographic detail than the representations of unstimulated hands or of passively stimulated control hands. 4. In all well-trained monkeys the representations of the restricted skin location trained in the behavioral task were significantly (1.5 to greater than 3 times) greater in area than were the representations of equivalent skin locations on control digits. However, the overall extents of the representations of behaviorally stimulated fingers were not larger than those of control fingers in the same hemisphere, or in opposite hemisphere controls. 5. The receptive fields representing the trained skin were significantly larger than receptive fields representing control digits in all but one trained monkey. The largest receptive fields were centered in the zone of representation of the behaviorally engaged skin, but they were not limited to it. Large receptive fields were recorded in a 1- to 2-mm-wide zone in the area 3b maps of trained hands. 6. Receptive-field sizes were also statistically significantly larger on at least one adjacent, untrained digit when compared with the receptive fields recorded on the homologous digit of the opposite hand. 7. There was an increase in the percent overlaps of receptive fields in the cortical zone of representation of the trained skin. A significant number of receptive fields were centered on the behaviorally trained skin site. 8. The effects of increased topographic complexity, increased representation of the trained skin location, increased receptive-field size, and increased receptive-field overlap were not observed in the representations of the untrained hands in these same monkeys. Only modest increases in topographic complexity were recorded in the representations of passively stimulated hands, and no effects on receptive-field size or overlap were noted.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  J COLE,et al.  Effects of small lesions in sensory cortex in trained monkeys. , 1954, Journal of neurophysiology.

[2]  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.

[3]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[4]  J. Semmes,et al.  A comparison of precentral and postcentral cortical lesions on somatosensory discrimination in the monkey. , 1972, Cortex; a journal devoted to the study of the nervous system and behavior.

[5]  K. O. Johnson,et al.  Reconstruction of population response to a vibratory stimulus in quickly adapting mechanoreceptive afferent fiber population innervating glabrous skin of the monkey. , 1974, Journal of neurophysiology.

[6]  J. Semmes,et al.  Further studies of anterior postcentral lesions in monkeys. , 1974, Cortex; a journal devoted to the study of the nervous system and behavior.

[7]  P. Wall,et al.  Restructuring of the somatotopic map and appearance of abnormal neuronal activity in the gracile nucleus after partial deafferentation , 1976, Experimental Neurology.

[8]  N. Weinberger,et al.  Differential plasticity of morphologically distinct neuron populations in the medical geniculate body of the cat during classical conditioning. , 1978, Behavioral biology.

[9]  D. Robinson,et al.  Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. , 1978, Journal of neurophysiology.

[10]  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.

[11]  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.

[12]  R H LaMotte,et al.  Disorders in somesthesis following lesions of parietal lobe. , 1979, Journal of neurophysiology.

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

[14]  D. Albe-Fessard,et al.  Organization of somatic thalamus in monkeys with and without section of dorsal spinal tracts , 1979, Brain Research.

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

[16]  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.

[17]  D. Robinson,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. , 1981, Journal of neurophysiology.

[18]  B. C. Motter,et al.  The influence of attentive fixation upon the excitability of the light- sensitive neurons of the posterior parietal cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  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.

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

[21]  B. Whitsel,et al.  Dose- and time-dependent effects of ketamine on SI neurons with cutaneous receptive fields. , 1982, Journal of neurophysiology.

[22]  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.

[23]  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.

[24]  P. Wall,et al.  Plasticity in the nucleus gracilis of the rat , 1983, Experimental Neurology.

[25]  R. Dykes,et al.  Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition , 1983, Brain Research.

[26]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[27]  M Carlson,et al.  Development of tactile discrimination capacity in Macaca mulatta. II. Effects of partial removal of primary somatic sensory cortex (SmI) in infants and juveniles. , 1984, Brain research.

[28]  T. P. S. Powell,et al.  The callosal connexions of the primary somatic sensory cortex in the monkey , 1985, Brain Research Reviews.

[29]  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.

[30]  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.

[31]  B. C. Motter,et al.  Common and differential effects of attentive fixation on the excitability of parietal and prestriate (V4) cortical visual neurons in the macaque monkey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  M. Merzenich,et al.  Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. , 1987, Progress in brain research.

[33]  H. Sakai,et al.  Enhancement of inferior temporal neurons during visual discrimination. , 1987, Journal of neurophysiology.

[34]  T. Sato,et al.  Effects of attention and stimulus interaction on visual responses of inferior temporal neurons in macaque. , 1988, Journal of neurophysiology.

[35]  M. Merzenich,et al.  Somatotopically inappropriate projections from thalamocortical neurons to the SI cortex of the cat demonstrated by the use of intracortical microstimulation. , 1988, Somatosensory research.

[36]  Michael B. Calford,et al.  Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation , 1988, Nature.

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

[39]  M. Merzenich,et al.  Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. , 1990, Journal of neurophysiology.

[40]  Michael Merzenich,et al.  Hebb-Type Dynamics is Sufficient to Account for the Inverse Magnification Rule in Cortical Somatotopy , 1990, Neural Computation.

[41]  M. Merzenich,et al.  Receptive-field changes induced by peripheral nerve stimulation in SI of adult cats. , 1990, Journal of neurophysiology.

[42]  G. Doetsch,et al.  Physiological changes in the somatosensory forepaw cerebral cortex of adult raccoons following lesions of a single cortical digit representation , 1990, Experimental Neurology.

[43]  G. Recanzone,et al.  Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task. , 1992, Journal of neurophysiology.

[44]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[45]  W M Jenkins,et al.  Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. , 1992, Journal of neurophysiology.