Neuronal activity in normal and deafferented forelimb somatosensory cortex of the awake cat

Three hundred and seventy-three neurons were recorded from the forelimb representation in the primary somatosensory cortex of unanesthetized, quietly resting adult cats. Of these, 177 were studied from 2 days to 3 weeks after transection of the radial, median and ulnar nerves. Following deafferentation the proportion of cells without receptive fields increased from 24 to 82%, however, the average rate of spontaneous activity did not change nor did the probability of encountering a neuron with a receptive field as a function of depth. Receptive field sizes increased dramatically following deafferentation and the response changed from a reliable short-latency, brisk discharge to one that did not occur on every stimulus. After deafferentation the edges of the receptive field often could not be defined accurately. Spontaneous activity in 31% (n = 47) of the neurons from deprived cortex could be modulated by manipulations of the body but these changes were sufficiently slow and ill-defined that they were not classified as a receptive field. In some cases, manipulation of the body gradually reduced the discharge rate. This slow decline in activity was different from the abrupt inhibition of spontaneous activity elicited by somatic stimuli in another class of cells (n = 18). In other cases the manipulation produced a gradual increase in the discharge rate. After deafferentation antidromically identified corticothalamic and pyramidal tract neurons did not display behaviors different from their counterparts in normal cortex. However, the mean latency for synaptic activation from the ventroposterior thalamus increased from 2.7 ms to 4.6 ms. The lost forelimb receptive fields were rarely replaced by inputs from adjacent body parts over the two-week duration of this study. Most responses to somatic stimuli obtained from cortical neurons in the deafferented cortex were clearly abnormal.

[1]  P. Dutar,et al.  Somatosensory cortical neurons with an identifiable electrophysiological signature , 1988, Brain Research.

[2]  Y. Lamarre,et al.  A stereotaxic method for repeated sessions of central unit recording in the paralyzed or moving animal. , 1970, Revue canadienne de biologie.

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

[4]  G. Doetsch,et al.  Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. , 1984, Somatosensory research.

[5]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[6]  R. Dykes,et al.  An electrophysiological laminar analysis of single somatosensory neurons in partially deafferented rat hindlimb granular cortex subsequent to transection of the sciatic nerve , 1988, Brain Research.

[7]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[8]  D. Rasmusson,et al.  Reorganization of raccoon somatosensory cortex following removal of the fifth digit , 1982, The Journal of comparative neurology.

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

[10]  P. Zarzecki,et al.  Synaptic potentials evoked by convergent somatosensory and corticocortical inputs in raccoon somatosensory cortex: substrates for plasticity. , 1991, Journal of neurophysiology.

[11]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[12]  H. Swadlow Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. , 1989, Journal of neurophysiology.

[13]  L. Descarries,et al.  Decrease and long‐term recovery of choline acetyltransferase immunoreactivity in adult cat somatosensory cortex after peripheral nerve transections , 1995, The Journal of comparative neurology.

[14]  M. Calford,et al.  C-fibres provide a source of masking inhibition to primary somatosensory cortex , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  M. Armstrong‐James,et al.  Spatiotemporal convergence and divergence in the rat S1 “Barrel” cortex , 1987, The Journal of comparative neurology.

[16]  D. Rasmusson,et al.  Acute effects of total or partial digit denervation on raccoon somatosensory cortex. , 1990, Somatosensory & motor research.

[17]  R. H. Ray,et al.  Effects of early peripheral lesions on the somatotopic organization of the cerebral cortex. , 1981, Clinical neurosurgery.

[18]  R. Dykes,et al.  Neurons without demonstrable receptive fields outnumber neurons having receptive fields in samples from the somatosensory cortex of anesthetized or paralyzed cats and rats , 1988, Brain Research.

[19]  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.

[20]  J. Pettigrew,et al.  A variant of the mammalian somatotopic map in a bat , 1985, Nature.

[21]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[22]  M. Calford,et al.  Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation. , 1991, Somatosensory & motor research.

[23]  P. Zarzecki,et al.  Synaptic mechanisms of cortical representational plasticity: somatosensory and corticocortical EPSPs in reorganized raccoon SI cortex. , 1993, Journal of neurophysiology.

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

[25]  M Armstrong-James,et al.  Thalamo‐cortical processing of vibrissal information in the rat. II. Spatiotemporal convergence in the thalamic ventroposterior medial nucleus (VPm) and its relevance to generation of receptive fields of S1 cortical “Barrel” neurones , 1991, The Journal of comparative neurology.

[26]  M. Calford,et al.  Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox. , 1991, Journal of neurophysiology.

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

[28]  R. H. Ray,et al.  Functional reorganization of adult raccoon somatosensory cerebral cortex following neonatal digit amputation , 1981, Brain Research.

[29]  M. A. Friedman,et al.  Thalamo‐cortical processing of vibrissal information in the rat. I. Intracortical origins of surround but not centre‐receptive fields of layer IV neurones in the rat S1 barrel field cortex , 1991, The Journal of comparative neurology.

[30]  D. Rasmusson,et al.  Immediate effects of digit amputation on SI cortex in the raccoon: unmasking of inhibitory fields , 1983, Brain Research.

[31]  J. Kalaska,et al.  Chronic paw denervation causes an age-dependent appearance of novel responses from forearm in "paw cortex" of kittens and adult cats. , 1979, Journal of neurophysiology.

[32]  R. Dykes,et al.  An electrophysiological study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis. , 1988, Journal of neurophysiology.

[33]  J. Wall,et al.  Cutaneous responsiveness in primary somatosensory (S-I) hindpaw cortex before and after partial hindpaw deafferentation in adult rats , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  C. Palmer A microwire technique for recording single neurons in unrestrained animals , 1978, Brain Research Bulletin.

[35]  D. Rasmusson,et al.  Unexpected reorganization of somatosensory cortex in a raccoon with extensive forelimb loss , 1985, Neuroscience Letters.

[36]  R. Dykes,et al.  Magnification functions and receptive field sequences for submodality‐specific bands in SI cortex of cats , 1981, The Journal of comparative neurology.