Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex.

After long-term denervation of an upper limb in macaque monkeys, the representation of the face in somatosensory cortex expands over many millimeters into the silenced representation of the hand. Various brainstem and cortical mechanisms have been proposed to explain this phenomenon. Reorganization in the thalamus has been largely ignored. In monkeys with deafferented upper limbs for 12 to 20 years, it was found that the brainstem cuneate and the thalamic ventral posterior nuclei had undergone severe transneuronal atrophy, and physiological mapping in the thalamus revealed that the face and trunk representations were adjoined while the normally small representation of the lower face had expanded comparable to the expansion in cortex. Reorganization of brainstem and thalamic nuclei associated with slow transneuronal atrophy is likely to be a progressive process. When coupled with divergence of ascending connections, it is likely to make a substantial contribution to representational changes in cortex.

[1]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[2]  G. Recanzone,et al.  Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation. , 1992, Cerebral cortex.

[3]  C Xerri,et al.  Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. , 1998, Journal of neurophysiology.

[4]  P. Garraghty,et al.  Somatotopic consolidation: a third phase of reorganization after peripheral nerve injury in adult squirrel monkeys , 1998, Experimental Brain Research.

[5]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[6]  V. Mountcastle,et al.  The representation of tactile sensibility in the thalamus of the monkey , 1952, The Journal of comparative neurology.

[7]  C. Shatz,et al.  Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  J. Kaas,et al.  Functional reorganization in adult monkey thalamus after peripheral nerve injury , 1991, Neuroreport.

[9]  C Pantev,et al.  Reorganizational and perceptional changes after amputation. , 1996, Brain : a journal of neurology.

[10]  V. Ramachandran,et al.  Perceptual correlates of massive cortical reorganization. , 1992, Neuroreport.

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

[12]  T. Powell Transneuronal Cell Degeneration in the Olfactory Bulb shown by the Golgi Method , 1967, Nature.

[13]  P. Wall,et al.  The immediate shift of afferent drive of dorsal column nucleus cells following deafferentation: A comparison of acute and chronic deafferentation in gracile nucleus and spinal cord , 1976, Experimental Neurology.

[14]  M. Nicolelis,et al.  Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information , 1993, Nature.

[15]  E G Jones,et al.  Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[17]  D. Rasmusson Changes in the organization of the ventroposterior lateral thalamic nucleus after digit removal in adult raccoon , 1996, The Journal of comparative neurology.

[18]  H. Schwark,et al.  Receptive field reorganization in dorsal column nuclei during temporary denervation. , 1993, Science.

[19]  H. Killackey,et al.  Receptive-field properties of rat ventral posterior medial neurons before and after selective kainic acid lesions of the trigeminal brain stem complex. , 1987, Journal of neurophysiology.

[20]  M. D. Egger,et al.  Formation of New Connexions in Adult Rat Brains after Partial Deafferentation , 1971, Nature.

[21]  J. Kaas,et al.  Pattern of peripheral deafferentation predicts reorganizational limits in adult primate somatosensory cortex. , 1994, Somatosensory & motor research.

[22]  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.

[23]  J. Kaas,et al.  Consistent features of the representation of the hand in area 3b of macaque monkeys. , 1987, Somatosensory research.

[24]  J. Dostrovsky,et al.  A Focal Zone of Thalamic Plasticity , 1998, The Journal of Neuroscience.

[25]  J. Hahm,et al.  Cortically induced thalamic plasticity in the primate somatosensory system , 1998, Nature Neuroscience.

[26]  J. Wall,et al.  The consistency, extent, and locations of early-onset changes in cortical nerve dominance aggregates following injury of nerves to primate hands , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  J. Kaas,et al.  Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M P Stryker,et al.  Rapid remodeling of axonal arbors in the visual cortex. , 1993, Science.

[29]  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.

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

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

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

[33]  J. Kalaska,et al.  Chronic peripheral nerve injuries alter the somatotopic organization of the cuneate nucleus in kittens , 1982, Brain Research.

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

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

[36]  Hyung-Cheul Shin,et al.  Responses from new receptive fields of VPL neurones following deafferentation , 1995, Neuroreport.

[37]  H C Kwan,et al.  Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection. , 1994, Journal of neurophysiology.

[38]  J. Kaas,et al.  Limits on plasticity in somatosensory cortex of adult rats: hindlimb cortex is not reactivated after dorsal column section. , 1995, Journal of neurophysiology.

[39]  P. Taylor,et al.  Identification of nicotinic receptor ACh-binding subunits , 1990, Trends in Neurosciences.