Induction of bilateral plasticity in sensory cortical maps by small unilateral cortical infarcts in rats

Behavioural impairments caused by brain lesions show a considerable, though often incomplete, recovery. It is hypothesized that cortical and subcortical plasticity of sensory representations contribute to this recovery. In the hindpaw representation of somatosensory cortex of adult rats we investigated the effects of focal unilateral cortical lesions on remote areas. Cortical lesions with a diameter of ≈ 2 mm were induced in the parietal cortex by photothrombosis with the photosensitive dye Rose Bengal. Subsequently, animals were kept in standard cages for 7 days. On day seven, animals were anaesthetized and cutaneous receptive fields in the cortical hindpaw representations ipsi‐ and contralateral to the lesion were constructed from extracellular recordings of neurons in layer IV using glass microelectrodes. Receptive fields in the lesioned animals were compared to receptive fields measured in nonlesioned animals serving as controls. Quantitative analysis of receptive fields revealed a significant increase in size in the lesioned animals. This doubling in receptive field size was observed equally in the hemispheres ipsi‐ and contralateral to the lesion. The results indicate that the functional consequences of restricted cortical lesions are not limited to the area surrounding the lesion, but affect the cortical maps on the contralateral, nonlesioned hemisphere.

[1]  Prof. Dr. Karl Zilles.  The Cortex of the Rat , 1985, Springer Berlin Heidelberg.

[2]  H R Dinse,et al.  Reversible relocation of representational boundaries of adult rats by intracortical microstimulation. , 1994, Neuroreport.

[3]  J S Kim,et al.  Discriminative sensory dysfunction after unilateral stroke. , 1996, Stroke.

[4]  Liisa A. Tremere,et al.  Role of inhibition in cortical reorganization of the adult raccoon revealed by microiontophoretic blockade of GABA(A) receptors. , 2001, Journal of neurophysiology.

[5]  C. Monakow,et al.  Experimentelle und pathologisch-anatomische Untersuchungen über die Haubenregion, den Sehhügel und die Regio subthalamica, nebst Beiträgen zur Kenntniss früh erworbener Gross- und Kleinhirn-defecte , 2005, Archiv für Psychiatrie und Nervenkrankheiten.

[6]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[7]  M. Kotila,et al.  Epilepsy After Stroke , 1992, Epilepsia.

[8]  M Hallett,et al.  Modulation of practice-dependent plasticity in human motor cortex. , 2001, Brain : a journal of neurology.

[9]  H R Dinse,et al.  Effects of ageing on topographic organization of somatosensory cortex. , 1995, Neuroreport.

[10]  Karl J. Zilles,et al.  The Cortex of the Rat: A Stereotaxic Atlas , 1985 .

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

[12]  T. Poggio,et al.  Adaptation of Inputs in the Somatosensory System , 2002 .

[13]  K. Zilles,et al.  Neuronal Hyperexcitability and Reduction of GABAA-Receptor Expression in the Surround of Cerebral Photothrombosis , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  Jochen F Staiger,et al.  Enlargement of cortical vibrissa representation in the surround of an ischemic cortical lesion , 1999, Journal of the Neurological Sciences.

[15]  T. Neumann-Haefelin,et al.  Upregulation of GABAA-receptor alpha1- and alpha2-subunit mRNAs following ischemic cortical lesions in rats. , 1999, Brain research.

[16]  C. Monakow,et al.  Die Lokalisation im Grosshirn und der Abbau der Funktion durch kortikale Herde , 1914 .

[17]  T. Jones,et al.  Use-dependent growth of pyramidal neurons after neocortical damage , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  H. Dinse,et al.  Shifts in cortical representations predict human discrimination improvement , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[19]  G. Hagemann,et al.  Electrophysiological transcortical diaschisis after cortical photothrombosis in rat brain. , 1996, Stroke.

[20]  R. Busto,et al.  Induction of reproducible brain infarction by photochemically initiated thrombosis , 1985, Annals of neurology.

[21]  D. Feldman,et al.  Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. , 1999, Journal of neurobiology.

[22]  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.

[23]  R. Dykes,et al.  Bicuculline-induced alterations of response properties in functionally identified ventroposterior thalamic neurones , 2004, Experimental Brain Research.

[24]  H. Burton,et al.  Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats , 2004, Experimental Brain Research.

[25]  J. Kleim,et al.  Selective Synaptic Plasticity within the Cerebellar Cortex Following Complex Motor Skill Learning , 1998, Neurobiology of Learning and Memory.

[26]  C. Monakow,et al.  Experimentelle und pathologisch-anatomische Untersuchungen Ulber die Haufoenregion, den Sehhügel und die Regio subthalamica, nebst Beiträgen zur Kenntniss früh erworbener Gross- und Kleinhirndefecte , 1895, Archiv für Psychiatrie und Nervenkrankheiten.

[27]  E P Gardner,et al.  Simulation of motion on the skin. II. Cutaneous mechanoreceptor coding of the width and texture of bar patterns displaced across the OPTACON. , 1989, Journal of neurophysiology.

[28]  J. Kaas,et al.  Reorganization of Somatosensory Cortex After Nerve and Spinal Cord Injury. , 1998, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[29]  E P Gardner,et al.  Simulation of motion on the skin. I. Receptive fields and temporal frequency coding by cutaneous mechanoreceptors of OPTACON pulses delivered to the hand. , 1989, Journal of neurophysiology.

[30]  B. Godde,et al.  Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing. , 1997, Advances in neurology.

[31]  A. Schleicher,et al.  Transient increase of manganese-superoxide dismutase in remote brain areas after focal photothrombotic cortical lesion. , 1998, Stroke.

[32]  L. Carey,et al.  Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. , 1993, Archives of physical medicine and rehabilitation.

[33]  T. Neumann-Haefelin,et al.  Electrophysiological transcortical diaschisis after middle cerebral artery occlusion (MCAO) in rats , 1999, Neuroscience Letters.

[34]  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.

[35]  Hubert R. Dinse,et al.  Associative pairing of tactile stimulation induces somatosensory cortical reorganization in rats and humans , 1996, Neuroreport.

[36]  T. Neumann-Haefelin,et al.  Enhancement of whole cell calcium currents following transient MCAO , 2000, Brain Research.

[37]  T. Neumann-Haefelin,et al.  Upregulation of GABAA-receptor α1- and α2-subunit mRNAs following ischemic cortical lesions in rats , 1999, Brain Research.

[38]  M. Nicolelis,et al.  Immediate thalamic sensory plasticity depends on corticothalamic feedback. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  H. Dinse,et al.  Functional characterization of cutaneous mechanoreceptor properties in aged rats , 1996, Neuroscience Letters.

[40]  K Zilles,et al.  Structural alterations and changes in cytoskeletal proteins and proteoglycans after focal cortical ischemia , 1997, Neuroscience.

[41]  J. Dostrovsky,et al.  Cortical Involvement in the Induction, But Not Expression, of Thalamic Plasticity , 1999, The Journal of Neuroscience.

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

[43]  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.

[44]  J. Liepert,et al.  Motor cortex disinhibition in acute stroke , 2000, Clinical Neurophysiology.

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

[46]  U. Eysel,et al.  Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. , 1999, Cerebral cortex.

[47]  J. Liepert,et al.  Treatment-induced cortical reorganization after stroke in humans. , 2000, Stroke.

[48]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[49]  G. Hagemann,et al.  Brain Hypometabolism in a Model of Chronic Focal Epilepsy in Rat Neocortex , 1998, Epilepsia.

[50]  M. Hallett,et al.  Rapid plasticity of human cortical movement representation induced by practice. , 1998, Journal of neurophysiology.