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Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions

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Summary

In the accompanying paper (Sanes et al. 1989), we demonstrated that the map of motor cortex (MI) output was reorganized when examined 1 week to 4 months after a motor nerve lesion in adult rats. The present experiments measured the extent of functional reorganization that occurs within the first hours after this lesion. Shifts in MI output were examined by testing the effect of stimulation at a site in MI vibrissa area before and up to 10 h after nerve section of the branches of the facial nerve that innervate the vibrissa. Immediately following nerve transection, no movement or forelimb EMG activity was evoked by intracortical electrical stimulation within the vibrissa area. Within hours of the nerve transection, however, stimulation elicited forelimb EMG responses that were comparable to those obtained by stimulating within the pre-transection forelimb area. Remapping of MI after nerve transection indicated that the forelimb boundary had shifted about 1 mm medially from its original location into the former vibrissa territory. Forelimb EMG could be evoked for up to 10 h within this reorganized cortex. These results indicated that the output circuits of MI can be quickly reorganized by nerve lesions in adult mammals.

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References

  • Akhtar ND, Land PW (1987) The effects of sensory deprivation on glutamic acid decarboxylase immunoreactivity in the rat SmI barrel cortex. Neurosci Abstr 13: 77

    Google Scholar 

  • Brons JF, Woody CD (1980) Long-term changes in excitability of cortical neurons after Pavlovian conditioning and extinction. J Neurophysiol 44: 605–615

    Google Scholar 

  • Brown TG, Sherrington CS (1912) On the instability of a cortical point. Proc R Soc Lond [Biol] 85: 250–277

    Google Scholar 

  • Calford MB, Tweedale R (1988) Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature 332: 446–448

    Google Scholar 

  • Conrad B (1978) The motor cortex as a primary device for fast adjustment of programmed motor patterns to afferent signals. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Prog Clin Neurophysiol 4: 123–140

  • Cope TC, Nelson SG, Mendell LM (1980) Factors outside the neuraxis mediate the acute increase in EPSP amplitude caudal to spinal cord transection. J Neurophysiol 44: 174–183

    Google Scholar 

  • Craggs MD, Rushton DN (1976) The stability of the electrical stimulation map of the motor cortex of the anesthetized baboon. Brain 99: 575–600

    Google Scholar 

  • DeFelipe J, Conley M, Jones EG (1986) Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J Neurosci 6: 3749–3766

    Google Scholar 

  • Devor M, Wall PD (1978) Reorganization of spinal cord sensory map after peripheral nerve injury. Nature 276: 75–76

    Google Scholar 

  • Donoghue JP, Kitai S (1981) A collateral pathway to the neostriatum from corticofugal neurons of the rat sensorimotor cortex: an intracellular HRP study. J Comp Neurol 201: 1–13

    Google Scholar 

  • Donoghue JP, Sanes JN (1987) Peripheral nerve injury in developing rats reorganizes representation pattern in motor cortex. Proc Natl Acad Sci USA 84: 1123–1126

    Google Scholar 

  • Donoghue JP, Sanes JN (1988) Organization of adult motor cortex representation patterns following neonatal forelimb nerve injury in rats. J Neurosci 8: 3221–3232

    Google Scholar 

  • Donoghue JP, Suner S, Lando JF, Sanes JN (1987) Motor cortical representation patterns shift rapidly following motor nerve section. Neurosci Abstr 13: 242

    Google Scholar 

  • Dostrovsky JO, Millar J, Wall PD (1976) 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. Exp Neurol 52: 480–495

    Google Scholar 

  • Dykes RW, Landry P, Metherate R, Hicks TP (1984) Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J Neurophysiol 52: 1066–1093

    Google Scholar 

  • Endo K, Araki T, Yagi N (1973) The distribution and pattern of axon branching of pyramidal tract cells. Brain Res 57: 484–491

    Google Scholar 

  • Fetz EE, Cheney PD, German DC (1976) Corticomotoneuronal connections of precentral cells detected by post spike averages of EMG activity in behaving monkeys. Brain Res 114: 505–510

    Google Scholar 

  • Gellhorn E, Hyde J (1953) Influence of proprioception on map of cortical responses. J Physiol (Lond) 122: 371–385

    Google Scholar 

  • Gershoni H (1979) An investigation of behavior changes of subjects learning manual tasks. Ergonomics 22: 1195–1206

    Google Scholar 

  • Ghosh S, Porter R (1988) Corticocortical synaptic influences on morphologically identified pyramidal neurons in the motor cortex of the monkey. J Physiol (Lond) 400: 617–629

    Google Scholar 

  • Hendry SHC, Jones EG (1986) Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320: 750–753

    Google Scholar 

  • Hubel DH, Wiesel TN (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28: 1041–1059

    Google Scholar 

  • Hummelsheim H, Wiesendanger M (1986) Is the hindlimb representation of the rat's cortex a “sensorimotor amalgam”? Brain Res 346: 75–81

    Google Scholar 

  • Jacobs KM, Donoghue JP (1988) Inhibition shapes the size of motor cortex representations. Neurosci Abstr 14: 679

    Google Scholar 

  • Kennard MA (1942) Cortical reorganization of motor function: studies on series of monkeys of various ages from infancy to maturity. Arch Neurol Psychiat 47: 227–240

    Google Scholar 

  • Leyton ASF, Sherrington CS (1917) Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Q J Exp Physiol 11: 135–222

    Google Scholar 

  • Neilson PD, Lance JW (1978) Reflex transmission characteristics during voluntary activity in normal man and patients with movement disorders. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Prog Clin Neurophysiol 4: 263–299

  • Nelson SG, Collatos TC, Niechaj A, Mendell LM (1979) Immediate increase in Ia-motoneuron synaptic transmission caudal to spinal cord transection. J Neurophysiol 42: 655–664

    Google Scholar 

  • Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D (1983) 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. Neuroscience 10: 639–665

    Google Scholar 

  • Metzler J, Marks PS (1979) Functional changes in cat somatic sensory-motor cortex during short term reversible epidermal blocks. Brain Res 177: 379–383

    Google Scholar 

  • Milner-Brown HS, Stein RB, Lee RG (1975) Synchronization of human motor units: possible role of exercise and supraspinal reflexes. Electroenceph Clin Neurophysiol 38: 245–254

    Google Scholar 

  • Normand MC, Lagassé PP, Rouillard CA, Tremblay LE (1982) Modifications occurring in motor programs during learning of a complex task in man. Brain Res 241: 87–93

    Google Scholar 

  • Raisman G, Field PM (1973) A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei. Brain Res 50: 241–264

    Google Scholar 

  • Raivich G, Kreutzberg GW (1987) Expression of growth factor receptors in injured nervous tissue. I. Axotomy leads to a shift in the cellular distribution of specific beta-nerve growth factor binding in the injured and regenerating PNS. J Neurocytol 16: 689–700

    Google Scholar 

  • Rosén I, Asanuma H (1972) Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-ouput relations. Exp Brain Res 14: 257–273

    Google Scholar 

  • Sakamoto T, Porter LL, Asanuma H (1987) Long-lasting potentiation of synaptic potentials in the motor cortex produced by stimulation of the sensory cortex in the cat: a basis of motor learning. Brain Res 413: 360–364

    Google Scholar 

  • Sanes JN, Suner S, Lando JF, Donoghue JP (1988) Adult motor cortex representation patterns reorganize after motor nerve injury. Proc Natl Acad Sci USA 86: 2003–2007

    Google Scholar 

  • Sanes JN, Suner S, Donoghue JP (1989) Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp Brain Res 79: 479–491

    Google Scholar 

  • Sasaki K, Gemba H (1987) Plasticity of cortical function related to voluntary movement, motor learning, and compensation following brain dysfunction. Acta Neurochir 41: 18–28

    Google Scholar 

  • Schneider K, Zernicke RF (1989) Jerk-cost modulation during the learning of unrestrained arm movements. Biol Cyber 60: 221–230

    Google Scholar 

  • Sherman SM, Spear PD (1982) Organization of visual pathways in normal and visually deprived cats. Physiol Rev 62: 738–855

    Google Scholar 

  • Shinoda Y, Zarzeki P, Asanuma H (1979) Spinal branching of pyramidal tract neurons in the monkey. Exp Brain Res 34: 59–72

    Google Scholar 

  • Shinoda Y, Yamaguchi T, Futami T (1986) Multiple axon collaterals of single corticospinal axons in cat spinal cord. J Neurophysiol 55: 425–448

    Google Scholar 

  • Sievert CF, Neafsey EJ (1986) A chronic unit study of the sensory properties of neurons in the forelimb areas of rat sensorimotor cortex. Brain Res 381: 15–23

    Google Scholar 

  • Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol (Lond) 250: 305–329

    Google Scholar 

  • Strick PL, Preston JB (1982) Two representations of the hand in area 4 of a primate. II. Somatosensory input organization. J Neurophysiol 48: 150–159

    Google Scholar 

  • Tetzlaff W, Bisby MA, Kreutzberg GW (1988) Changes in cytoskeletal proteins in the rat facial nucleus following axotomy. J Neurosci 8: 3181–3189

    Google Scholar 

  • Wall PD, Egger MD (1971) Formation of new connections in adult rat brains after partial deafferentation. Nature 232: 542–545

    Google Scholar 

  • Yumiya H, Larsen KD, Asanuma H (1979) Motor readjustment and input-output relationship of motor cortex following cross-connection of forearm muscles in cats. Brain Res 177: 566–570

    Google Scholar 

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Authors and Affiliations

  1. Center for Neural Science, Brown University, Box 1953, 02912, Providence, RI, USA

    J. P. Donoghue, S. Suner & J. N. Sanes

  2. Human Motor Control Section, Medical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 20892, Bethesda, MD, USA

    J. N. Sanes

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  1. J. P. Donoghue
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  2. S. Suner
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  3. J. N. Sanes
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Donoghue, J.P., Suner, S. & Sanes, J.N. Dynamic organization of primary motor cortex output to target muscles in adult rats II. Rapid reorganization following motor nerve lesions. Exp Brain Res 79, 492–503 (1990). https://doi.org/10.1007/BF00229319

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  • DOI: https://doi.org/10.1007/BF00229319

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