The Journal of Neurophysiology Vol. 79 No. 4 April 1998, pp. 2119-2148
Copyright ©1998 The American Physiological Society

Plasticity of Primary Somatosensory Cortex Paralleling Sensorimotor Skill Recovery From Stroke in Adult Monkeys

Christian Xerri, Michael M. Merzenich, Bret E. Peterson, and William Jenkins

Keck Center and Coleman Laboratory, University of California at San Francisco, San Francisco, California 94143-0732

Xerri, Christian, Michael M. Merzenich, Bret E. Peterson, and William Jenkins. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J. Neurophysiol. 79: 2119-2148, 1998. Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with "substitution" and "vicariation" (adaptive plasticity) models of recovery from brain damage and stroke.

This article has been cited by other articles:

				A. Kumar, C. Juhasz, E. Asano, S.K. Sundaram, M.I. Makki, D.C. Chugani, and H.T. Chugani Diffusion Tensor Imaging Study of the Cortical Origin and Course of the Corticospinal Tract in Healthy Children AJNR Am. J. Neuroradiol., November 1, 2009; 30(10): 1963 - 1970. [Abstract] [Full Text] [PDF]

				A. Sigler, M. H. Mohajerani, and T. H. Murphy Imaging rapid redistribution of sensory-evoked depolarization through existing cortical pathways after targeted stroke in mice PNAS, July 14, 2009; 106(28): 11759 - 11764. [Abstract] [Full Text] [PDF]

				C. E. Brown, K. Aminoltejari, H. Erb, I. R. Winship, and T. H. Murphy In Vivo Voltage-Sensitive Dye Imaging in Adult Mice Reveals That Somatosensory Maps Lost to Stroke Are Replaced over Weeks by New Structural and Functional Circuits with Prolonged Modes of Activation within Both the Peri-Infarct Zone and Distant Sites J. Neurosci., February 11, 2009; 29(6): 1719 - 1734. [Abstract] [Full Text] [PDF]

				B. L. Whitsel, O. V. Favorov, Y. Li, M. Quibrera, and M. Tommerdahl Area 3a Neuron Response to Skin Nociceptor Afferent Drive Cereb Cortex, February 1, 2009; 19(2): 349 - 366. [Abstract] [Full Text] [PDF]

				A. O. Ballantyne, A. M. Spilkin, J. Hesselink, and D. A. Trauner Plasticity in the developing brain: intellectual, language and academic functions in children with ischaemic perinatal stroke Brain, November 1, 2008; 131(11): 2975 - 2985. [Abstract] [Full Text] [PDF]

				I. R. Winship and T. H. Murphy In Vivo Calcium Imaging Reveals Functional Rewiring of Single Somatosensory Neurons after Stroke J. Neurosci., June 25, 2008; 28(26): 6592 - 6606. [Abstract] [Full Text] [PDF]

				R. S. Marshall, J. J. Ferrera, A. Barnes, Xian Zhang, K. A. O'Brien, M. Chmayssani, J. Hirsch, and R. M. Lazar Brain Activity Associated With Stimulation Therapy of the Visual Borderzone in Hemianopic Stroke Patients Neurorehabil Neural Repair, April 1, 2008; 22(2): 136 - 144. [Abstract] [PDF]

				Y. Nishimura, H. Onoe, Y. Morichika, S. Perfiliev, H. Tsukada, and T. Isa Time-Dependent Central Compensatory Mechanisms of Finger Dexterity After Spinal Cord Injury Science, November 16, 2007; 318(5853): 1150 - 1155. [Abstract] [Full Text] [PDF]

				A.M.O. Bakheit, S. Shaw, L. Barrett, J. Wood, S. Carrington, S. Griffiths, K. Searle, and F. Koutsi A prospective, randomized, parallel group, controlled study of the effect of intensity of speech and language therapy on early recovery from poststroke aphasia Clinical Rehabilitation, October 1, 2007; 21(10): 885 - 894. [Abstract] [PDF]

				Y. Dong, C. J. Winstein, R. Albistegui-DuBois, and B. H. Dobkin Evolution of fMRI Activation in the Perilesional Primary Motor Cortex and Cerebellum With Rehabilitation Training-Related Motor Gains After Stroke: A Pilot Study Neurorehabil Neural Repair, October 1, 2007; 21(5): 412 - 428. [Abstract] [PDF]

				J. M. Smith, P. Lunga, D. Story, N. Harris, J. Le Belle, M. F James, J. D. Pickard, and J. W. Fawcett Inosine promotes recovery of skilled motor function in a model of focal brain injury Brain, April 1, 2007; 130(4): 915 - 925. [Abstract] [Full Text] [PDF]

				P. D. Marasco and K. C. Catania Response properties of primary afferents supplying Eimer's organ J. Exp. Biol., March 1, 2007; 210(5): 765 - 780. [Abstract] [Full Text] [PDF]

				K. M. Friel, S. Barbay, S. B. Frost, E. J. Plautz, A. M. Stowe, N. Dancause, E. V. Zoubina, and R. J. Nudo Effects of a Rostral Motor Cortex Lesion on Primary Motor Cortex Hand Representation Topography in Primates Neurorehabil Neural Repair, January 1, 2007; 21(1): 51 - 61. [Abstract] [PDF]

				D. Ramanathan, J. M. Conner, and M. H. Tuszynski A form of motor cortical plasticity that correlates with recovery of function after brain injury PNAS, July 25, 2006; 103(30): 11370 - 11375. [Abstract] [Full Text] [PDF]

				C. Gerloff, K. Bushara, A. Sailer, E. M. Wassermann, R. Chen, T. Matsuoka, D. Waldvogel, G. F. Wittenberg, K. Ishii, L. G. Cohen, et al. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke Brain, March 1, 2006; 129(3): 791 - 808. [Abstract] [Full Text] [PDF]

				K. M. Friel, S. Barbay, S. B. Frost, E. J. Plautz, D. M. Hutchinson, A. M. Stowe, N. Dancause, E. V. Zoubina, B. M. Quaney, and R. J. Nudo Dissociation of Sensorimotor Deficits After Rostral Versus Caudal Lesions in the Primary Motor Cortex Hand Representation J Neurophysiol, August 1, 2005; 94(2): 1312 - 1324. [Abstract] [Full Text] [PDF]

				A. Jaillard, C. D. Martin, K. Garambois, J. F. Lebas, and M. Hommel Vicarious function within the human primary motor cortex?: A longitudinal fMRI stroke study Brain, May 1, 2005; 128(5): 1122 - 1138. [Abstract] [Full Text] [PDF]

				K. R. Huxlin and T. Pasternak Training-induced Recovery of Visual Motion Perception after Extrastriate Cortical Damage in the Adult Cat Cereb Cortex, January 1, 2004; 14(1): 81 - 90. [Abstract] [Full Text] [PDF]

				S. B. Frost, S. Barbay, K. M. Friel, E. J. Plautz, and R. J. Nudo Reorganization of Remote Cortical Regions After Ischemic Brain Injury: A Potential Substrate for Stroke Recovery J Neurophysiol, June 1, 2003; 89(6): 3205 - 3214. [Abstract] [Full Text] [PDF]

				S. Barbay, E. K. Peden, G. Falchook, and R. J. Nudo An Index of Topographic Normality in Rat Somatosensory Cortex: Application to a Sciatic Nerve Crush Model J Neurophysiol, September 1, 2002; 88(3): 1339 - 1351. [Abstract] [Full Text] [PDF]

				S. L. Small, P. Hlustik, D. C. Noll, C. Genovese, and A. Solodkin Cerebellar hemispheric activation ipsilateral to the paretic hand correlates with functional recovery after stroke Brain, July 1, 2002; 125(7): 1544 - 1557. [Abstract] [Full Text] [PDF]

				J. H. Cauraugh and S. Kim Two Coupled Motor Recovery Protocols Are Better Than One: Electromyogram-Triggered Neuromuscular Stimulation and Bilateral Movements Stroke, June 1, 2002; 33(6): 1589 - 1594. [Abstract] [Full Text] [PDF]

				R. N. S. Sachdev and K. C. Catania Receptive Fields and Response Properties of Neurons in the Star-Nosed Mole's Somatosensory Fovea J Neurophysiol, May 1, 2002; 87(5): 2602 - 2611. [Abstract] [Full Text] [PDF]

				H Duffau, D Denvil, and L Capelle Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy J. Neurol. Neurosurg. Psychiatry, April 1, 2002; 72(4): 511 - 516. [Abstract] [Full Text] [PDF]

				S J BONIFACE Plasticity after acute ischaemic stroke studied by transcranial magnetic stimulation J. Neurol. Neurosurg. Psychiatry, December 1, 2001; 71(6): 713 - 715. [Full Text] [PDF]

				R. Pineiro, S. Pendlebury, H. Johansen-Berg, and P. M. Matthews Functional MRI Detects Posterior Shifts in Primary Sensorimotor Cortex Activation After Stroke : Evidence of Local Adaptive Reorganization? Stroke, May 1, 2001; 32(5): 1134 - 1139. [Abstract] [Full Text] [PDF]

				A. W. Dromerick, D. F. Edwards, and M. Hahn Does the Application of Constraint-Induced Movement Therapy During Acute Rehabilitation Reduce Arm Impairment After Ischemic Stroke? Stroke, December 1, 2000; 31(12): 2984 - 2988. [Abstract] [Full Text] [PDF]

				J. Cauraugh, K. Light, S. Kim, M. Thigpen, and A. Behrman Chronic Motor Dysfunction After Stroke : Recovering Wrist and Finger Extension by Electromyography-Triggered Neuromuscular Stimulation Stroke, June 1, 2000; 31(6): 1360 - 1364. [Abstract] [Full Text] [PDF]

				S. T. Bland, T. Schallert, R. Strong, J. Aronowski, J. C. Grotta, and D. M. Feeney Early Exclusive Use of the Affected Forelimb After Moderate Transient Focal Ischemia in Rats : Functional and Anatomic Outcome Editorial Comment: Functional and Anatomic Outcome Stroke, May 1, 2000; 31(5): 1144 - 1152. [Abstract] [Full Text] [PDF]

				S. C. Cramer, C. I. Moore, S. P. Finklestein, and B. R. Rosen A Pilot Study of Somatotopic Mapping After Cortical Infarct Stroke, March 1, 2000; 31(3): 668 - 671. [Abstract] [Full Text] [PDF]

				M. J. Aminoff Brown-Sequard: Selected Contributions of a Nineteenth-Century Neuroscientist Neuroscientist, February 1, 2000; 6(1): 60 - 65. [Abstract] [PDF]

				B. B. Johansson Brain Plasticity and Stroke Rehabilitation : The Willis Lecture Stroke, January 1, 2000; 31(1): 223 - 230. [Abstract] [Full Text] [PDF]

				R. J. Seitz, N. P. Azari, U. Knorr, F. Binkofski, H. Herzog, and H.-J. Freund The Role of Diaschisis in Stroke Recovery Stroke, September 1, 1999; 30(9): 1844 - 1850. [Abstract] [Full Text] [PDF]

				G. Nelles, G. Spiekermann, M. Jueptner, G. Leonhardt, S. Muller, H. Gerhard, and H. C. Diener Reorganization of Sensory and Motor Systems in Hemiplegic Stroke Patients : A Positron Emission Tomography Study Stroke, August 1, 1999; 30(8): 1510 - 1516. [Abstract] [Full Text] [PDF]

				C. Xerri, M. M. Merzenich, W. Jenkins, and S. Santucci Representational Plasticity in Cortical Area 3b Paralleling Tactual-motor Skill Acquisition in Adult Monkeys Cereb Cortex, April 1, 1999; 9(3): 264 - 276. [Abstract] [Full Text] [PDF]

				Y. Li, N. Jiang, C. Powers, M. Chopp, and B. B. Johansson Neuronal Damage and Plasticity Identified by Microtubule-Associated Protein 2, Growth-Associated Protein 43, and Cyclin D1 Immunoreactivity After Focal Cerebral Ischemia in Rats • Editorial Comment Stroke, September 1, 1998; 29(9): 1972 - 1981. [Abstract] [Full Text] [PDF]