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      Recovery after brain injury: mechanisms and principles

      review-article
      Frontiers in Human Neuroscience
      Frontiers Media S.A.
      motor cortex, stroke, traumatic brain injury, axonal sprouting, motor learning, recovery

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          Abstract

          The past 20 years have represented an important period in the development of principles underlying neuroplasticity, especially as they apply to recovery from neurological injury. It is now generally accepted that acquired brain injuries, such as occur in stroke or trauma, initiate a cascade of regenerative events that last for at least several weeks, if not months. Many investigators have pointed out striking parallels between post-injury plasticity and the molecular and cellular events that take place during normal brain development. As evidence for the principles and mechanisms underlying post-injury neuroplasticity has been gleaned from both animal models and human populations, novel approaches to therapeutic intervention have been proposed. One important theme has persisted as the sophistication of clinicians and scientists in their knowledge of neuroplasticity mechanisms has grown: behavioral experience is the most potent modulator of brain plasticity. While there is substantial evidence for this principle in normal, healthy brains, the injured brain is particularly malleable. Based on the quantity and quality of motor experience, the brain can be reshaped after injury in either adaptive or maladaptive ways. This paper reviews selected studies that have demonstrated the neurophysiological and neuroanatomical changes that are triggered by motor experience, by injury, and the interaction of these processes. In addition, recent studies using new and elegant techniques are providing novel perspectives on the events that take place in the injured brain, providing a real-time window into post-injury plasticity. These new approaches are likely to accelerate the pace of basic research, and provide a wealth of opportunities to translate basic principles into therapeutic methodologies.

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          Most cited references89

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          Compensatory strategies for reaching in stroke.

          A major prerequisite for successful rehabilitation therapy after stroke is the understanding of the mechanisms underlying motor deficits common to these patients. Studies have shown that in stroke patients multijoint pointing movements are characterized by decreased movement speed and increased movement variability, by increased movement segmentation and by spatial and temporal incoordination between adjacent arm joints with respect to healthy subjects. We studied how the damaged nervous system recovers or compensates for deficits in reaching, and correlated reaching deficits with the level of functional impairment. Nine right-hemiparetic subjects and nine healthy subjects participated. All subjects were right-hand dominant. Data from the affected arm of hemiparetic subjects were compared with those from the arm in healthy subjects. Seated subjects made 40 pointing movements with the right arm in a single session. Movements were made from an initial target, for which the arm was positioned alongside the trunk. Then the subject lifted the arm and pointed to the final target, located in front of the subject in the contralateral workspace. Kinematic data from the arm and trunk were recorded with a three-dimensional analysis system. Arm movements in stroke subjects were longer, more segmented, more variable and had larger movement errors. Elbow-shoulder coordination was disrupted and the range of active joint motion was decreased significantly compared with healthy subjects. Some aspects of motor performance (duration, segmentation, accuracy and coordination) were significantly correlated with the level of motor impairment. Despite the fact that stroke subjects encountered all these deficits, even subjects with the most severe motor impairment were able to transport the end-point to the target. All but one subject involved the trunk to accomplish this motor task. In others words, they recruited new degrees of freedom typically not used by healthy subjects. The use of compensatory strategies may be related to the degree of motor impairment: severely to moderately impaired subjects recruited new degrees of freedom to compensate for motor deficits while mildly impaired subjects tended to employ healthy movement patterns. We discuss the possibility that there is a critical level of recovery at which patients switch from a strategy employing new degrees of freedom to one in which motor recovery is produced by improving the management of degrees of freedom characteristic of healthy performance. Our data also suggest that stroke subjects may be able to exploit effectively the redundancy of the motor system.
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            Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct.

            Substantial functional reorganization takes place in the motor cortex of adult primates after a focal ischemic infarct, as might occur in stroke. A subtotal lesion confined to a small portion of the representation of one hand was previously shown to result in a further loss of hand territory in the adjacent, undamaged cortex of adult squirrel monkeys. In the present study, retraining of skilled hand use after similar infarcts resulted in prevention of the loss of hand territory adjacent to the infarct. In some instances, the hand representations expanded into regions formerly occupied by representations of the elbow and shoulder. Functional reorganization in the undamaged motor cortex was accompanied by behavioral recovery of skilled hand function. These results suggest that, after local damage to the motor cortex, rehabilitative training can shape subsequent reorganization in the adjacent intact cortex, and that the undamaged motor cortex may play an important role in motor recovery.
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              The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography.

              We have studied regional cerebral blood flow changes in 6 patients after their recovery from a first hemiplegic stroke. All had a single well-defined hemispheric lesion and at least a brachial monoparesis that subsequently recovered. Each patient had 6 measurements of cerebral blood flow by positron tomography with 2 scans at rest, 2 during movement of fingers of the recovered hand, and 2 during movement of fingers of the normal hand. When the normal fingers were moved, regional cerebral blood flow increased significantly in contralateral primary sensorimotor cortex and in the ipsilateral cerebellar hemisphere. When the fingers of the recovered hand were moved, significant regional cerebral blood flow increases were observed in both contralateral and ipsilateral primary sensorimotor cortex and in both cerebellar hemispheres. Other regions, namely, insula, inferior parietal, and premotor cortex, were also bilaterally activated with movement of the recovered hand. We have also demonstrated, by using a new technique of image analysis, different functional connections between the thalamic nuclei and specific cortical and cerebellar regions during these movements. Our results suggest that ipsilateral motor pathways may play a role in the recovery of motor function after ischemic stroke.
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                Author and article information

                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                24 December 2013
                2013
                : 7
                : 887
                Affiliations
                Department of Molecular and Integrative Physiology, Landon Center on Aging, University of Kansas Medical Center Kansas, KS, USA
                Author notes

                Edited by: Edward Taub, University of Alabama at Birmingham, USA

                Reviewed by: Athena Demertzi, University of Liège, Belgium; Gitendra Uswatte, University of Alabama at Birmingham, USA

                *Correspondence: Randolph J. Nudo, Department of Molecular and Integrative Physiology, Landon Center on Aging, University of Kansas Medical Center, 3901 Rainbow Boulevard, MS 1005, Kansas, KS 66160, USA e-mail: rnudo@ 123456kumc.edu

                This article was submitted to the journal Frontiers in Human Neuroscience.

                Article
                10.3389/fnhum.2013.00887
                3870954
                24399951
                08d52c25-90f0-4423-87c1-7832f4a9b352
                Copyright © 2013 Nudo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 06 November 2013
                : 05 December 2013
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 100, Pages: 14, Words: 11871
                Categories
                Neuroscience
                Review Article

                Neurosciences
                stroke,traumatic brain injury,motor cortex,axonal sprouting,motor learning,recovery
                Neurosciences
                stroke, traumatic brain injury, motor cortex, axonal sprouting, motor learning, recovery

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