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Capitalizing on Neuroplasticity
Brain and Cognition 42, 106–109 (2000) doi:10.1006/brcg.1999.1175, available online at http://www.idealibrary.com on
Capitalizing on Neuroplasticity Catherine A. Mateer and Kimberly A. Kerns University of Victoria, British Columbia, Canada
The past two decades have witnessed an explosion of information regarding the brain and behavior interface. We now have detailed profiles of the cognitive impairments associated with many neurological conditions, ever more elegant techniques for imaging brain activity during cognitive processing, and an arsenal of neuropsychological tests. To date, however, neuropsychology has had little new to offer in the way of improving or changing impaired brain function due to injury or developmental abnormality. This is perhaps all the more striking given that many of the pioneers in the field, including Kurt Goldstein, Alexander Luria, Henry Head, and Ritchie Russell, all developed their theories about brain organization in the context of rehabilitation. This is not to say that people with brain injuries are not treated. Thousands of professionals treat individuals with brain damage, though for the most part with little guidance or theoretical understanding about how rehabilitation might work. In the upcoming millennium, research should focus on an increased understanding of brain plasticity and how to capitalize on the brain’s striking capacity for reorganization and recovery of function, and this should become a major goal in the field. It is well acknowledged that normal associative learning and experience evoke changes in the brain and it is believed that such mechanisms underlie recovery of function following acquired brain injury. Substantial literature supports the view that experience-dependent changes occur in the brain throughout the lifespan through modification of synaptic activity, changes in synaptic firing, dendritic arborization, and axonal sprouting. Recent evidence is converging to support the principle that ‘‘cells that fire together, wire together.’’ Connections between cells stimulated to fire in synchrony are strengthened, whereas nonsynchronous firing inhibits connectivity. There is abundant evidence for behaviorally induced and experienceAddress correspondence and reprint requests to Catherine A. Mateer or Kimberly A. Kerns, Department of Psychology, University of Victoria, Victoria, BC, Canada, V8W 3P5. E-mail: [email protected] or [email protected]. 106 0278-2626/00 $35.00 Copyright 2000 by Academic Press All rights of reproduction in any form reserved.
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dependent plastic reorganization of lesioned brain systems. Recovery has been documented for motor disorders, language disorders, perceptual deficits, unilateral neglect, attention deficits, tactile discrimination, and other functions, probably through a combination of compensatory processes and plastic reorganization. These improvements are viewed as natural extensions of normal learning and experience-dependent processes; as such, variations in experience will shape synaptic interconnections and influence recovery. Recent studies have highlighted the importance of external patterned input on neural plasticity and functional recovery. For example, rats given striatal transplants only benefitted behaviorally when given the opportunity for perceptual motor learning. Similarly, squirrel monkeys with motor cortex lesions showed less loss of hand movement representation with intensive behavioral training of skilled hand use. Much of the literature on adult cortical plasticity is based on reorganization of primary sensory and motor circuitry. Functional improvements have been demonstrated with repeated stimulation of gait patterns, ‘‘blind’’ visual fields and deafferented limbs. However, there is also ample evidence to indicate similar potential for representations underlying attention, memory, language, and executive functions. Improvements in Wernicke’s aphasia, for example, are associated with cortical reorganization as revealed by functional imaging (Weiller et al., 1995). Merzenich et al. (1996) and Tallal et al. (1996) have reported behavioral evidence of experience-dependent training-induced improvement in certain auditory processing abilities critical to phonemic discrimination and other linguistic capacities. Improvements in attentional processing at both the behavioral and electrophysiological level have been demonstrated following structured attention training programs (Sohlberg et al., 1998). All of these changes have been proposed to result from changes in synaptic connectivity in the relevant areas of the cortex. In spite of the success to date in the area of rehabilitation, much is still not known and we are only now beginning to understand the full importance of different approaches to rehabilitative treatment. Interestingly, the role of attention has recently been highlighted as playing a critical role in modulating change in other cognitive and perceptual systems. Frontal attention circuits have been shown to ‘‘gate’’ the processing of information, and neural plasticity appears to respond to this phenomena. Subjects showed more activation to fingertip vibration on functional imaging when they were attending to the sensation than when they were not (Meyer et al., 1991). Such results suggest that reorganization of neural circuitry is facilitated by active attention to the relevant task or stimulus. Perhaps this is why unstructured and relatively unattended activation of systems as one goes about daily activities is insufficient to result in maximum recovery of function. Recent research is also identifying that residual functioning of a damaged system can be suppressed, masked, or dominated by the functioning of other systems which remain intact. This suggests that compensatory processes not
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only can deter the utilization of partially lesioned circuits, but they may also actively inhibit such utilization via inhibitory circuits. As an example of this phenomenon, visually decorticate rats ignored visual cues, responding only to nonvisual cues to avoid shock. However, they began to respond to visual cues if the nonvisual cues were made irrelevant to shock avoidance. Restitution of function in damaged circuits may actually be hindered by compensatory adjustments which may support adaptive function in the short term, but which result in long-term inhibition of the activity of damaged circuits. Even in a normal brain, short-term loss of sensory input results in shrinkage of the related motor cortex. Such phenomena are leading to dramatic changes in the treatment of individuals with paretic limbs, involving restriction of use of the spare limb and intense stimulation and use of the involved limb. An appreciation of the impact of inhibitory factors has also led to exciting new approaches to the treatment of unilateral neglect that focus on diminishing the dominant hemisphere’s activity and enhancing the activity of circuits in the damaged hemisphere. As an example, simply clenching the left hand continuously can reduce the amount of spatial neglect or bias demonstrated as a patient with left spatial neglect walks through a doorway, presumably by boosting nondominant hemisphere activation (Robertson, Hogg, & McMillan, 1998). The field has only begun to identify mechanisms by which experiencedependent plasticity may be helped or hindered, but this information is crucial to guiding recovery of function and developing effective rehabilitation methods. It will be important to explore how age, gender, cognitive capacity, hormonal status, and prior experience of the individual influence recovery patterns. Plastic changes have been shown to be operative long past the period in which maximum spontaneous recovery takes place (e.g., recovery of function in a paretic limb, Balliet, Levy, & Blood, 1986), but we do not know when to take best advantage of this potential. Creative and committed exploration of ways in which we can exploit inherent neural mechanisms to facilitate, shape, and guide recovery must be a priority for the next millennium. The fruits of such exploration will not only improve our clients’ potential for recovery of function, but will enliven, challenge, and enhance the field of neuropsychology. REFERENCES Balliet, R., Levy, B., & Blood, K. M. T. 1986. Upper extremity sensory feedback therapy in chronic cerebrovascular accident patients with expressive aphasia and auditory comprehension. Archives of Physical Medicine and Rehabilitation, 67, 304–310. Merzenich, M., Jenkins, W. M., Johnston, P., Schreiner, C., Miller, S. L., & Tallal, P. 1996. Temporal processing deficits of language-learning impaired children ameliorated by training. Science, 271, 77–81. Meyer, E., Ferguson, S. S. G., Zatorre, R. J., Alivisatos, B., Marrett, S., Evans, A. C., & Hakim, A. M. 1991, Attention modulates somatosensory cerebral blood-flow response
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to vibrotactile stimulation as measured by positron emission tomography. Annals of Neurology, 29, 440–443. Robertson, I. H., Hogg, K., & McMillan, T. M. 1998. Rehabilitation of unilateral neglect: Reducing inhibitory competition by contralesional limb activation. Neuropsychological Rehabilitation, 8, 19–29. Sohlberg, M. M., McLaughlin, K. A., Pavese, A., Heidrich, A., & Posner, M. I. 1998. Evaluation of attention process training in persons with acquired brain injury. University of Oregon, Institute of Cognitive and Decision Sciences, Technical Report 98-08. Tallal, P., Miller, S. L., Bedi, G., Byma, G., Wang, X. Q., Nagarajan, S. S., Schreiner, C., Jenkins, W. M., & Merzenick, M. M. 1996. Language comprehension in language-learning impaired children improved with acoustically modified speech. Science, 271, 81–84. Weiller, C., Isensee, C., Rijntjes, M., Huber, W., Muller, S., Bier, D., Dutschka, K., Woods, R. P., Noth, J. & Dienere, H. C. 1995. Recovery from Wernicke’s aphasia: A positron emission tomographic study. Annals of Neurology, 37, 723–732.
Capitalizing on Neuroplasticity Catherine A. Mateer and Kimberly A. Kerns University of Victoria, British Columbia, Canada
The past two decades have witnessed an explosion of information regarding the brain and behavior interface. We now have detailed profiles of the cognitive impairments associated with many neurological conditions, ever more elegant techniques for imaging brain activity during cognitive processing, and an arsenal of neuropsychological tests. To date, however, neuropsychology has had little new to offer in the way of improving or changing impaired brain function due to injury or developmental abnormality. This is perhaps all the more striking given that many of the pioneers in the field, including Kurt Goldstein, Alexander Luria, Henry Head, and Ritchie Russell, all developed their theories about brain organization in the context of rehabilitation. This is not to say that people with brain injuries are not treated. Thousands of professionals treat individuals with brain damage, though for the most part with little guidance or theoretical understanding about how rehabilitation might work. In the upcoming millennium, research should focus on an increased understanding of brain plasticity and how to capitalize on the brain’s striking capacity for reorganization and recovery of function, and this should become a major goal in the field. It is well acknowledged that normal associative learning and experience evoke changes in the brain and it is believed that such mechanisms underlie recovery of function following acquired brain injury. Substantial literature supports the view that experience-dependent changes occur in the brain throughout the lifespan through modification of synaptic activity, changes in synaptic firing, dendritic arborization, and axonal sprouting. Recent evidence is converging to support the principle that ‘‘cells that fire together, wire together.’’ Connections between cells stimulated to fire in synchrony are strengthened, whereas nonsynchronous firing inhibits connectivity. There is abundant evidence for behaviorally induced and experienceAddress correspondence and reprint requests to Catherine A. Mateer or Kimberly A. Kerns, Department of Psychology, University of Victoria, Victoria, BC, Canada, V8W 3P5. E-mail: [email protected] or [email protected]. 106 0278-2626/00 $35.00 Copyright 2000 by Academic Press All rights of reproduction in any form reserved.
MILLENNIUM ISSUE
107
dependent plastic reorganization of lesioned brain systems. Recovery has been documented for motor disorders, language disorders, perceptual deficits, unilateral neglect, attention deficits, tactile discrimination, and other functions, probably through a combination of compensatory processes and plastic reorganization. These improvements are viewed as natural extensions of normal learning and experience-dependent processes; as such, variations in experience will shape synaptic interconnections and influence recovery. Recent studies have highlighted the importance of external patterned input on neural plasticity and functional recovery. For example, rats given striatal transplants only benefitted behaviorally when given the opportunity for perceptual motor learning. Similarly, squirrel monkeys with motor cortex lesions showed less loss of hand movement representation with intensive behavioral training of skilled hand use. Much of the literature on adult cortical plasticity is based on reorganization of primary sensory and motor circuitry. Functional improvements have been demonstrated with repeated stimulation of gait patterns, ‘‘blind’’ visual fields and deafferented limbs. However, there is also ample evidence to indicate similar potential for representations underlying attention, memory, language, and executive functions. Improvements in Wernicke’s aphasia, for example, are associated with cortical reorganization as revealed by functional imaging (Weiller et al., 1995). Merzenich et al. (1996) and Tallal et al. (1996) have reported behavioral evidence of experience-dependent training-induced improvement in certain auditory processing abilities critical to phonemic discrimination and other linguistic capacities. Improvements in attentional processing at both the behavioral and electrophysiological level have been demonstrated following structured attention training programs (Sohlberg et al., 1998). All of these changes have been proposed to result from changes in synaptic connectivity in the relevant areas of the cortex. In spite of the success to date in the area of rehabilitation, much is still not known and we are only now beginning to understand the full importance of different approaches to rehabilitative treatment. Interestingly, the role of attention has recently been highlighted as playing a critical role in modulating change in other cognitive and perceptual systems. Frontal attention circuits have been shown to ‘‘gate’’ the processing of information, and neural plasticity appears to respond to this phenomena. Subjects showed more activation to fingertip vibration on functional imaging when they were attending to the sensation than when they were not (Meyer et al., 1991). Such results suggest that reorganization of neural circuitry is facilitated by active attention to the relevant task or stimulus. Perhaps this is why unstructured and relatively unattended activation of systems as one goes about daily activities is insufficient to result in maximum recovery of function. Recent research is also identifying that residual functioning of a damaged system can be suppressed, masked, or dominated by the functioning of other systems which remain intact. This suggests that compensatory processes not
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only can deter the utilization of partially lesioned circuits, but they may also actively inhibit such utilization via inhibitory circuits. As an example of this phenomenon, visually decorticate rats ignored visual cues, responding only to nonvisual cues to avoid shock. However, they began to respond to visual cues if the nonvisual cues were made irrelevant to shock avoidance. Restitution of function in damaged circuits may actually be hindered by compensatory adjustments which may support adaptive function in the short term, but which result in long-term inhibition of the activity of damaged circuits. Even in a normal brain, short-term loss of sensory input results in shrinkage of the related motor cortex. Such phenomena are leading to dramatic changes in the treatment of individuals with paretic limbs, involving restriction of use of the spare limb and intense stimulation and use of the involved limb. An appreciation of the impact of inhibitory factors has also led to exciting new approaches to the treatment of unilateral neglect that focus on diminishing the dominant hemisphere’s activity and enhancing the activity of circuits in the damaged hemisphere. As an example, simply clenching the left hand continuously can reduce the amount of spatial neglect or bias demonstrated as a patient with left spatial neglect walks through a doorway, presumably by boosting nondominant hemisphere activation (Robertson, Hogg, & McMillan, 1998). The field has only begun to identify mechanisms by which experiencedependent plasticity may be helped or hindered, but this information is crucial to guiding recovery of function and developing effective rehabilitation methods. It will be important to explore how age, gender, cognitive capacity, hormonal status, and prior experience of the individual influence recovery patterns. Plastic changes have been shown to be operative long past the period in which maximum spontaneous recovery takes place (e.g., recovery of function in a paretic limb, Balliet, Levy, & Blood, 1986), but we do not know when to take best advantage of this potential. Creative and committed exploration of ways in which we can exploit inherent neural mechanisms to facilitate, shape, and guide recovery must be a priority for the next millennium. The fruits of such exploration will not only improve our clients’ potential for recovery of function, but will enliven, challenge, and enhance the field of neuropsychology. REFERENCES Balliet, R., Levy, B., & Blood, K. M. T. 1986. Upper extremity sensory feedback therapy in chronic cerebrovascular accident patients with expressive aphasia and auditory comprehension. Archives of Physical Medicine and Rehabilitation, 67, 304–310. Merzenich, M., Jenkins, W. M., Johnston, P., Schreiner, C., Miller, S. L., & Tallal, P. 1996. Temporal processing deficits of language-learning impaired children ameliorated by training. Science, 271, 77–81. Meyer, E., Ferguson, S. S. G., Zatorre, R. J., Alivisatos, B., Marrett, S., Evans, A. C., & Hakim, A. M. 1991, Attention modulates somatosensory cerebral blood-flow response
MILLENNIUM ISSUE
109
to vibrotactile stimulation as measured by positron emission tomography. Annals of Neurology, 29, 440–443. Robertson, I. H., Hogg, K., & McMillan, T. M. 1998. Rehabilitation of unilateral neglect: Reducing inhibitory competition by contralesional limb activation. Neuropsychological Rehabilitation, 8, 19–29. Sohlberg, M. M., McLaughlin, K. A., Pavese, A., Heidrich, A., & Posner, M. I. 1998. Evaluation of attention process training in persons with acquired brain injury. University of Oregon, Institute of Cognitive and Decision Sciences, Technical Report 98-08. Tallal, P., Miller, S. L., Bedi, G., Byma, G., Wang, X. Q., Nagarajan, S. S., Schreiner, C., Jenkins, W. M., & Merzenick, M. M. 1996. Language comprehension in language-learning impaired children improved with acoustically modified speech. Science, 271, 81–84. Weiller, C., Isensee, C., Rijntjes, M., Huber, W., Muller, S., Bier, D., Dutschka, K., Woods, R. P., Noth, J. & Dienere, H. C. 1995. Recovery from Wernicke’s aphasia: A positron emission tomographic study. Annals of Neurology, 37, 723–732.