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PHYS THER
Vol. 87, No. 1, January 2007, pp. 74-76
DOI: 10.2522/ptj.20060093.ic

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Research Reports

Invited Commentary

Lara A Boyd

LA Boyd, PT, PhD, is Canadian Research Chair, Neurobiology of Motor Learning; Assistant Professor, School of Rehabilitation Sciences, University of British Columbia, T325-2211 Westbrook Mall, Vancouver, British Columbia, Canada V6T 2B5; and Adjunct Faculty, Department of Physical Therapy and Rehabilitation Science, University of Kansas Medical Center, Kansas City, KS

Address all correspondence to Dr Boyd at: laraboyd{at}interchange.ubc.edu


How often have you treated an individual with stroke who, based on your experience and expertise, should have regained function but did not. What is going on? Routinely we generate a list of reasons to explain why sometimes our clients fail to recover function when seemingly they should thrive: poor motivation, concomitant medical problems, lack of family support, inadequate rehabilitation interventions, and so on. What if we had better tools with which to categorize some of these patients? Maybe we do.

In their article, Pohl et al describe a cognitive deficit associated with disrupted executive function after stroke. Switching between tasks is an essential component of normal function and an ability that most of us take absolutely for granted. In their research, Pohl et al used an elegant method demonstrating that task switching is not a motor function but rather a cognitive function. More importantly for physical therapists, the ability to switch between 2 tasks was impaired by the most common distribution of stroke: the middle cerebral artery. This switching deficit, or "switch cost," was particularly acute when the switch was not externally cued (ie, it was under "endogenous" control); yet, endogenous control of switching between tasks is essential for independent function. What makes this work even more relevant to physical therapists is the finding that a switching deficit was noted in individuals in the subacute phase (1–3 months) after stroke; a period that corresponds to the typical time frame for rehabilitation.

Pohl and colleagues’ work raises a larger issue confronting physical therapists across practice domains: impairments in executive function may severely limit physical rehabilitation outcomes. Generally, physical therapists are ill prepared to deal with cognitive problems. Our lack of training to recognize and understand how cognitive impairments affect therapeutic outcomes is further compounded by a paucity of rehabilitation-related research considering these complex problems. Thus, the data presented by Pohl et al illustrate an important point: in some cases, successful rehabilitation requires consideration of the interaction between the motor and cognitive systems. Indeed, neural connectivity confirms the integrated nature of motor and cognitive systems for both motor learning and the production of voluntary movement.

Recent functional magnetic resonance imaging data in young adults who are healthy illustrates the interaction between cognitive and motor regions of the brain during voluntary movements in response to external (exogenous) or internal (endogenous) cues.1 Externally triggered, or exogenous, movements require online processing of sensory cues and invoke activity in a parietal-prefrontal network that both attends to and transforms sensory (in this case, visuospatial) information into a plan for action. In contrast, internally triggered, or endogenous, motor responses benefit from advance planning of movement. In the case of endogenous movements, a frontal-basal ganglia-supplementary and cingulate motor area circuit is activated. The key player for endogenous movements appears to be the basal ganglia, which function to guide learning and performance by determining how much and when motor or cognitive effort are required for successful task completion.1 Reciprocal connections with the prefrontal, frontal, cingulate, and parietal cortices ideally situate the basal ganglia to exert a strong influence over both cognitive and motor function.25 Indeed, the richness of the neuroanatomic connectivity between the basal ganglia and the cortex has led to speculation that the striatum may participate in the coordination of cognitive and motor information necessary for the production of voluntary movement.69

One limitation of Pohl et al and colleagues’ work is the lack of detail concerning stroke lesion location. In this case, knowledge of lesion location would be informative for 2 reasons. First, it would expand our understanding of which brain regions are necessary for successful task switching. Second, and perhaps more important, knowing which brain regions are invoked during task switching could inform clinical practice. In general, relating stroke location with anticipated behavioral deficits enables the implementation of individualized and precisely formed therapeutic interventions. For example, focal damage to the parietal lobe might disrupt the transformation of sensory (ie, visuospatial) information into the correct plan for movement during task switching. In this case, switching between tasks during rehabilitation might be stimulated by other sensory cues (eg, auditory). Alternately, visuospatial information could be emphasized during physical therapy in an effort to stimulate neuroplastic change in the parietal lobe and associated regions. In either scenario, an understanding of both lesion location and the underlying brain-behavior relationship enables the genesis of informed rehabilitation interventions, specifically designed to address the unique deficits of each client.

Two details of the work by Pohl et al distinguish it as particularly enlightening for physical therapists. Once again, prominent deficits have been noted in individuals with stroke even when they use their less-involved, ipsilesional upper extremity for task completion. The robustness of the finding of ipsilesional deficits are striking and range from those relating to motor control,1014 to motor learning,8,1518 and now executive function. Taken together, these data indicate that, although motor control of the contralateral hemibody is most obviously affected by stroke, the effect of even unilateral brain damage is widespread and deleterious for both motor and cognitive function.

Secondly, Pohl et al found improvements in response time for task switching for individuals with stroke across the 2 testing time points (1 month to 3 months after stroke). It is possible that reductions in response time across the testing sessions related to physiologic recovery. I think this explanation is unlikely because the healthy control group also improved. More plausible is the possibility that both groups learned something about the task during the first session, which allowed them to improve their performance during the second test. Although not explicitly tested in this study, the incidental demonstration of learning suggests that patients may benefit from practicing skills that specifically require task switching.

Although not the focus of Pohl and colleagues’ article, their data raise a host of questions concerning why individuals with stroke demonstrated impaired task switching. For instance, was impaired ability to pay attention the cause of higher switch costs after stroke? Similarly (and not mutually exclusive), were deficits in working memory (the short-term maintenance of information necessary to guide upcoming action19) after stroke to blame for poorer accuracy? Last, the authors suggest that impulsivity after stroke might explain their finding of preserved response time but sacrificed accuracy during task switching. However, they offer no independent measure of impulsivity or any of the other executive functions mentioned above. Future work will have to endeavor to address each of the possibilities outlined here as well as consider the effect of impairments in other domains of executive functions on motor recovery after stroke.

It is becoming increasingly important for both physical therapists and research scientists to acknowledge that a wide variety of cognitive factors may critically affect the rehabilitation of motor function, regardless of diagnosis. As knowledge is gained regarding the intricate interconnections between neural regions, it is apparent that damage to both motor and nonmotor brain regions can and does have widespread implications for the functional recovery of voluntary movement. Pohl et al demonstrate the effect of impairments in one domain of executive function: task switching. They also tacitly point out a critical need for more research that considers how stroke and other diagnoses disrupt the elegant relationship between cognitive and motor systems. As our understanding of these factors expands, we will be confronted with the need to design novel interventions that account for disruptions in the cognitive-motor interface and incorporate knowledge of lesion location when it is available.


    References
 

  1. Elsinger CL, Harrington DL, Rao SM. From preparation to online control: reappraisal of neural circuitry mediating internally generated and externally guided actions. Neuroimage. 2006;31:1177–1187.[CrossRef][ISI][Medline]
  2. Cavada C, Goldman-Rakic PS. Posterior parietal cortex in rhesus monkey, II: evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol. 1989;287:422–445.[CrossRef][ISI][Medline]
  3. Cavada C, Goldman-Rakic PS. Topographic segregation of corticostriatal projections from posterior parietal subdivisions in the macaque monkey. Neuroscience. 1991;42:683–696.[CrossRef][ISI][Medline]
  4. Middleton FA, Strick PL, Obeso JA, et al. New concepts about the organization of basal ganglia outputs. In: Advances in Neurology: Basal Ganglia and New Surgical Treatment of Parkinson’s Disease. New York, NY: Lippincott-Raven; 1997:57–68.
  5. Alexander GE, DeLong MR, Strick PL, Cowan WM. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986;9:357–381.[CrossRef][ISI][Medline]
  6. Poldrack RA, Clark J, Pare-Blagoev EJ, et al. Interactive memory systems in the human brain. Nature. 2001;414(6863):546–550.
  7. Harrington DL, Haaland KY, Rosenbaum DA, Collyer CE. Sequencing and timing operations of the basal ganglia. In: Timing of Behavior: Neural, Psychological and Computational Perspectives. Cambridge, Mass: MIT Press; 1998:35–61.
  8. Boyd LA, Winstein CJ. Providing explicit information disrupts implicit motor learning after basal ganglia stroke. Learn Mem. 2004;11:388–396.[Abstract/Free Full Text]
  9. Jennings PJ. Evidence of incomplete motor programming in Parkinson’s disease. J Mot Behav. 1995;27:310–324.[ISI][Medline]
  10. Pohl PS, Luchies CW, Stoker-Yates J, Duncan PW. Upper extremity control in adults post stroke with mild residual impairment. Neurorehabilitation and Neural Repair. 2000;14:33–41.
  11. Pohl PS, Winstein CJ. Practice effects on the less-affected upper extremity after stroke. Arch Phys Med Rehabil. 1999;80:668–675.[CrossRef][ISI][Medline]
  12. Pohl PS, Winstein CJ, OnlaOr S. Sensory-motor control in the ipsilesional upper extremity after stroke. NeuroRehabilitation. 1997;9:245–249.[CrossRef][ISI]
  13. Velicki MR, Winstein CJ, Pohl PS. Impaired direction and extent specification of aimed arm movements in humans with stroke-related brain damage. Exp Brain Res. 2000;130:362–374.[CrossRef][ISI][Medline]
  14. Winstein CJ, Pohl PS. Effects of unilateral brain damage on the control of goal-directed hand movements. Exp Brain Res. 1995;105:163–174.[ISI][Medline]
  15. Boyd LA, Winstein CJ. Explicit information interferes with implicit motor learning of both continuous and discrete movement tasks after stroke. Journal of Neurologic Physical Therapy. 2006;30(2):46–57; discussion 58–49.
  16. Boyd LA, Winstein CJ. Implicit motor-sequence learning in humans following unilateral stroke: the impact of practice and explicit knowledge. Neurosci Lett. 2001;298:65–69.[CrossRef][ISI][Medline]
  17. Boyd LA, Winstein CJ. Impact of explicit information on implicit motor-sequence learning following middle cerebral artery stroke. Phys Ther. 2003;83:976–989.[Abstract/Free Full Text]
  18. Boyd LA, Winstein CJ. Cerebellar stroke impairs temporal but not spatial accuracy during implicit motor learning. Neurorehabilitation and Neural Repair. 2004;18:134–143.
  19. Lezak M, Howieson DB, Loring DW. Neuropsychological Assessment. New York, NY: Oxford University Press; 2004




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