Cognitive Context Determines Dorsal Premotor Cortical Activity During Hand Movement in Patients After Stroke

Background and Purpose— Stroke patients often have difficulties in simultaneously performing a motor and cognitive task. Functional imaging studies have shown that movement of an affected hand after stroke is associated with increased activity in multiple cortical areas, particularly in the contralesional hemisphere. We hypothesized patients for whom executing simple movements demands greater selective attention will show greater brain activity during movement. Methods— Eight chronic stroke patients performed a behavioral interference test using a visuo-motor tracking with and without a simultaneous cognitive task. The magnitude of behavioral task decrement under cognitive motor interference (CMI) conditions was calculated for each subject. Functional MRI was used to assess brain activity in the same patients during performance of a visuo-motor tracking task alone; correlations between CMI score and movement-related brain activation were then explored. Results— Movement-related activation in the dorsal precentral gyrus of the contralesional hemisphere correlated strongly and positively with CMI score (r2 at peak voxel=0.92; P<0.05). Similar but weaker relationships were observed in the ventral precentral and middle frontal gyrus. There was no independent relationship between hand motor impairment and CMI. Conclusions— Results suggest that variations in the degree to which a cognitive task interferes with performance of a concurrent motor task explains a substantial proportion of the variations in movement-related brain activity in patients after stroke. The results emphasize the importance of considering cognitive context when interpreting brain activity patterns and provide a rationale for further evaluation of integrated cognitive and movement interventions for rehabilitation in stroke.

[1]  B. Rosen,et al.  A functional MRI study of subjects recovered from hemiparetic stroke. , 1997, Stroke.

[2]  Edward T. Bullmore,et al.  The relationship between motor deficit and hemisphere activation balance after stroke: A 3T fMRI study , 2007, NeuroImage.

[3]  Mark W. Woolrich,et al.  Robust group analysis using outlier inference , 2008, NeuroImage.

[4]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[5]  Stephen M. Smith,et al.  Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. , 2002, Brain : a journal of neurology.

[6]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[7]  K. Ottenbacher,et al.  Unilateral and bilateral upper extremity weight-bearing effect on upper extremity impairment and functional performance after brain injury. , 2009, Occupational therapy international.

[8]  R. E Passingham,et al.  Cerebral dominance for action in the human brain: the selection of actions , 2001, Neuropsychologia.

[9]  P. Haggard,et al.  Concurrent Performance of Cognitive and Motor Tasks in Neurological Rehabilitation , 1998 .

[10]  J. Baron,et al.  Motor Imagery: A Backdoor to the Motor System After Stroke? , 2006, Stroke.

[11]  C. Calautti,et al.  Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery , 2001, Neuroreport.

[12]  Heidi Johansen-Berg,et al.  Attention to movement modulates activity in sensori-motor areas, including primary motor cortex , 2001, Experimental Brain Research.

[13]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[14]  A. Luxen,et al.  Involvement of both prefrontal and inferior parietal cortex in dual-task performance. , 2005, Brain research. Cognitive brain research.

[15]  Richard S. J. Frackowiak,et al.  Neural correlates of motor recovery after stroke: a longitudinal fMRI study. , 2003, Brain : a journal of neurology.

[16]  H. Freund,et al.  Role of the premotor cortex in recovery from middle cerebral artery infarction. , 1998, Archives of neurology.

[17]  Karl J. Friston,et al.  Attention to Action: Specific Modulation of Corticocortical Interactions in Humans , 2001, NeuroImage.

[18]  B. Bussel,et al.  Evidence for Cognitive Processes Involved in the Control of Steady State of Walking in Healthy Subjects and after Cerebral Damage , 2005, Neurorehabilitation and neural repair.

[19]  P. Matthews,et al.  The role of ipsilateral premotor cortex in hand movement after stroke , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Steven C. Cramer,et al.  Somatotopy and movement representation sites following cortical stroke , 2005, Experimental Brain Research.

[21]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[22]  P. Nathan,et al.  Effects of two unilateral cordotomies on the motility of the lower limbs. , 1973, Brain : a journal of neurology.

[23]  J. Krakauer,et al.  Evolution of cortical activation during recovery from corticospinal tract infarction. , 2000, Stroke.

[24]  A. Fugl-Meyer,et al.  The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. , 1975, Scandinavian journal of rehabilitation medicine.

[25]  Guang H. Yue,et al.  Fractal dimension assessment of brain white matter structural complexity post stroke in relation to upper-extremity motor function , 2008, Brain Research.

[26]  Karl J. Friston,et al.  Functional reorganization of the brain in recovery from striatocapsular infarction in man , 1992, Annals of neurology.

[27]  M. Wardle,et al.  Use of a Test of Psychomotor Ability in an Expanded Role , 1981, Perceptual and motor skills.

[28]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[29]  A Ashburn,et al.  Interference between balance, gait and cognitive task performance among people with stroke living in the community , 2006, Disability and rehabilitation.

[30]  H. Dawes,et al.  Fast walking under cognitive-motor interference conditions in chronic stroke , 2009, Brain Research.

[31]  Hannah S. Locke,et al.  Flexible neural mechanisms of cognitive control within human prefrontal cortex , 2009, Proceedings of the National Academy of Sciences.

[32]  T. A. Carpenter,et al.  Motor Imagery After Subcortical Stroke: A Functional Magnetic Resonance Imaging Study , 2009, Stroke.

[33]  Claudia Voelcker-Rehage,et al.  Age-related Differences in Working Memory and Force Control under Dual-task Conditions , 2006, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[34]  A Baddeley,et al.  Working memory and the control of action: evidence from task switching. , 2001, Journal of experimental psychology. General.

[35]  L. Boyd,et al.  Implicit sequence‐specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: An fMRI Study , 2011, Human brain mapping.

[36]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[37]  E. Esbjörnsson,et al.  Recovery after stroke: cognition, ADL function and return to work , 2007, Acta neurologica Scandinavica.

[38]  P. Langhorne,et al.  Motor recovery after stroke: a systematic review , 2009, The Lancet Neurology.

[39]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  John W Krakauer,et al.  Early imaging correlates of subsequent motor recovery after stroke , 2009, Annals of neurology.