The structural and functional mechanisms of motor recovery: complementary use of diffusion tensor and functional magnetic resonance imaging in a traumatic injury of the internal capsule

OBJECTIVES Recovery from focal motor pathway lesions may be associated with a functional reorganisation of cortical motor areas. Previous studies of the relation between structural brain damage and the functional consequences have employed MRI and CT, which provide limited structural information. The recent development of diffusion tensor imaging (DTI) now provides quantitative measures of fibre tract integrity and orientation. The objective was to use DTI and functional MRI (fMRI) to determine the mechanisms underlying the excellent recovery found after a penetrating injury to the right capsular region. METHODS DTI and fMRI were performed on the patient described; DTI was performed on five normal controls. RESULTS The injury resulted in a left hemiplegia which resolved fully over several weeks. When studied 18 months later there was no pyramidal weakness, a mild hemidystonia, and sensory disturbance. fMRI activation maps showed contralateral primary and supplementary motor cortex activation during tapping of each hand; smaller ipsilateral primary motor areas were activated by the recovered hand only. DTI disclosed preserved structural integrity and orientation in the posterior capsular limb by contrast with the disrupted structure in the anterior limb on the injured side. CONCLUSIONS The findings suggest that the main recovery mechanism was a preservation of the integrity and orientation of pyramidal tract fibres. The fMRI studies do not suggest substantial reorganisation of the motor cortex, although ipsilateral pathways may have contributed to the recovery. The initial deficit was probably due to reversible local factors including oedema and mass effect; permanent damage to fibre tracts in the anterior capsular limb may account for the persistent sensory deficit. This study shows for the first time the potential value of combining fMRI and DTI together to investigate mechanisms of recovery and persistent deficit in an individual patient.

[1]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[2]  D. Feinberg,et al.  Human brain motion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. , 1987, Radiology.

[3]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[4]  Richard S. J. Frackowiak,et al.  The functional anatomy of motor recovery after stroke in humans: A study with positron emission tomography , 1991, Annals of neurology.

[5]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[6]  W. Fries,et al.  Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. , 1993, Brain : a journal of neurology.

[7]  J. Binder,et al.  Functional magnetic resonance imaging of complex human movements , 1993, Neurology.

[8]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

[9]  Karl J. Friston,et al.  Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction , 1993, Annals of neurology.

[10]  C. Marsden,et al.  The behavioural and motor consequences of focal lesions of the basal ganglia in man. , 1994, Brain : a journal of neurology.

[11]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[12]  C. Beaulieu,et al.  Determinants of anisotropic water diffusion in nerves , 1994, Magnetic resonance in medicine.

[13]  J. A. Frost,et al.  Somatotopic mapping of the human primary motor cortex with functional magnetic resonance imaging , 1995, Neurology.

[14]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[15]  R. J. Seitz,et al.  Thalamic metabolism and corticospinal tract integrity determine motor recovery in stroke , 1996, Annals of neurology.

[16]  E. Bullmore,et al.  Statistical methods of estimation and inference for functional MR image analysis , 1996, Magnetic resonance in medicine.

[17]  R. Nudo,et al.  Neural Substrates for the Effects of Rehabilitative Training on Motor Recovery After Ischemic Infarct , 1996, Science.

[18]  P. Wall,et al.  A clinical and neurophysiological study of a patient with an extensive transection of the spinal cord sparing only a part of one anterolateral quadrant. , 1996, Brain : a journal of neurology.

[19]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[20]  J. Cummings,et al.  The insistent call from functional MRI , 1997, Neurology.

[21]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.