Following perinatal hemispheric injury, the developing brain reorganizes hand motor control interhemispherically, reallocating some lost functional representation and processing capacity to the intact hemisphere.1,2 A curious self-reported observation of mirror movement augmentation3 by a patient of ours led us to measure this reorganization electrophysiologically, and from this, make simple observations about the way the brain remaps itself following hemispheric stroke.
Case report.
A 19-year-old man with epilepsy was implanted with subdural electrocorticographic (ECoG) electrodes that included left frontoparietal cortex in order to identify the focus of seizure initiation. The right-handed patient had left-sided spastic hemiplegic cerebral palsy, following a perinatal hemispheric stroke. In the course of his hospital stay, he described and then demonstrated the mirror movement effect of his condition. He gripped 2 of the physician's fingers with his left hand, and then reported he was squeezing with full strength. He then raised his right hand, and slowly formed a fist and contracted with his right hand. As he contracted with his right hand, the grip strength with his left hand grew immensely. We measured the electrophysiology underlying this phenomenon by comparing broadband ECoG change while he opened and closed his right and left hands independently, and then both hands at the same time (see e-Methods on the Neurology® Web site at www.neurology.org). Simple power measurements in different frequency ranges of the ECoG voltage time series allow us to segregate different underlying cortical physiology,4 comparing the power during rest to that during the different movements. Although the hemispheric stroke was in the perinatal, plastic brain and ongoing seizures may have played a part in later reorganization, the physiology may still inform us about general motifs in reorganization which occur to different degree in the adult, nonepileptic brain.
β-Band (12–30 Hz) oscillations are associated with widespread and synchronized thalamic projections to cortex.5 We observe that the changes in β-band power in precentral hand area (electrode pairs 2 and 3 in the figure) are significant with movement of either hand or both hands together. Unlike patients without motor deficits,6 the changes in power are not statistically different between types of movement. This suggests a common mechanism, and that the reorganization of the physiology underlying β-band changes co-opts an existing thalamocortical mechanism, which is shared between movement types.
Figure. Electrocorticographic imaging.
(A) Electrocorticographic electrode positions with respect to anatomy. The central sulcus is shown in yellow, and the transverse sulcus is shown in green. (B) The power spectral density from the electrode pair labeled “2” in A, during bimanual movement during movement and rest. Broadband (χ-band, 65–200 Hz, orange) and β-band (12–30 Hz, green) ranges are examined. (C) The shift in power between movement and rest in broadband power, during ipsilateral (red), contralateral (blue), and bilateral (purple) hand movement. Error bars indicate SD. Colored asterisks indicate significant shift (e.g., p < 0.05, by resampling against the mean). Gray asterisks with lines indicate significant difference in shift between types of movement. (D) As in C, for β-band power.
Broadband spectral change (χ-band, 65–200 Hz) in the ECoG potential can be used to map motor cortical activity in real time, and is correlated with average neuronal population activity in the cortex immediately beneath each electrode.7 In patients without motor deficits, ipsilateral hand movement is associated with broadband spectral changes, but with a weaker, nonoverlapping, representation than with contralateral hand movements.6 In the precentral hand area of our patient (electrode pairs 2 and 3), however, we found that this change in local activity during movement of both hands simultaneously was of the same order or larger than the combined change associated with movement of each independently. This implies that the aspect of neuronal physiology reflected in broadband spectral change is separate for each hand following postinfarct reorganization.
Discussion.
The dynamic interplay between the physiology underlying the β-band and broadband spectral change is revealed by the behavior-related changes observed. The broadband spectral changes support a separate cortical representation for the ipsilateral hand. However, there was no significant variation of β suppression between behavioral tasks. Therefore, the mechanism underlying beta rhythm change is shared, or borrowed from the normal, contralateral mechanism. As the strength of contraction of the ipsilateral hand is facilitated by movement of the contralateral hand, we propose that this borrowing is incomplete.
Development of normal interhemispheric connection appears important for suppression of mirror movement effects in development. The ability to (re) recruit ipsilateral motor representations seems to utilize preexisting ipsilateral representations, but with incomplete utilization of the normal release of β synchronization. Thus, the mirror movement allows for more complete β suppression release, suggesting the coordination between β suppression and local activity is optimal for the native or preferred cortical activity.
Supplementary Material
ACKNOWLEDGMENT
The authors thank the patient, who suggested this study; the staff at Harborview Hospital, Seattle, WA, for their time and dedication; and Dora Hermes for discussion.
Footnotes
Supplemental data at www.neurology.org
Disclosure: Dr. Miller, Dr. Abel, and Dr. Hebb report no disclosures. Dr. Ojemann serves on the editorial boards of the Journal of Neurosurgery: Pediatrics and Neurosurgery and on the Professional Advisory Board of the Epilepsy Foundation of America; and receives research support from the NIH, the NSF, the Seattle Children's Research Institute, the Charles A. Dana Foundation, and CURE (Citizens United for Research in Epilepsy).
AUTHOR CONTRIBUTIONS
Statistical analysis was conducted by Dr. K.J. Miller.
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