Dynamics of Motor Network Overactivation After Striatocapsular Stroke: A Longitudinal PET Study Using a Fixed-Performance Paradigm

Abstract

Background and Purpose-Although excessive brain activation during affected hand motion after stroke is well documented, its time course has been rarely studied, and when studied, this has either been with passive movement or with active but cognitively complex task and uncontrolled performance over time, complicating interpretation. Methods-According to a prospective and longitudinal design, we studied 5 right-handed patients with right-sided hemiparesis due to first-ever left striatocapsular infarction. Three-dimensional PET H 2 O 15 studies were performed twice (Ϸ7 and Ϸ31 weeks after stroke [PET1 and PET2, respectively]) during right thumb-to-index tapping executed at the same rate in both studies (1.26 Hz, auditory cued). With SPM96 software, significant group and individual overactivations (PϽ0.05, corrected for multiple comparisons) were computed by comparison with a group of 7 healthy age-matched right-handed control subjects performing the same task. Results-Motor recovery was significant from PET1 to PET2. Both the group and individual analyses revealed striking overactivations at PET1, affecting notably the cortical hand area and the whole motor network bilaterally. These overactivations were less prominent at PET2 over both hemispheres, not only in terms of Z score but also in terms of spatial extent (almost reaching statistical significance in the affected hemisphere for the latter, Pϭ0.09). However, new overactivations were found at PET2 in the left prefrontal areas, the putamen, and the premotor cortex. Conclusions-This study is the first to document that to perform the same simple movement of the paretic fingers, the brain with subcortical infarction shows less overactivations at the late than at the early timepoint, especially on the affected side, suggesting reduced recruitment of affected-hemisphere motor networks. However, unaffected-hemisphere prefrontal, premotor, and putaminal overactivations, observed at PET2 only, may suggest late-appearing compensatory reorganization. (Stroke. 2001;32:2534-2542.)

Imaging correlates of motor recovery from cerebral infarction and their physiological significance in well-recovered patients

“…This finding agrees with several previous studies, which reported that with functional recovery, focusing of the initial over-activation seen in stroke patients mainly occurs to the ipsilesional M1 (Nelles et al, 1999;Marshall et al, 2000;Calautti et al, 2001;Cramer et al, 2002;Feydy et al, 2002;Ward et al, 2003, Binkofski & Seitz, 2004, Carey et al, 2005. Greater and widespread neural activation has been reported in previous studies of stroke recovery, both cross-sectional and longitudinal (Chollet et al, 1991;Weiller et al, 1992;Cramer et al, 1997;Cramer 1999;Nelles et al, 1999;Marshall et al, 2000;Calautti et al, 2001;Ward et al, 2003, Carey et al, 2005. It seems that the system is somehow "upregulated" for execution of any movement and it is possible that such an increase in neural activity is essential to send sufficient signal to the motor neurons downstream.…”

“…Thus, if activation in the contralesional M1 persists during the initial post-stroke period (Marshall et al, 2000;Calautti et al, 2001;Johansen-Berg et al, 2002a;Carey et al, 2002) and even after good recovery, and this area does not relay direct corticomotoneuronal connections, it is reasonable to conclude that contralesional M1 activation arises out of altered intracortical and transcallosal interactions. An alternative explanation is that contralesional M1 activation arises from top-down activation from higher order areas, and is an epiphenomenon not contributing to recovery.…”

“…Important results from the above studies can be summarized as a) Focusing of activation -the initial widespread activation of the primary motor (M1) and other areas such as the Supplementary Motor Area (SMA), Cerebellum, Premotor, Parietal and Insula, become less widespread and focused (Chollet et al, 1991;Weiller et al, 1992;Nelles et al, 1999;Ward et al, 2003) b) Change in laterality -an initial increase in activity in the contralesional primary sensorimotor cortex changes to more ipsilesional activity (Marshall et al, 2000;Calautti et al, 2001;Johansenberg et al, 2002a) and c) Activation in the peri-infarct region (Cramer et al, 1997;Luft et al, 2004a). The temporal evolution of neural activation and reorganization revealed by these studies suggest that well-recovered patients, despite being able to perform motor tasks and being functionally independent, may have a different representation of hand movements after recovery than age-matched control subjects.…”

Activation of Brain Sensorimotor Network by Somatosensory Input in Patients with Hemiparetic Stroke: A Functional MRI Study

“…The contralesional shift of activation may return to ipsilesional S1M1 activation with functional gains (Feydy et al, 2002;Takeda et al, 2007), but worse outcome may correlate with a shift in the balance of activation toward the contralesional S1M1 (Calautti et al, 2001;Feydy et al, 2002;Zemke et al, 2003). Thus, the patterns of cerebral activation evoked by active hand movement show impaired organization and reorganization of brain sensorimotor network, and best recovery may depend on how much original motor system is reusable.…”

“…Initial cross-sectional studies at chronic stages of stroke have demonstrated that the pattern of brain activation is different between paretic and normal hand movements, and suggested that long-term recovery is facilitated by compensation, recruitment and reorganization of cortical motor function in both damaged and non-damaged hemispheres (Chollet et al, 1991;Weiller et al, 1992;Cramer et al, 1997;Cao et al, 1998;Ward et al, 2003a). Subsequent longitudinal studies from subacute to chronic stages (before and after rehabilitation) have revealed a dynamic, bihemispheric reorganization of motor network, and emphasized the necessity of successive studies (Marshall et al, 2000;Calautti et al, 2001;Feydy et al, 2002;Ward et al, 2003b).…”