Network activation during bimanual movements in humans

Abstract

The coordination of movement between the upper limbs is a function highly distributed across the animal kingdom. How the central nervous system generates such bilateral, synchronous movements, and how this differs from the generation of unilateral movements, remains uncertain. Electrophysiologic and functional imaging studies support that the activity of many brain regions during bimanual and unimanual movement are quite similar. Thus, the same brain regions (and indeed the same neurons) respond similarly during unimanual and bimanual movements as measured by electrophysiological responses. How then are different motor behaviors generated?To address this question, we studied unimanual and bimanual movements using fMRI and constructed networks of activation using Structural Equation Modeling (SEM). Our results suggest that (1) the dominant hemisphere appears to initiate activity responsible for bimanual movement; (2) activation during bimanual movement does not reflect the sum of right and left unimanual activation; (3) production of unimanual movement involves a network that is distinct from, and not a mirror of, the network for contralateral unimanual movement; and (4) using SEM, it is possible to obtain robust group networks representative of a population and to identify individual networks which can be used to detect subtle differences both between subjects as well as within a single subject over time. In summary, these results highlight a differential role for the dominant and non-dominant hemispheres during bimanual movements, further elaborating the concept of handedness and dominance. This knowledge increases our understanding of cortical motor physiology in health and after neurological damage.

Congenital mirror movements: a clue to understanding bimanual motor control

“…Mirror movements could be due to abnormal spread of the motor plan to both M1 regions, either from a single motor planning area or from independent planning centers located in each hemisphere. More specifically, since the dominant hemisphere appears to initiate activity responsible for synchronous bimanual movement [86], it is possible that the dominant hemisphere is responsible for MM during intended independent bimanual tasks because of an interhemispheric miscommunication due to abnormal transcallosal connections (Fig. 1).…”

“…Dissociation of the motor output arising from each hemisphere also requires appropriate inhibition of the motor cortex ipsilateral to the voluntary movement, through inhibitory transcallosal projections. During complex bimanual movements, the dominant hemisphere should play a modulatory role in finding a good balance with the other hemisphere to ensure the coordination of action plans and the dissociation of motor outputs [86]. Dysfunction or morphological alterations of the multiple neural circuits underlying bimanual control may result in involuntary MM (Fig.…”

Coordination of Uncoupled Bimanual Movements by Strictly Timed Interhemispheric Connectivity

“…This view has been challenged by evidence in monkeys that showed a subset of neurons within the primary motor cortex (M1) specifically engaged in the control of bimanual movements (Donchin et al, 1998;Gribova et al, 2002). Several neuroimaging studies in humans have demonstrated that anti-phase and in-phase movements share a large core motor network, but additional activations in bihemispheric motor networks have also been detected during anti-phase activities (Sadato et al, 1997;Ehrsson et al, 2002;Ullen et al, 2003;Rocca et al, 2007;Walsh et al, 2008;Meister et al, 2010). In previous studies using functional magnetic resonance imaging (fMRI), brain activity related to transitions from anti-phase to in-phase has been reported to occur in right-lateralized prefrontal, SMA, dorsal premotor (PMd), parietal regions and cerebellum (MeyerLindenberg et al, 2002;Aramaki et al, 2006b).…”

Spatiotemporal re-organization of large-scale neural assemblies underlies bimanual coordination

“…For example, bimanual coupling necessary for the maintenance of stable relative phase patterns appears to require simultaneous activity of several cortical areas, some of which may also be engaged in purely unimanual tasks (Kazennikov et al, 1999;Debaere et al, 2001;Cardoso de Oliveira, 2002;Nair et al, 2003;Koeneke et al, 2004;Aramaki et al, 2006a,b;Daffertshofer et al, 2005;Serrien, 2008;Walsh et al, 2008). Primary motor cortices (M1), supplementary motor areas (SMA), dorsal premotor cortex, cingulate motor area (CMA), primary somatosensory cortices (S1), superior parietal lobule (PAR), posterior parietal cortex (PP) have all been shown to play a contributory role.…”