Recruitment of distinct basal ganglia territories at different stages of motor processing: from planning to execution

Purpose: The basal ganglia-thalamo-cortical circuits are viewed as segregated parallel feed back loops crucially involved in motor control, cognition, and emotional processing. So far, there is only limited data on the differential roles of the basal ganglia when proceeding from movement planning to movement execution. Recent fMRI studies have demonstrated rostro-caudal shifts of activity within the basal ganglia during planning and execution of simple, automated finger movements. Using event related fMRI, we aimed to extend these data by analyzing the generation and execution of novel, cognitively demanding sequential movements, which is a critical cognitive requirement for non-routine motor behavior. We hypothesized a shift from bilateral anterior basal ganglia as part of the „associative loop“ during planning to more posterior regions as part of the „sensorimotor loop“ during execution.

Materials and Methods: 14 right-handed, healthy male volunteers were included in the study. Within the scanner, they newly generated a four digit finger sequence for each of the 30 trials following a visual instruction. The finger sequence had to be determined by themselves, using each of fingers II, III, IV and V once. Following a visual cue, which occurred at random 0.6s to 7.6s after the instruction to generate the sequence, they executed this sequence. FMRI was performed on a Philips 3.0T Achieva MRI scanner using a whole brain GE-Single Shot EPI sequence (TE/TR/Flip=35ms/2600ms/90°, resolution: 3.6×3.6×3.6mm³). Data was analysed with SPM5 including standard preprocessing, 8mm smoothing, with planning and movement phases modelled by separate regressors.

Results: Planning compared to baseline was associated with widespread activation in the well established motor control network, including mesial/lateral premotor cortices, motor cingulate cortex, superior parietal cortex, basal ganglia, insula, thalamus, and midbrain nuclei, and was shifted to motor executive regions during movement execution. During planning, the focus of basal ganglia activations was located bilaterally within anterior putamen and caudate nucleus, wheras activation maxima during movement execution were located within more dorso-posterior parts of the striatum.

Conclusion: Our data show the involvement of the anterior striatum in cognitive motor planning operations, compatible with a specific involvement of the „associative“ cortico-basal ganglia-thalamo-cortical loop. During movement execution, activity is shifted to more dorso-posterior basal ganglia territories, corresponding to parts of the „sensori-motor“ loop. These findings illustrate the propagation of activity from rostral to dorsal basal ganglia sites during different stages of motor processing..