Does the cerebellum shape the spatiotemporal organization of muscle patterns? Insights from subjects with cerebellar ataxias

• Published in: Journal of neurophysiology 2020-05, Vol.123 (5), p.1691-1710
• Main Authors: Berger, Denise J, Masciullo, Marcella, Molinari, Marco, Lacquaniti, Francesco, d'Avella, Andrea
• Format: Article
• Language: English
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00657.2018

The role of the cerebellum in motor control has been investigated extensively, but its contribution to the muscle pattern organization underlying goal-directed movements is still not fully understood. Muscle synergies may be used to characterize multimuscle pattern organization irrespective of time (spatial synergies), in time irrespective of the muscles (temporal synergies), and both across muscles and in time (spatiotemporal synergies). The decomposition of muscle patterns as combinations of different types of muscle synergies offers the possibility to identify specific changes due to neurological lesions. In this study, we recorded electromyographic activity from 13 shoulder and arm muscles in subjects with cerebellar ataxias (CA) and in age-matched healthy subjects (HS) while they performed reaching movements in multiple directions. We assessed whether cerebellar damage affects the organization of muscle patterns by extracting different types of muscle synergies from the muscle patterns of each HS and using these synergies to reconstruct the muscle patterns of all other participants. We found that CA muscle patterns could be accurately captured only by spatial muscle synergies of HS. In contrast, there were significant differences in the reconstruction values for both spatiotemporal and temporal synergies, with an interaction between the two synergy types indicating a larger difference for spatiotemporal synergies. Moreover, the reconstruction quality using spatiotemporal synergies correlated with the severity of impairment. These results indicate that cerebellar damage affects the temporal and spatiotemporal organization, but not the spatial organization, of the muscle patterns, suggesting that the cerebellum plays a key role in shaping their spatiotemporal organization. In recent studies, the decomposition of muscle activity patterns has revealed a modular organization of the motor commands. We show, for the first time, that muscle patterns of subjects with cerebellar damage share with healthy controls spatial, but not temporal and spatiotemporal, modules. Moreover, changes in spatiotemporal organization characterize the severity of the subject's impairment. These results suggest that the cerebellum has a specific role in shaping the spatiotemporal organization of the muscle patterns.