Specialized Neural Systems Underlying Representations of Sequential Movements

Abstract

Abstract The ease by which movements are combined into skilled actions depends on many factors, including the complexity of movement sequences. Complexity can be defined by the surface structure of a sequence, including motoric properties such as the types of effectors, and by the abstract or sequence-specific structure, which is apparent in the relations amongst movements, such as repetitions. It is not known whether different neural systems support the cognitive and the sensorimotor processes underlying different structural properties of sequential actions. We investigated this question using whole-brain functional magnetic resonance imaging (fMRI) in healthy adults as they performed sequences of five key presses involving up to three fingers. The structure of sequences was defined by two factors that independently lengthen the time to plan sequences before movement: the number of different fingers (1-3; surface structure) and the number of finger transitions (0-4; sequence-specific structure). The results showed that systems involved in visual processing (extrastriate cortex) and the preparation of sensory aspects of movement (rostral inferior parietal and ventral premotor cortex (PMv)) correlated with both properties of sequence structure. The number of different fingers positively correlated with activation intensity in the cerebellum and superior parietal cortex (anterior), systems associated with sensorimotor, and kinematic representations of movement, respectively. The number of finger transitions correlated with activation in systems previously associated with sequence-specific processing, including the inferior parietal and the dorsal premotor cortex (PMd), and in interconnecting superior temporal-middle frontal gyrus networks. Different patterns of activation in the left and right inferior parietal cortex were associated with different sequences, consistent with the speculation that sequences are encoded using different mnemonics, depending on the sequence-specific structure. In contrast, PMd activation correlated positively with increases in the number of transitions, consistent with the role of this area in the retrieval or preparation of abstract action plans. These findings suggest that the surface and the sequence-specific structure of sequential movements can be distinguished by distinct distributed systems that support their underlying mental operations.