The hippocampus binds movements to their temporal position in a motor sequence

Abstract

A plethora of daily motor tasks consist of sequences of movements or steps that need to be performed in a specific order. Yet, it remains unclear how the brain represents sequential motor actions in a way that preserves their temporal order. Here, we used multivoxel pattern similarity analysis of functional Magnetic Resonance Imaging (fMRI) data acquired during motor sequence practice to investigate whether the hippocampus, a brain region known to support temporal order in the non-motor memory domain, represents information about the temporal order of sequential motor actions. We also examined such representation in other regions of the motor network (i.e., the premotor cortex (PMC), supplementary motor area (SMA), anterior superior parietal lobule (aSPL) and striatum) known for their critical role in motor sequence learning. Our results show that hippocampal activation patterns carried information about movements in their learned temporal position in the sequence (i.e., movement-position binding), but not about movements or positions in random movement patterns. In contrast, other ROIs showed evidence of binding in the sequence as well as movement (M1, SMA, PMC, putamen and aSPL) and position (aSPL and PMC) coding in random movement patterns. Importantly, movement coding contributed to sequence learning patterns in M1, SMA and PMC but not in the putamen and aSPL, suggesting a specific involvement of these regions in movement-position binding. Altogether, our findings provide novel insight into the role of the hippocampus in the motor memory domain and point to its capacity to bind movements to their temporal position in a motor sequence. Our results also deepen our understanding of how striatal and cortical regions contribute to motor sequence learning via movement coding or movement-position binding. Significance StatementConsistent evidence collected over the last two decades indicates that the hippocampus - a brain structure traditionally associated to declarative memory - is critically involved in motor memory. Yet, the functional role and representational contribution of the hippocampus during motor learning remains to be elucidated. Using a multivariate functional MRI approach, we show here that the hippocampus binds movements to their temporal position in a learned sequence of actions. These results point towards the involvement of the hippocampus in preserving information about temporal order in motor memory - a process well described for declarative memories. We suggest that the ability of the hippocampus to encode temporal order during sequence learning is common across declarative and non-declarative memory systems.