Altered functional connectivity in the hippocampal and striatal systems after motor sequence learning consolidation in medial temporal lobe epilepsy individuals.

ABSTRACT

Both the hippocampal and striatal systems participate in motor sequence learning (MSL) in healthy subjects, and the prominent role of the hippocampal system in sleep-related consolidation has been demonstrated. However, some pathological states may change the functional dominance between these two systems in MSL consolidation. To better understand the functional performance within these two systems under the pathological condition of hippocampal impairment, we compared the functional differences after consolidation between patients with left medial temporal lobe epilepsy (LmTLE) and healthy control subjects (HCs). We assessed participants' performance on the finger-tapping task (FTT) during acquisition (on day 1) and after consolidation during sleep (on day 2). All participants underwent an MRI scan (T1 and resting state) before each FTT. We found that the LmTLE group showed performance deficits in offline consolidation compared to the HC group. The LmTLE group exhibited structural changes, such as decreased gray matter volume (GMV) in the left hippocampus and increased GMV in the right putamen (striatum). Our results also revealed that whereas the main effect of consolidation was observed in the hippocampus-related functional connection in the HC group, it was only evident in the striatum-related functional loop in the LmTLE group. Our findings indicated that LmTLE patients may rely more on the striatal system for offline consolidation because of structural impairments in the hippocampus. Additionally, this compensatory mechanism may not fully substitute for the role of the impaired hippocampus itself.NEW & NOTEWORTHY Motor sequence learning (MSL) relies on both the hippocampal and striatal systems, but whether functional performance is altered after MSL consolidation when the hippocampus is impaired remains unknown. Our results indicated that whereas the main effect of consolidation was observed in the hippocampus-related functional connection in the healthy control (HC) group, it was only evident in the striatum-related functional loop in the left medial temporal lobe epilepsy (LmTLE) group.