Hippocampal ripples mediate motor learning during brief rest breaks in humans
Although research on the hippocampus has largely focused on its role in active learning, critical aspects of learning and memory happen offline, during both wake and sleep. When healthy young people learn a motor sequence task, most of their performance improvement happens not while typing, but offline, during interleaved rest breaks. Although patients with dense amnesia due to hippocampal damage show a normal amount of motor sequence learning, they show a different pattern. They actually lose speed over the breaks and compensate while typing. This indicates that an intact hippocampus is necessary for offline motor learning during wake but does not specify its mechanism. Here, we studied epilepsy patients (n=20) undergoing direct intracranial EEG monitoring of the hippocampus as they learned the same motor sequence task. Like healthy young people, they showed greater speed gains across rest breaks than while typing. They also showed a higher ripple rate during the breaks that predicted offline gains in speed. This suggests that motor learning during brief rest breaks during wake is mediated by hippocampal ripples. These findings complement rodent studies showing memory replay during hippocampal ripples in the wakeful rest that follows learning. Disrupting these ripples impairs memory, consistent with a causal role. The findings also provide a mechanistic explanation of human neuroimaging reports of increased hippocampal activation and sequential motor memory replay during rest breaks that predict performance improvement. Finally, they expand our understanding of the role of hippocampal ripples beyond declarative memory to include enhancing motor procedural memory.