Uncovering the role of the human hippocampus in procedural motor learning: Insights from implicit sensorimotor adaptation

Recent evidence suggests that the human hippocampus, traditionally associated with declarative memory, plays a role in motor sequence learning (MSL). However, the classic MSL paradigm depends initially on declarative learning. Thus, it is critical to discern whether the participation of the hippocampus relates to its canonical role or to processing a general aspect of learning that transcends the declarative/non-declarative distinction. To address this issue, here we turned to visuomotor adaptation -a type of motor learning involving skill recalibration- which unlike MSL can be easily manipulated to eliminate the explicit component. We examined the broader involvement of the hippocampus in procedural motor learning by using diffusion MRI in a sample of males and females to assess structural plasticity associated with memory consolidation in visuomotor adaptation (VMA) and an implicit-only version (IVMA). We found that both VMA and IVMA engaged the left posterior hippocampus in a learning-specific manner. Remarkably, while VMA induced only transient hippocampal alterations, IVMA elicited structural changes that persisted overnight, underscoring the reliance on implicit learning for enduring neuroplasticity. As expected, training on both tasks impacted the microstructure of the cerebellum, the motor and posterior parietal cortex. Notably, the temporal dynamics of changes in these regions paralleled those of the left hippocampus, suggesting that motor and limbic regions operate together as part of the same network. Collectively, our findings support an active role of the hippocampus in implicit motor learning and argue for a unified function in memory encoding regardless of the declarative or non-declarative nature of the task. Significance Statement Brenda Milner's work on patient H.M. introduced the concept of specialized memory systems in the brain but also inevitably initiated a dichotomy in cognitive neuroscience, with episodic learning viewed as hippocampus-dependent, and procedural learning as hippocampus-independent. This distinction fragmented the field of cognitive neuroscience, with studies on declarative and procedural memory progressing along parallel paths. Here, we show that a purely implicit motor task induces learning-specific structural plasticity in the human hippocampus. Notably, the temporal dynamics of these hippocampal changes were mirrored by key motor regions involved in acquisition, pointing to a close interaction between memory systems. Our findings provide evidence supporting the involvement of the human hippocampus in procedural motor memory and argue for common mechanisms supporting memory formation.