Bidirectional competitive interactions between motor memory and declarative memory during interleaved learning

Sungshin Kim

doi:10.1038/s41598-020-64039-8

Abstract

Distinct motor and declarative memory systems are widely thought to compete during memory consolidation and retrieval, yet the nature of their interactions during learning is less clear. Recent studies have suggested motor learning not only depend on implicit motor memory system supporting gradual tuning of responses by feedback but also depend on explicit declarative memory system. However, this competition has been identified when both systems are engaged in learning the same material (motor information), and so competition might be emphasized. We tested whether such competition also occurs when learning involved separate motor memory and declarative information presented distinctly but yet in close temporal proximity. We measured behavioral and brain-activity correlates of motor-declarative competition during learning using a novel task with interleaved motor-adaptation and declarative-learning demands. Despite unrelated motor versus declarative information and temporal segregation, motor learning interfered with declarative learning and declarative learning interfered with motor learning. This reciprocal competition was tightly coupled to corresponding reductions of fMRI activity in motor versus declarative learning systems. These findings suggest that distinct motor and declarative learning systems compete even when they are engaged by system-specific demands in close temporal proximity during memory formation.

Highlights

Distinct motor and declarative memory systems are widely thought to compete during memory consolidation and retrieval, yet the nature of their interactions during learning is less clear
We developed a novel fMRI task in which subjects performed visuomotor adaptation, which is a standard type of motor learning[3,4,5,6,17], interleaved with object-location association learning, which is a standard type of hippocampal-dependent declarative learning[18,19,20,21] (Fig. 1)
We predicted that the negative influence of motor learning on declarative learning would correlate with reduced activity in an declarative-memory network including hippocampal and medial-prefrontal areas

Summary

Introduction

Distinct motor and declarative memory systems are widely thought to compete during memory consolidation and retrieval, yet the nature of their interactions during learning is less clear. In the consolidation period after motor learning, presentation of word-list material to be learned explicitly interferes with subsequent expression of the previous motor learning, suggesting motor-declarative competition during consolidation that may arise from consolidation bandwidth limits[12,13,14,15,16] These studies retrospectively inferred interaction between the memory systems based on performance of tasks after consolidation period without any direct demonstration of underlying neural signatures[12,13,16] or pre-assumed that specific brain regions (e.g., DLPFC, M1) are associated with separate memory processing[14,15]. We predicted that the negative influence of motor learning on declarative learning would correlate with reduced activity in an declarative-memory network including hippocampal and medial-prefrontal areas This predicted pattern of findings would provide evidence for general competition between distinct motor and declarative memory systems; that is, competition even when learning involves distinct system-specific information presented in relatively close temporal proximity

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