Disruption of M1 Activity during Performance Plateau Impairs Consolidation of Motor Memories

Abstract

Upon exposure to a new sensorimotor relationship, motor behaviors iteratively change early in adaptation but eventually stabilize as adaptation proceeds. Behavioral work suggests that motor memory consolidation is initiated upon the attainment of asymptotic levels of performance. Separate lines of evidence point to a critical role of the primary motor cortex (M1) in consolidation. However, a causal relationship between M1 activity during asymptote and consolidation has yet to be demonstrated. The present study investigated this issue in male and female participants using single-pulse transcranial magnetic stimulation (TMS) to interfere with postmovement activity in M1 in two behavioral phases of a ramp-and-hold visuomotor adaptation paradigm. TMS was either provided after each trial of the ramp phase of adaptation when a gradual increase in the visuomotor rotation caused movements to be changing, or after each trial of the hold phase of adaptation when the rotation was held constant and movements tended to stabilize. Consolidation was assessed by measuring performance on the same task 24 h later. Results revealed that TMS did not influence adaptation to the new visuomotor relationship in either condition. Critically, however, TMS disruption of M1 activity selectively impaired consolidation of motor memories when it was provided during the hold phase of adaptation. This effect did not take place when TMS was delivered over adjacent dorsal premotor cortex or when motor behaviors in late adaptation were prevented from plateauing. Together, these data suggest that the impaired consolidation stemmed from interference with mechanisms of repetition-dependent plasticity in M1. The present work demonstrates that TMS disruption of M1 activity impairs the consolidation of motor memories selectively when performance reaches asymptotic levels during sensorimotor adaptation. These findings provide evidence for a causal contribution of M1 to motor memory formation when movements tend to repeat, likely through mechanisms of repetition-dependent plasticity.

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“…6B). We quantified spontaneous recovery as the change in the 9 displacement from the end of extinction trials (time 2 t ) to the error clamp block (time 3 t ), that is: 10…”