Prefrontal stimulation disrupts motor memory consolidation at the micro timescale

Abstract

Functional brain responses in hippocampo- and striato-cortical networks during initial motor sequence learning (MSL) are critical for memory consolidation. We have recently shown that prefrontal stimulation applied prior to initial MSL can alter these learning-related responses. In the present study, we investigated whether such stimulation-induced modulations of brain responses can influence motor memory consolidation at different timescales. Specifically, we examined the effect of prefrontal stimulation on the behavioral and neural responses associated to (i) fast consolidation processes occurring during short rest episodes interspersed with practice during initial learning (i.e., micro timescale) and (ii) slow consolidation process taking place across practice sessions separated by 24h (i.e., macro timescale). To do so, we applied active (inhibitory or facilitatory) or control theta-burst stimulation to the prefrontal cortex of young healthy participants before they were trained on an MSL task while their brain activity was recorded using functional magnetic resonance imaging (fMRI). Motor performance was retested, in the MRI scanner, after a night of sleep. Both our behavioral and brain imaging results indicate that while stimulation did not modulate consolidation at the macro timescale, it disrupted the micro-offline consolidation process. Specifically, our behavioral data indicate that active - as compared to control - stimulation resulted in a decrease in micro-offline gains in performance over the short rest intervals. At the brain level, stimulation disrupted activity in the caudate nucleus and the hippocampus during the micro-offline intervals. Additionally, multivariate pattern persistence from task into inter-practice rest episodes - which is thought to reflect the reactivation of learning-related patterns - was hindered by active prefrontal stimulation in the hippocampus and caudate nucleus. Importantly, stimulation also altered the link between the brain and the behavioral markers of the micro-offline consolidation process. These results collectively suggest that active prefrontal stimulation prior to MSL disrupted both the behavioral and neural correlates of motor memory consolidation at the micro timescale.