Coupling between motor cortex and striatum increases during sleep over long-term skill learning

Abstract

The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or 'offline' during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-REM (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.

Entrainment to sleep spindles reflects dissociable patterns of connectivity between cortex and basal ganglia

“…4D and 5A) also supports an MSN role in cross-region spindling. Indeed, sleep spindles were recently shown to facilitate corticostriatal transmission between M1 and dorsolateral striatum in rodents (Lemke et al, 2021).…”

“…Electrophysiological work in rodents has reported the replay of task-related activity in motor cortex, linked to the coincidence of SOs and bursts of spindle activity, and implicated these replay events with offline improvements in a skilled upper limb task (Ramanathan et al, 2015). Finally, a recent work showed that striatal reactivations during sleep spindles reflected cortical input (Lemke et al, 2021).…”

“…An EEG-fMRI study employing a motor sequence learning task in humans found that the degree of striatal reactivations, time-locked to sleep spindles, was correlated with overnight task improvement (Fogel et al, 2017). Finally, a recent study in rodents associated sleep spindles with peak corticostriatal transmission and demonstrated their importance in modifying the spiking relationship between specific M1 and striatal neurons during skill learning (Lemke et al, 2021).…”

Distributed and gradual microstructure changes track the emergence of behavioural benefit from memory reactivation

“…This late plasticity could also underpin the TMR-related functional engagement and grey matter volume increase of the sensorimotor cortex which we observed previously 24 . Interestingly, a recent rodent study found that cortico-striatal functional coupling increases during offline periods of rest and is required for long-term skill learning 49 . Furthermore, this coupling seems to be mediated by NREM sleep spindles 49 , which are known to be involved in motor learning 50 .…”

Dorsolateral striatum, not motor cortex, is a bottleneck for responding to task-relevant stimuli in a learned whisker detection task in mice

“…And yet, we do not believe that response inhibition is the sole function of motor cortex in rodents. Ample evidence, across species, supports motor cortex involvement in the learning and execution of skilled movements (Gandolfo et al, 2000;Hikosaka et al, 1995;Hwang et al, 2021;Kawai et al, 2015;Lemke et al, 2021;Muellbacher et al, 2002;Nakamura et al, 1998Nakamura et al, , 1999Puzerey et al, 2018). A more general framework of motor cortex is its involvement in 'motor control', which includes both motor activation and suppression as needed for performing a goal-directed task.…”