Cued Reactivation of Motor Learning during Sleep Leads to Overnight Changes in Functional Brain Activity and Connectivity - PubMed (original) (raw)

Cued Reactivation of Motor Learning during Sleep Leads to Overnight Changes in Functional Brain Activity and Connectivity

James N Cousins et al. PLoS Biol. 2016.

Abstract

Sleep plays a role in memory consolidation. This is demonstrated by improved performance and neural plasticity underlying that improvement after sleep. Targeted memory reactivation (TMR) allows the manipulation of sleep-dependent consolidation through intentionally biasing the replay of specific memories in sleep, but the underlying neural basis of these altered memories remains unclear. We use functional magnetic resonance imaging (fMRI) to show a change in the neural representation of a motor memory after targeted reactivation in slow-wave sleep (SWS). Participants learned two serial reaction time task (SRTT) sequences associated with different auditory tones (high or low pitch). During subsequent SWS, one sequence was reactivated by replaying the associated tones. Participants were retested on both sequences the following day during fMRI. As predicted, they showed faster reaction times for the cued sequence after targeted memory reactivation. Furthermore, increased activity in bilateral caudate nucleus and hippocampus for the cued relative to uncued sequence was associated with time in SWS, while increased cerebellar and cortical motor activity was related to time in rapid eye movement (REM) sleep. Functional connectivity between the caudate nucleus and hippocampus was also increased after targeted memory reactivation. These findings suggest that the offline performance gains associated with memory reactivation are supported by altered functional activity in key cognitive and motor networks, and that this consolidation is differentially mediated by both REM sleep and SWS.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1

Fig 1. Schematic of experiment design.

(a) Learning (L) of the SRTT task consisted of interleaved blocks of the cued and uncued sequence, and also random blocks. (b) The cued sequence is replayed during periods of SWS in groups of 12 sequences (CUE) and equivalent periods of silence (NO-CUE). (c) Retest (R) of the SRTT takes place the following morning in the MRI scanner, followed shortly afterwards by the explicit memory test outside of the scanner.

Fig 2

Fig 2. Performance improvement at retest.

(a) Comparison of presleep sequence performance to early blocks of sequence retest showed a significant cueing effect. (b) Accuracy improvement was also significantly greater for the cued sequence at early blocks. (c) Performance improvement for both sequences was comparable at late sequence blocks and random blocks that followed. Error bars represent standard error of the mean (SEM) (S1 Data).

Fig 3

Fig 3. Changes in brain activity after targeted-memory reactivation.

(a) The basic comparison between cued and uncued showed reduced activity in left caudate (−20, 24, −10) for the cued sequence. (b) SWS was associated with enhanced activation in bilateral caudate (16, 8, 20 and −12, 20, 12), and bilateral hippocampi (26, −34, 2 and −22, −34, 6) for the cued sequence relative to the uncued. (b) REM sleep was associated with cueing related activity enhancement in left cerebellum (−32, −54, −44 and 20 −72, −26), left superior parietal cortex (−28, −56, 68 and 22, −54, 38), left sensorimotor cortex (SMC) (−40, −32, 68), left dorsolateral prefrontal cortex (dlPFC) (−30, 34, 28) and right premotor cortex (PMC) (42, −2, 32 and 42, −2, 58). These findings were whole brain corrected (p < 0.05) and displayed as sagittal and coronal projections superimposed on a standard Montreal Neurological Institute (MNI) brain. Colour bar indicates t-values. Anatomical labelling based on peak z-score location.

Fig 4

Fig 4. Regions of increased functional connectivity after TMR.

A PPI analysis revealed enhanced connectivity for the cued sequence between left hippocampus (−22, −34, 6) and right putamen (36, −2, 4) and PMC (58, 4, 22). Contrasts displayed as sagittal and coronal projections superimposed on a standard MNI brain. Colour bar indicates t-values. Anatomical labelling based on peak z-score location.

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