Sleep consolidates stimulus-response learning

Abstract

Performing a motor response to a sensory stimulus creates a memory trace whose behavioral correlates are classically investigated in terms of repetition priming effects. Such stimulus-response learning entails two types of associations that are partly independent: (1) an association between the stimulus and the motor response and (2) an association between the stimulus and the classification task in which it is encountered. Here, we tested whether sleep supports long-lasting stimulus-response learning on a task requiring participants (1) for establishing stimulus-classification associations to classify presented objects along two different dimensions ("size" and "mechanical") and (2) as motor response (action) to respond with either the left or right index finger. Moreover, we examined whether strengthening of stimulus-classification associations is preferentially linked to nonrapid eye movement (non-REM) sleep and strengthening of stimulus-action associations to REM sleep. We tested 48 healthy volunteers in a between-subjects design comparing postlearning retention periods of nighttime sleep versus daytime wakefulness. At postretention testing, we found that sleep supports consolidation of both stimulus-action and stimulus-classification associations, as indicated by increased reaction times in "switch conditions"; that is, when, at test, the acutely instructed classification task and/or correct motor response for a given stimulus differed from that during original learning. Polysomnographic recordings revealed that both kinds of associations were correlated with non-REM spindle activity. Our results do not support the view of differential roles for non-REM and REM sleep in the consolidation of stimulus-classification and stimulus-action associations, respectively.

Figure 1.

Task and experimental procedure. (A) Learning trial: Each trial started with a task cue followed by presentation of an object image and ended after a response was given or the time limit of 1800 msec elapsed. (B) Task conditions during immediate and remote tests: Each object could be associated with the same classification task and response side as during learning (that is, classification repeat/action repeat [CrAr]) or presented with switched task or response associations (CrAs, CsAr, and CsAs). (C) Experimental procedure for wake and sleep groups.

Figure 2.

RT switch costs and accuracy at the immediate and remote tests for the wake (green) and sleep (black) groups. (A) Action switch costs decreased across the wake retention interval but increased across the sleep interval. (B) Classification switch costs decreased across both wake and sleep retention intervals. (C) If classification task and action jointly switched, full switch costs slightly decreased across retention intervals and remained above zero in both wake and sleep groups. (D) Accuracy only decayed across the wake retention interval, leading to a higher accuracy for the sleep than the wake group at remote test. Means ± SEM are indicated (dot plots overlaid). Asterisks above individual conditions indicate significant differences from zero. (***) P < 0.001, (**) P < 0.01, (*) P < 0.05.

Figure 3.

(A) Slow (green triangles) and fast (black circles) spindle activity in stage 2 sleep positively correlated with action switch costs (remote test–immediate test). (B) Slow and fast spindle activity during non-REM sleep (stage 2 sleep + SWS) positively correlated with classification switch costs. Results are shown for the sites of maximum correlations.