Slow Oscillation-Spindle Coupling Predicts Sequence-Based Language Learning.

Sentence comprehension involves the decoding of both semantic and grammatical information, a process fundamental to communication. As with other complex cognitive processes, language comprehension relies, in part, on long-term memory. However, the electrophysiological mechanisms underpinning the encoding and generalization of higher-order linguistic knowledge remain elusive, particularly from a sleep-based consolidation perspective. One candidate mechanism that may support the consolidation of higher-order language is the coordination of slow oscillations (SO) and sleep spindles during nonrapid eye movement sleep (NREM). To examine this hypothesis, we analyzed electroencephalographic (EEG) data recorded from 35 participants (  = 25.4; SD = 7.10; 16 males) during an artificial language learning task, contrasting performance between individuals who were given an 8 h nocturnal sleep period or an equivalent period of wake. We found that sleep relative to wake was associated with superior performance for sequence-based word order rules. Postsleep sequence-based word order processing was further associated with less task-related theta desynchronization, an electrophysiological signature of successful memory consolidation, as well as cognitive control and working memory. Frontal NREM SO-spindle coupling was also positively associated with behavioral sensitivity to sequence-based word order rules, as well as with task-related theta power. As such, theta activity during retrieval of previously learned information correlates with SO-spindle coupling, thus linking neural activity in the sleeping and waking brain. Taken together, this study presents converging behavioral and neurophysiological evidence for a role of NREM SO-spindle coupling and task-related theta activity as signatures of memory consolidation and retrieval in the context of higher-order language learning.