Diminished Auditory Responses during NREM Sleep Correlate with the Hierarchy of Language Processing

Abstract

Natural sleep provides a powerful model system for studying the neuronal correlates of awareness and state changes in the human brain. To quantitatively map the nature of sleep-induced modulations in sensory responses we presented participants with auditory stimuli possessing different levels of linguistic complexity. Ten participants were scanned using functional magnetic resonance imaging (fMRI) during the waking state and after falling asleep. Sleep staging was based on heart rate measures validated independently on 20 participants using concurrent EEG and heart rate measurements and the results were confirmed using permutation analysis. Participants were exposed to three types of auditory stimuli: scrambled sounds, meaningless word sentences and comprehensible sentences. During non-rapid eye movement (NREM) sleep, we found diminishing brain activation along the hierarchy of language processing, more pronounced in higher processing regions. Specifically, the auditory thalamus showed similar activation levels during sleep and waking states, primary auditory cortex remained activated but showed a significant reduction in auditory responses during sleep, and the high order language-related representation in inferior frontal gyrus (IFG) cortex showed a complete abolishment of responses during NREM sleep. In addition to an overall activation decrease in language processing regions in superior temporal gyrus and IFG, those areas manifested a loss of semantic selectivity during NREM sleep. Our results suggest that the decreased awareness to linguistic auditory stimuli during NREM sleep is linked to diminished activity in high order processing stations.

Modulation of phase-locked neural responses to speech during different arousal states is age-dependent

“…However, a recent study found no evidence that neural responses to speech signals were reduced at subcortical levels during nREM sleep (Wilf et al, 2016). Whilst FFRs were obtained in the present study by scalp-EEG, BOLD responses were obtained from fMRI in Wilf et al (2016).…”

“…However, neural responses to speech in subcortical (Portas et al, 2000) and cortical (Czisch et al, 2002(Czisch et al, , 2004Wilf et al, 2016) auditory regions reduce during sleep compared to wakefulness. Phase-locked responses to complex auditory signals change in different arousal states.…”

Relationship between neural phase-locked responses to speech and perception of speech in noise in young and older adults

“…It was found that both subcortical and cortical responses showed significant suppression in low arousal/nREM states compared to high arousal states (Mai et al, 2019). This accords with earlier functional imaging work that showed that neural responses to speech in subcortical (Portas et al, 2000) and cortical (Czisch et al, 2004; Wilf et al, 2016) auditory regions reduce during sleep compared to wakefulness. Also, significant correlations between behavioral measures and EEG parameters (FFRs and θ-PLV) were only found in the high arousal state (Mai et al, 2018).…”

Functional diversity of brain networks supports consciousness and verbal intelligence

“…Our results are consistent with previous findings from resting state studies, suggesting that anesthesia reduces the repertoire of discriminable brain states (52-53), and that during loss of consciousness global synchrony impairs information processing by leading to a breakdown of causal interactions between brain areas (54-56). Further, they are consistent with resting state studies using sleep-induced altered states of consciousness, which show that hyper-synchrony perturbs the feed-forward propagation of auditory information (57), as well as feedback projections (58), and more broadly, the stable patterns of causal interactions in response to external stimulation across the brain (59). While these previous resting state studies suggest that global synchrony breaks down causal interactions, the investigation of causal cortico-cortical interactions was outside the scope of this work.…”