Sleep Disrupts High-Level Speech Parsing Despite Significant Basic Auditory Processing

Abstract

The extent to which the sleeping brain processes sensory information remains unclear. This is particularly true for continuous and complex stimuli such as speech, in which information is organized into hierarchically embedded structures. Recently, novel metrics for assessing the neural representation of continuous speech have been developed using noninvasive brain recordings that have thus far only been tested during wakefulness. Here we investigated, for the first time, the sleeping brain's capacity to process continuous speech at different hierarchical levels using a newly developed Concurrent Hierarchical Tracking (CHT) approach that allows monitoring the neural representation and processing-depth of continuous speech online. Speech sequences were compiled with syllables, words, phrases, and sentences occurring at fixed time intervals such that different linguistic levels correspond to distinct frequencies. This enabled us to distinguish their neural signatures in brain activity. We compared the neural tracking of intelligible versus unintelligible (scrambled and foreign) speech across states of wakefulness and sleep using high-density EEG in humans. We found that neural tracking of stimulus acoustics was comparable across wakefulness and sleep and similar across all conditions regardless of speech intelligibility. In contrast, neural tracking of higher-order linguistic constructs (words, phrases, and sentences) was only observed for intelligible speech during wakefulness and could not be detected at all during nonrapid eye movement or rapid eye movement sleep. These results suggest that, whereas low-level auditory processing is relatively preserved during sleep, higher-level hierarchical linguistic parsing is severely disrupted, thereby revealing the capacity and limits of language processing during sleep. Despite the persistence of some sensory processing during sleep, it is unclear whether high-level cognitive processes such as speech parsing are also preserved. We used a novel approach for studying the depth of speech processing across wakefulness and sleep while tracking neuronal activity with EEG. We found that responses to the auditory sound stream remained intact; however, the sleeping brain did not show signs of hierarchical parsing of the continuous stream of syllables into words, phrases, and sentences. The results suggest that sleep imposes a functional barrier between basic sensory processing and high-level cognitive processing. This paradigm also holds promise for studying residual cognitive abilities in a wide array of unresponsive states.

Sleep differentially affects early and late neuronal responses to sounds in auditory and perirhinal cortices

“…TMR has been shown to influence hippocampal activity during sleep (Rasch et al, 2007;Rothschild et al, 2017), suggesting that sounds can modulate activity in association cortices. On the other hand, non-invasive imaging in humans suggests that during sleep, auditory responses downstream from auditory cortex (AC) are attenuated: studies using magnetoencephalography (MEG) (Kakigi et al, 2003;Strauss et al, 2015), electroencephalography (EEG) (Makov et al, 2017), and functional magnetic resonance imaging (fMRI) (Portas et al, 2000) suggest comparable responses across vigilance states in early sensory regions and robust attenuation in association cortex. However, investigation of sensory responses downstream from sensory cortical regions at the level of neuronal spiking activity is still missing.…”

Anesthesia-induced loss of consciousness disrupts auditory responses beyond primary cortex

“…properties and PAC responses(50) vs. high-order activity in association cortex (51). Thus, a functional disconnection between primary sensory and association cortex may be a general property of LOC not only due to anesthesia, as demonstrated also by direct perturbation of cortical activity with transcranial magnetic stimulation (TMS) (52)(53)(54).…”

Low-frequency Neural Activity Reflects Rule-based Chunking during Speech Listening

“…Neural tracking of linguistic structures strongly depends on the task, demonstrating an active chunking process. Neural tracking of multisyllabic words and multi-word chunks is largely abolished during sleep (Makov et al, 2017) or when the listeners are distracted by competing sensory stimuli . Here, it is further demonstrated that neural tracking of a structurally ambiguous sequence relies on the chunking rule.…”

“…Recent neurophysiological results have been shown that when presented with speech, the brain concurrently tracks multiple levels of linguistic units, such as sentences, phrases, words, and syllables ( Fig. 1) (Ding et al, 2016;Makov et al, 2017;Brodbeck et al, 2018;Broderick et al, 2018;Ding et al, 2018;Keitel et al, 2018).…”