Impaired top-down auditory processing despite extensive single-neuron responses during human sleep

Abstract

Sleep is defined as a reversible, homeostatically-regulated state of a reduced behavioral responsiveness, and a high arousal threshold in response to external sensory stimulation defines sleep across all species. However, it remains unclear whether sleep mainly gates motor output or affects responses along sensory pathways, and if sleep primarily modulates specific aspects of the sensory response such as feedforward vs. feedback signaling. Here, we simultaneously recorded polysomnography, iEEG, microwire LFPs, and neuronal spiking activity in epilepsy patients implanted with clinical depth electrodes, while presenting auditory stimuli (e.g. click-trains, words, music) during wakefulness and sleep. We found robust spiking and induced LFP high-gamma (80-200Hz) power responses during both NREM and REM sleep across the lateral temporal lobe whose magnitude was only moderately attenuated, most notably for late responses beyond early auditory cortex. Nonetheless, sleep responses maintained their tight locking with soundwave envelopes and their information content was minimally affected. By contrast, LFP alpha-beta (10-30Hz) power decrease was prevalent in wakefulness but significantly disrupted in sleep. Entrainment to 40Hz click-trains was comparable across REM sleep and wakefulness but reduced in NREM sleep. Together, our results establish extensive and robust auditory responses during sleep while LFP alpha-beta power decrease, likely reflecting top-down processes, is deficient. More broadly, they point to feedback signalling as key in conscious sensory processing.

Sleep-like changes in neural processing emerge during sleep deprivation in early auditory cortex

“…During deep anesthesia, responses to high-frequency stimuli are attenuated in cat visual cortex (Rager, 1998) and in rodent somatosensory (Castro-Alamancos, 2004) and auditory cortex (Marguet and Harris, 2011). In natural sleep and light propofol anesthesia, auditory cortex of both rodents and humans reveals reduced responses to 40Hz click-trains (Bergman et al, 2022;Hayat et al, 2021;Krom et al, 2020), as has been originally observed with scalp EEG (Lustenberger et al, 2017;Plourde, 1990). Here, we extend these results to show that already during wakefulness, SD-induced Tired conditions entail sensory adaptation at significantly lower frequencies, acting like a low-pass filter that quenches high-frequency neural inputs and diminishes rapid transmission of information across brain regions.…”

“…How do the present results stand with respect to whether primary cortices are robustly modulated, or largely invariant, to brain states and arousal? On one hand, the effects of states such as sleep and anesthesia are typically more modest in primary cortex than in high-order regions (Davis et al, 2007; Hayat et al, 2021; Krom et al, 2020; Liu et al, 2012; Makov et al, 2017; Nourski et al, 2018, 2016; Sela et al, 2020; Sellers et al, 2015; Sharon and Nir, 2018). Similarly, the effects of neuromodulation, attention, and consciousness are more prevalent in high-order regions compared to early sensory cortex (Atiani et al, 2014; Gelbard-Sagiv et al, 2018; Leopold and Logothetis, 1996).…”

Sleep-like changes in neural processing emerge during sleep deprivation in early auditory cortex

“…How do the present results stand with respect to whether primary cortices are robustly modulated, or largely invariant, to brain states and arousal? On one hand, the effects of states such as sleep and anesthesia are typically more modest in primary cortex than in high-order regions (Davis et al, 2007;Hayat et al, 2021;Krom et al, 2020;Liu et al, 2012;Makov et al, 2017;Nourski et al, 2018Nourski et al, , 2016Sela et al, 2020;Sellers et al, 2015;Sharon and Nir, 2018). Similarly, the effects of neuromodulation, attention, and consciousness are more prevalent in high-order regions compared to early sensory cortex (Atiani et al, 2014;Gelbard-Sagiv et al, 2018;Leopold and Logothetis, 1996).…”

“…During deep anesthesia, responses to high-frequency stimuli are attenuated in cat visual cortex (Rager, 1998) and in rodent somatosensory (Castro-Alamancos, 2004) and auditory cortex (Marguet and Harris, 2011). In natural sleep and light propofol anesthesia, auditory cortex of both rodents and humans reveals reduced responses to 40Hz click-trains (Bergman et al, 2022;Hayat et al, 2021;Krom et al, 2020), as has been originally observed with scalp EEG (Lustenberger et al, 2017;Plourde, 1990). Here, we extend these results to show that already during wakefulness, SD-induced Tired conditions entail sensory adaptation at significantly lower frequencies, acting like a low-pass filter that quenches high-frequency neural inputs and diminishes rapid transmission of information across brain regions.…”