Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep

• Published in: Nature neuroscience Vol. 25; no. 7; pp. 935 - 943
• Main Authors: Hayat, Hanna, Marmelshtein, Amit, Krom, Aaron J., Sela, Yaniv, Tankus, Ariel, Strauss, Ido, Fahoum, Firas, Fried, Itzhak, Nir, Yuval
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.07.2022; Nature Publishing Group
• Subjects: 631/378/1385/519; 631/378/3917; 9/30; Acoustic Stimulation; Animal Genetics and Genomics; Auditory Cortex - physiology; Auditory stimuli; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Cortex (auditory); Cortex (somatosensory); Cortex (temporal); EEG; Electroencephalography; Entrainment; Epilepsy; Eye movements; Feedback; Firing pattern; Hearing; Humans; Information processing; Neurobiology; Neurons - physiology; Neurosciences; NREM sleep; REM sleep; Robustness; Sensory integration; Sensory perception; Sensory stimuli; Signaling; Sleep; Sleep - physiology; Sleep and wakefulness; Spiking; Synchronization; Temporal lobe; Wakefulness; Wakefulness - physiology
• ISSN: 1097-6256; 1546-1726; 1546-1726
• DOI: 10.1038/s41593-022-01107-4

During sleep, sensory stimuli rarely trigger a behavioral response or conscious perception. However, it remains unclear whether sleep inhibits specific aspects of sensory processing, such as feedforward or feedback signaling. Here, we presented auditory stimuli (for example, click-trains, words, music) during wakefulness and sleep in patients with epilepsy, while recording neuronal spiking, microwire local field potentials, intracranial electroencephalogram and polysomnography. Auditory stimuli induced robust and selective spiking and high-gamma (80–200 Hz) power responses across the lateral temporal lobe during both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Sleep only moderately attenuated response magnitudes, mainly affecting late responses beyond early auditory cortex and entrainment to rapid click-trains in NREM sleep. By contrast, auditory-induced alpha–beta (10–30 Hz) desynchronization (that is, decreased power), prevalent in wakefulness, was strongly reduced in sleep. Thus, extensive auditory responses persist during sleep whereas alpha–beta power decrease, likely reflecting neural feedback processes, is deficient. More broadly, our findings suggest that feedback signaling is key to conscious sensory processing. Intracortical recordings in humans reveal that auditory stimulation during sleep induces robust spiking and high-gamma responses, whereas alpha–beta desynchronization—likely reflecting neural feedback processes—is reduced compared to wakefulness.