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

Krom, Aaron J; Marmelshtein, Amit; Gelbard-Sagiv, Hagar; Tankus, Ariel; Hayat, Hanna; Matot, Idit; Strauss, Ido; Fahoum, Firas; Soehle, Martin; Boström, Jan; Mormann, Florian; Fried, Itzhak; Nir, Yuval

doi:10.1101/502385

Cited by 19 publications

(34 citation statements)

References 85 publications

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“…In AC, comparable early responses in natural sleep observed here are in line with several recent reports (Peña et al, 1999;Edeline et al, 2001;Issa and Wang, 2008;Nir et al, 2015). In addition, a recent study comparing auditory responses at the neuronal level in humans across wakefulness and light anesthesia found a similar distinction between relatively preserved early responses in AC versus robust attenuation of late responses in association cortex (Krom et al, 2018).…”

Section: Discussionsupporting

confidence: 92%

Sleep Differentially Affects Early and Late Neuronal Responses to Sounds in Auditory and Perirhinal Cortices

et al. 2020

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A fundamental feature of sleep is reduced behavioral responsiveness to external events, but the extent of processing along sensory pathways remains poorly understood. While responses are comparable across wakefulness and sleep in auditory cortex (AC), neuronal activity in downstream regions remains unknown. Here we recorded spiking activity in 435 neuronal clusters evoked by acoustic stimuli in the perirhinal cortex (PRC) and in AC of freely behaving male rats across wakefulness and sleep. Neuronal responses in AC showed modest (ϳ10%) differences in response gain across vigilance states, replicating previous studies. By contrast, PRC neuronal responses were robustly attenuated by 47% and 36% during NREM sleep and REM sleep, respectively. Beyond the separation according to cortical region, response latency in each neuronal cluster was correlated with the degree of NREM sleep attenuation, such that late (Ͼ40 ms) responses in all monitored regions diminished during NREM sleep. The robust attenuation of late responses prevalent in PRC represents a novel neural correlate of sensory disconnection during sleep, opening new avenues for investigating the mediating mechanisms.

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Section: Discussionsupporting

confidence: 92%

Sleep Differentially Affects Early and Late Neuronal Responses to Sounds in Auditory and Perirhinal Cortices

et al. 2020

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“…In addition, a recent study comparing auditory responses at the neuronal level in humans across wakefulness and light anesthesia found a similar distinction between relatively preserved early responses in AC vs. robust attenuation of late responses in association cortex (Krom et al, 2018). What could be the source of apparent discrepancy with earlier studies in other sensory modalities that reported attenuated spiking responses in primary cortices during natural sleep?…”

Section: Discussionmentioning

confidence: 86%

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

Sela

Krom

Bergman

et al. 2019

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Number of multimedia and 3D models: 0 Number of words for abstract (max 250): 171 Number of words for introduction (max 650): 596 Number of words for discussion (max 1500): 919Reduced behavioral responsiveness to sensory stimulation is at the core of sleep's definition, but it is still unclear how the sleeping brain responds differently to sensory stimuli. In the current study we recorded neuronal spiking responses to sounds along the cortical processing hierarchy of rats during wakefulness and natural sleep. Responses in auditory cortex only showed modest changes during sleep, whereas sleep robustly attenuated the responses of neurons in high-level perirhinal cortex. We also found that during NREM sleep, the response latency predicts the degree of sleep attenuation in individual neurons above and beyond their anatomical location. These results provide anatomical and temporal signatures of sensory disconnection during sleep and pave the way to understanding the underlying mechanisms.

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“…While the current results indicate that LC activity robustly modulates SEA, it remains unclear to what extent this co-occurs with corresponding response modulations along sensory pathways. While LC-NE signaling clearly modifies response fidelity across sensory modalities and species 49,94–96 , it is unlikely that it simply “gates” propagation of auditory signals to the cortex as auditory responses in primary cortex are largely comparable across vigilance states 97–99 . Instead, tonic LC activity that drives SEAs may facilitate sensory processing downstream from primary regions, by acting at higher-order regions or non-sensory pathways to promote awakenings.…”

Section: Discussionmentioning

confidence: 99%

Locus-coeruleus norepinephrine activity gates sensory-evoked awakenings from sleep

Hayat

Regev

Matosevich

et al. 2019

Preprint

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AbstractA defining feature of sleep is reduced responsiveness to external stimuli, but the mechanisms gating sensory-evoked arousal remain unclear. We hypothesized that reduced locus-coeruleus norepinephrine (LC-NE) activity during sleep mediates unresponsiveness, and its action promotes sensory-evoked awakenings. We tested this using electrophysiological, behavioral, pharmacological, and optogenetic techniques alongside auditory stimulation in freely behaving rats. We found that systemic reduction of NE signaling lowered probability of sound-evoked awakenings (SEAs). The level of tonic LC activity during sleep anticipated SEAs. Optogenetic LC activation promoted arousal as evident in sleep-wake transitions, EEG desynchronization, and pupil dilation. Importantly, liminal LC excitation before sound presentation increased SEA probability. Optogenetic LC silencing using a soma-targeted anion-conducting channelrhodopsin (stGtACR2) suppressed LC spiking and constricted pupils. Brief periods of LC opto-silencing reduced the probability of SEAs. Thus, LC-NE activity determines the likelihood of sensory-evoked awakenings and its reduction during sleep constitutes a key factor mediating behavioral unresponsiveness.

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

Cited by 19 publications

References 85 publications

Sleep Differentially Affects Early and Late Neuronal Responses to Sounds in Auditory and Perirhinal Cortices

Sleep Differentially Affects Early and Late Neuronal Responses to Sounds in Auditory and Perirhinal Cortices

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

Locus-coeruleus norepinephrine activity gates sensory-evoked awakenings from sleep

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