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 Sela Krom Bergman Regev Nir

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Sleep Differentially Affects Early and Late Neuronal Responses to Sounds in Auditory and Perirhinal Cortices 2020 Journal of Neuroscience 10.1523/jneurosci.1186-19.2020 Sela2020-sleep-differentially-affects-early-and-late Sela2020-sleep-differentially-affects-early-and-late.txt, the project's staged copy 6b396fafa26b56a046b63a87533f124ef623a9b0 not-redistributable sleep-neuroscience

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0 spans located by searching the stored text for the quote's exact words, allowing any whitespace between them Auditory responses of neurons in auditory cortex and in the downstream perirhinal cortex, compared across wakefulness, NREM and REM sleep. Quotation withheld because this record is not cleared for redistribution. Auditory cortex responds to sound much the same asleep as awake - so where along the pathway does the sleeping brain actually stop listening? Quotation withheld because this record is not cleared for redistribution. Perirhinal responses are attenuated by 47% in NREM and 36% in REM while auditory cortex barely changes - and response latency predicts the attenuation better than cortical region does. Quotation withheld because this record is not cleared for redistribution. existence Quotation withheld because this record is not cleared for redistribution. sleep attenuation of auditory responses in high-order cortex Quotation withheld because this record is not cleared for redistribution. electrophysiology electrophysiology Quotation withheld because this record is not cleared for redistribution. mechanisms NREM sleep imposes a graded, cumulative attenuation that builds up along the processing hierarchy rather than a single discrete gate at one anatomical station Quotation withheld because this record is not cleared for redistribution. mechanisms Breakdown of cortical effective connectivity in NREM sleep means signals lose more strength at each additional synapse, so responses arriving later are attenuated more Quotation withheld because this record is not cleared for redistribution. mechanisms the disconnection is not at the sensory front end: auditory cortex responds nearly as strongly asleep as awake, so whatever gates perception acts further downstream Quotation withheld because this record is not cleared for redistribution. mechanisms perirhinal cortex is the candidate site because it is multimodal, downstream of several primary cortices, and carries intrinsic inhibition controlling flow to the hippocampus Quotation withheld because this record is not cleared for redistribution. mechanisms the operative variable is TIME not PLACE: whatever suppresses the response acts on late activity wherever it occurs, not on a particular region Quotation withheld because this record is not cleared for redistribution. mechanisms the older explanation - thalamic gating - was already in trouble, because olfactory responses that bypass the thalamus are attenuated too Quotation withheld because this record is not cleared for redistribution. Stimulation was passive, so effects of behaviourally relevant or rewarded sounds were not assessed. what this limits: any claim about behaviourally relevant sounds: WE USED A PASSIVE AUDITORY STIMULATION SCHEME WHERE SOUNDS WERE NOT ASSOCIATED WITH SPECIFIC BEHAVIORS OR REWARDS Quotation withheld because this record is not cleared for redistribution. The latency-attenuation relationship found in NREM sleep did not hold in REM sleep. what this limits: the latency-attenuation relationship outside NREM: IN REM SLEEP, ATTENUATION DID NOT CLEARLY FOLLOW RESPONSE LATENCY AS WAS THE CASE DURING NREM SLEEP (DATA NOT SHOWN) Quotation withheld because this record is not cleared for redistribution. The proposed REM-sleep explanation is offered as speculation. what this limits: the REM explanation only: ALTHOUGH SPECULATIVE, IT IS POSSIBLE THAT, DURING REM SLEEP, ONGOING MNEMONIC ACTIVITY DURING DREAMING INTERFERES WITH BOTTOM-UP SENSORY PROCESSES Quotation withheld because this record is not cleared for redistribution. Ten rats, male only, in two strains. what this limits: the population the result speaks for: EXPERIMENTS WERE PERFORMED IN 8 LONG-EVANS AND 2 WISTAR ADULT MALE RATS Quotation withheld because this record is not cleared for redistribution. The result is a correlate, and the paper says the mediating mechanism remains to be investigated. what this limits: the causal reading: the finding REPRESENTS A NOVEL NEURAL CORRELATE OF SENSORY DISCONNECTION DURING SLEEP, with the mediating mechanism left to future work Quotation withheld because this record is not cleared for redistribution. Prior evidence about perirhinal auditory responses is inconsistent, with anaesthetised preparations failing to find them at all. what this limits: any comparison with the anaesthetised perirhinal literature: SEPARATE STUDIES DURING ANESTHESIA DID NOT REVEAL SIGNIFICANT AUDITORY RESPONSES AS ONE MOVES VENTRALLY TOWARD RHINAL cortex, while waking studies find reliable responses Quotation withheld because this record is not cleared for redistribution. The literature the study enters is thin: few studies have examined sensory responses in natural sleep at the neuronal level at all. what this limits: the evidence base this study joins: SURPRISINGLY, ONLY FEW STUDIES INVESTIGATED SENSORY RESPONSES DURING NATURAL SLEEP AT THE NEURONAL LEVEL Quotation withheld because this record is not cleared for redistribution. neurons with peak latencies in the 20-40 ms band DROPPED from the latency-based split, keeping only <20 ms and >40 ms eliminates: ambiguous cases deciding the early/late contrast - a neuron near the boundary can fall either side on noise, and those are exactly the cases a threshold chosen after looking would assign favourably · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. the first second after each auditory stimulus EXCLUDED before smoothing when detecting OFF periods eliminates: stimulus-induced firing reductions being counted as spontaneous OFF periods - the sound itself suppresses firing, so an OFF-period detector run over that window would find the stimulus and report sleep · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. sleep sleep Quotation withheld because this record is not cleared for redistribution. sensory disconnection sensory disconnection Quotation withheld because this record is not cleared for redistribution. response latency response latency Quotation withheld because this record is not cleared for redistribution. perirhinal cortex perirhinal cortex Quotation withheld because this record is not cleared for redistribution. auditory cortex auditory cortex Quotation withheld because this record is not cleared for redistribution. thalamic gating thalamic gating Quotation withheld because this record is not cleared for redistribution. targeted memory reactivation targeted memory reactivation Quotation withheld because this record is not cleared for redistribution. sleep - behavioural: the state in which an animal stops responding to what happens around it Quotation withheld because this record is not cleared for redistribution. sleep - neural: a set of vigilance states, NREM and REM, that attenuate responses by different amounts Quotation withheld because this record is not cleared for redistribution. disconnection - not an absence of processing: discriminative sensory processing continues while perception does not follow Quotation withheld because this record is not cleared for redistribution. claim_type: existence a second reading reaching the same value. Recorded: existence — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. phenomenon: sensory disconnection during sleep, and where along the cortical hierarchy it takes effect a second reading DIFFERING from the recorded value. Recorded: sleep attenuation of auditory responses in high-order cortex — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. replicates → reports of preserved auditory cortical responses across vigilance states (Issa and Wang, 2008; Nir et al., 2015) Quotation withheld because this record is not cleared for redistribution. extends → Krom et al. (2018), the same early/late distinction observed in humans under light anesthesia Quotation withheld because this record is not cleared for redistribution. contradicts → Pereira et al. (2007), increased hippocampal responses to somatosensory microstimulation during sleep Quotation withheld because this record is not cleared for redistribution. contradicts → the "thalamic gating" model (Steriade and McCarley, 1990), which posits a discrete gate rather than graded attenuation differs in: THE AXIS IS RESPONSE LATENCY. 'The robust correlation of NREM sleep attenuation with response latency suggests that NREM sleep may exert A GRADUAL ATTENUATION of cortical responses, RATHER THAN IMPOSING A DISCRETE GATE at a specific brain region.' A gate predicts a step at one locus; the graded alternative predicts a monotone relationship with latency - so the two accounts differ on a measurable parameter rather than on a location. Quotation withheld because this record is not cleared for redistribution. replicates → prior findings that auditory cortex responses are comparable across wakefulness and sleep Quotation withheld because this record is not cleared for redistribution. contradicts → the thalamic gating model of sleep-related sensory disconnection Quotation withheld because this record is not cleared for redistribution. extends → human imaging work showing attenuation downstream of sensory cortex during sleep Quotation withheld because this record is not cleared for redistribution. EVIDENCE CORRECTED (RE-GROUNDED) · perirhinal cortex —contrasted-with→ auditory cortex perirhinal cortex auditory cortex EVIDENCE CORRECTED: RE-GROUNDED. The old span named neither area. This sentence names both and states the contrast with its direction - modest changes in auditory cortex, robust attenuation in perirhinal. — strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. RETRACTED (THE 'to' ENDPOINT IS THE TAGGER'S PHRASE) · sleep —causes→ sensory disconnection sleep sensory disconnection RETRACTED: THE 'to' ENDPOINT IS THE TAGGER'S PHRASE. The edge is 'sleep --causes--> sensory disconnection'. The span: 'WERE ROBUSTLY…' 'Sensory disconnection' does not occur - as a word or at all. What the sentence reports is a MEASURED ATTENUATION with two numbers attached; 'sensory disconnection' is the interpretation those numbers are usually put to, supplied from knowledge of the literature. TRUE OF THE FIELD, UNSUPPORTED BY THE SPAN - and note the edge also drops the 47% and 36%, which are the only things the sentence actually establishes. Found by the neighbour query. — strength of the relation: 1 Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span says responses were attenuated during sleep; the endpoint 'sensory disconnection' is interpretive. Quotation withheld because this record is not cleared for redistribution. Mann-Whitney U test Mann-Whitney U test Quotation withheld because this record is not cleared for redistribution. Mann-Whitney test (one-tailed) Mann-Whitney test (one-tailed) Quotation withheld because this record is not cleared for redistribution. false discovery rate correction for multiple comparisons false discovery rate correction for multiple comparisons Quotation withheld because this record is not cleared for redistribution. significance level (alpha) significance level (alpha) Quotation withheld because this record is not cleared for redistribution. Wilcoxon signed-rank test Wilcoxon signed-rank test Quotation withheld because this record is not cleared for redistribution. correlation correlation Quotation withheld because this record is not cleared for redistribution. confidence interval confidence interval Quotation withheld because this record is not cleared for redistribution. z score z score Quotation withheld because this record is not cleared for redistribution. standard deviation standard deviation Quotation withheld because this record is not cleared for redistribution. correlation correlation Quotation withheld because this record is not cleared for redistribution. proportion proportion Quotation withheld because this record is not cleared for redistribution. Auditory cortex responses changed only about 10% across vigilance states, whereas perirhinal cortex responses were cut by 47% in NREM sleep and 36% in REM sleep. Quotation withheld because this record is not cleared for redistribution. Median gain factors quantified the perirhinal attenuation as -47% in NREM sleep and -36% in REM sleep, with confidence intervals excluding zero. Quotation withheld because this record is not cleared for redistribution. Auditory cortex neurons showed only small median gain changes of -12% in NREM sleep and -6% in REM sleep. Quotation withheld because this record is not cleared for redistribution. Across all recorded neurons, the later a neuron's peak response latency, the more its response was attenuated in NREM sleep, a strong negative correlation. Quotation withheld because this record is not cleared for redistribution. Neurons whose latency did not match their region behaved according to latency, not anatomy: late-responding auditory cortex neurons were attenuated by 43% while early-responding perirhinal neurons were attenuated by only 3%. Quotation withheld because this record is not cleared for redistribution. Early-responding neurons showed modest gain change in NREM sleep (-5.4%) against robust attenuation (-41%) for late-responding neurons, an eightfold difference. Quotation withheld because this record is not cleared for redistribution. 85% of neurons peaking under 20 ms were in auditory cortex and 89% of those peaking over 40 ms were in perirhinal cortex. Quotation withheld because this record is not cleared for redistribution. Baseline firing rates in auditory cortex were 21-26% higher in wakefulness and REM sleep than in NREM sleep. Quotation withheld because this record is not cleared for redistribution. Within NREM sleep, late-responding neurons responded more strongly to sounds delivered during local OFF periods than during ON periods. Quotation withheld because this record is not cleared for redistribution. Short-latency neurons tended to have narrower action potential waveforms than long-latency neurons. Quotation withheld because this record is not cleared for redistribution. Auditory cortex responses change only about 10% between waking and sleep - replicating earlier work. Quotation withheld because this record is not cleared for redistribution. Perirhinal responses fall by 47% in NREM and 36% in REM sleep. Quotation withheld because this record is not cleared for redistribution. Late responses are suppressed wherever they occur, so latency rather than anatomy is the better predictor of sleep attenuation. Quotation withheld because this record is not cleared for redistribution. Sleep does not abolish sensory processing - some discriminative processing survives even though stimuli rarely reach perception. Quotation withheld because this record is not cleared for redistribution. gain factor gain factor Quotation withheld because this record is not cleared for redistribution. early- and late-responding neurons early- and late-responding neurons Quotation withheld because this record is not cleared for redistribution. spontaneous firing rate spontaneous firing rate Quotation withheld because this record is not cleared for redistribution. thalamic gating thalamic gating Quotation withheld because this record is not cleared for redistribution. neuronal ON/OFF periods neuronal ON/OFF periods Quotation withheld because this record is not cleared for redistribution. sleep sleep Quotation withheld because this record is not cleared for redistribution. perirhinal cortex perirhinal cortex Quotation withheld because this record is not cleared for redistribution. vigilance state vigilance state Quotation withheld because this record is not cleared for redistribution. cortical region cortical region Quotation withheld because this record is not cleared for redistribution. response latency response latency Quotation withheld because this record is not cleared for redistribution. 435 — Number of neuronal clusters whose sound-evoked spiking was recorded Quotation withheld because this record is not cleared for redistribution. 47% and 36% — Attenuation of perirhinal cortex responses during NREM sleep and REM sleep respectively Quotation withheld because this record is not cleared for redistribution. r = −0.55, p = 10 −15 — Correlation between a neuron's peak response latency and its NREM sleep gain attenuation Quotation withheld because this record is not cleared for redistribution. 85% / 89% — Proportion of sub-20 ms neurons located in auditory cortex, and of over-40 ms neurons located in perirhinal cortex Quotation withheld because this record is not cleared for redistribution. −43% ... −3% — NREM gain factor for latency-atypical neurons: late-responding AC neurons versus early-responding PRC neurons Quotation withheld because this record is not cleared for redistribution. 8-fold — Difference in NREM attenuation between early- and late-responding neurons recorded on the same microwire Quotation withheld because this record is not cleared for redistribution. 21%–26% — Excess baseline firing rate of auditory cortex neurons in wakefulness or REM sleep relative to NREM sleep Quotation withheld because this record is not cleared for redistribution. n = 10 — Number of adult male rats implanted with microwire arrays Quotation withheld because this record is not cleared for redistribution. n = 178 ... n = 132 — Numbers of responsive neuronal clusters assigned to auditory cortex and to perirhinal cortex by histology Quotation withheld because this record is not cleared for redistribution. 15 ± 6.3%, 41 ± 6.2%, and 8 ± 2.4% — Proportion of experiment time spent in quiet wake, NREM sleep and REM sleep Quotation withheld because this record is not cleared for redistribution. 435 neuronal clusters — size of the recorded population across both regions Quotation withheld because this record is not cleared for redistribution. 47% (NREM) and 36% (REM) — attenuation of perirhinal auditory responses relative to wakefulness Quotation withheld because this record is not cleared for redistribution. ~10% — the much smaller change in auditory cortex response gain across vigilance states Quotation withheld because this record is not cleared for redistribution. <20 ms in AC, >40 ms in PRC — typical response latencies, and the axis along which attenuation is organised Quotation withheld because this record is not cleared for redistribution. 10 rats — 8 Long-Evans and 2 Wistar adult males Quotation withheld because this record is not cleared for redistribution.

The full text of this article is not redistributable, so it is not included here. The evidence sentences are withheld with it; the tag layer and its grounding status remain. The article itself is at https://doi.org/10.1523/jneurosci.1186-19.2020.