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

2019 ◽  
Author(s):  
Y. Sela ◽  
AJ. Krom ◽  
L. Bergman ◽  
N. Regev ◽  
Y. Nir

AbstractA 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 (around 10%) 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 (>40ms) 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.Significance StatementReduced 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.

SLEEP ◽  
2021 ◽  
Vol 44 (Supplement_2) ◽  
pp. A45-A45
Author(s):  
Irma Gvilia ◽  
Sunil Kumar ◽  
Dennis McGinty ◽  
Ronald Szymusiak

Abstract Introduction We have previously shown that pharmacological elevation of corticotropin releasing factor (CRF) signaling in the brain results in exacerbation of sleep disturbances evoked by the exposure of rats to an acute stressor, the dirty cage of a male rat. In the present study we (1) assessed wake-sleep behavior of mice after the exposure to the dirty cage stress paradigm, and (2) examined the effect of chemogenetic silencing of CRF neurons in the hypothalamic paraventricular nucleus (PVN) on sleep occurring following the exposure to this stressor. Methods First, a group of mice (n=12) was implanted with EEG/EMG electrodes. In two weeks, post-surgery, six mice were transferred to dirty cages of male rats and recorded for 24 hours. Control mice were transferred to clean cages. In the second study, a group of CRF-ires-cre mice (n=8) received bilateral injections of AAV-hSyn-DIO-hM4Di-mCherry targeting the PVN. The other group of CRF-ires-cre mice (n=8) was injected AAV-hSyn-DIO-mCherry (control vector). All mice were implanted with EEG/EMG electrodes. Dirty cage experiments were started following a 4-week postsurgical period to allow gene recombination and expression. Mice were subjected to intraperitoneal (IP) administration of clozapine-n-oxide (CNO; 3 mg/kg) at ZT1, placed into dirty cages, and recorded for post-stress sleep. Results: Results In mice expressing hM4Di inhibitory DREADDs (designer receptors activated by designer drugs) versus mice injected with control AAV, IP CNO (3 mg/kg) resulted in a significant decrease of post-stress sleep onset latency, decrease of time spent in wakefulness (first hour, 74±5.3 vs. 89±11.0, second hour, 37.2±10.3% vs. 81.3±9.3%; third hour, 40.1±3.3% vs. 47.1±14.3%; fourth hour, 44.4±6.0 vs. 55.5±9.9), and increase in non-rapid eye movement (NREM) sleep time (26.0±5.4% vs. 11.0±11.1%; 62.8%±9.8 vs. 18.7 ± 9.6%; 59.9±3.2% vs. 52.9±14.5%; 55.6±6.2 vs. 44.5±10.0). The hM4Di expressing mice exhibited longer episodes of NREM sleep, compared to mice injected with control AAV (first hour, 133.3±80.1sec vs. 21±1.7sec; second hour, 43256±83.4sec vs. 73.5±44.1sec; third hour, 459.2±139.8sec vs. 139±80.6sec; fourth hour, 233.1±82.6sec vs. 190±72.3sec). Conclusion Chemogenetic silencing of CRF neurons in the PVN attenuates acute stress-induced sleep disturbance in mice. Support (if any) Supported by Department of Veterans Affairs Merit Review Grant # BX00155605 and SRNSF (Georgia) grant FR-18-12533


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Caroline A. Wilson ◽  
Sarah Fouda ◽  
Shuzo Sakata

Abstract Neuronal activity can modify Alzheimer’s disease pathology. Overexcitation of neurons can facilitate disease progression whereas the induction of cortical gamma oscillations can reduce amyloid load and improve cognitive functions in mouse models. Although previous studies have induced cortical gamma oscillations by either optogenetic activation of cortical parvalbumin-positive (PV+) neurons or sensory stimuli, it is still unclear whether other approaches to induce gamma oscillations can also be beneficial. Here we show that optogenetic activation of PV+ neurons in the basal forebrain (BF) increases amyloid burden, rather than reducing it. We applied 40 Hz optical stimulation in the BF by expressing channelrhodopsin-2 (ChR2) in PV+ neurons of 5xFAD mice. After 1-h induction of cortical gamma oscillations over three days, we observed the increase in the concentration of amyloid-β42 in the frontal cortical region, but not amyloid-β40. Amyloid plaques were accumulated more in the medial prefrontal cortex and the septal nuclei, both of which are targets of BF PV+ neurons. These results suggest that beneficial effects of cortical gamma oscillations on Alzheimer’s disease pathology can depend on the induction mechanisms of cortical gamma oscillations.


2016 ◽  
Vol 124 (4) ◽  
pp. 766-778 ◽  
Author(s):  
Catherine Elizabeth Warnaby ◽  
Marta Seretny ◽  
Roísín Ní Mhuircheartaigh ◽  
Richard Rogers ◽  
Saad Jbabdi ◽  
...  

Abstract Background It has been postulated that a small cortical region could be responsible for the loss of behavioral responsiveness (LOBR) during general anesthesia. The authors hypothesize that any brain region demonstrating reduced activation to multisensory external stimuli around LOBR represents a key cortical gate underlying this transition. Furthermore, the authors hypothesize that this localized suppression is associated with breakdown in frontoparietal communication. Methods During both simultaneous electroencephalography and functional magnetic resonance imaging (FMRI) and electroencephalography data acquisition, 15 healthy volunteers experienced an ultraslow induction with propofol anesthesia while a paradigm of multisensory stimulation (i.e., auditory tones, words, and noxious pain stimuli) was presented. The authors performed separate analyses to identify changes in (1) stimulus-evoked activity, (2) functional connectivity, and (3) frontoparietal synchrony associated with LOBR. Results By using an FMRI conjunction analysis, the authors demonstrated that stimulus-evoked activity was suppressed in the right dorsal anterior insula cortex (dAIC) to all sensory modalities around LOBR. Furthermore, the authors found that the dAIC had reduced functional connectivity with the frontoparietal regions, specifically the dorsolateral prefrontal cortex and inferior parietal lobule, after LOBR. Finally, reductions in the electroencephalography power synchrony between electrodes located in these frontoparietal regions were observed in the same subjects after LOBR. Conclusions The authors conclude that the dAIC is a potential cortical gate responsible for LOBR. Suppression of dAIC activity around LOBR was associated with disruption in the frontoparietal networks that was measurable using both electroencephalography synchrony and FMRI connectivity analyses.


2008 ◽  
Vol 100 (3) ◽  
pp. 1622-1634 ◽  
Author(s):  
Ling Qin ◽  
JingYu Wang ◽  
Yu Sato

Previous studies in anesthetized animals reported that the primary auditory cortex (A1) showed homogenous phasic responses to FM tones, namely a transient response to a particular instantaneous frequency when FM sweeps traversed a neuron's tone-evoked receptive field (TRF). Here, in awake cats, we report that A1 cells exhibit heterogeneous FM responses, consisting of three patterns. The first is continuous firing when a slow FM sweep traverses the receptive field of a cell with a sustained tonal response. The duration and amplitude of FM response decrease with increasing sweep speed. The second pattern is transient firing corresponding to the cell's phasic tonal response. This response could be evoked only by a fast FM sweep through the cell's TRF, suggesting a preference for fast FM. The third pattern was associated with the off response to pure tones and was composed of several discrete response peaks during slow FM stimulus. These peaks were not predictable from the cell's tonal response but reliably reflected the time when FM swept across specific frequencies. Our A1 samples often exhibited a complex response pattern, combining two or three of the basic patterns above, resulting in a heterogeneous response population. The diversity of FM responses suggests that A1 use multiple mechanisms to fully represent the whole range of FM parameters, including frequency extent, sweep speed, and direction.


2015 ◽  
Vol 113 (2) ◽  
pp. 475-486
Author(s):  
Melanie A. Kok ◽  
Daniel Stolzberg ◽  
Trecia A. Brown ◽  
Stephen G. Lomber

Current models of hierarchical processing in auditory cortex have been based principally on anatomical connectivity while functional interactions between individual regions have remained largely unexplored. Previous cortical deactivation studies in the cat have addressed functional reciprocal connectivity between primary auditory cortex (A1) and other hierarchically lower level fields. The present study sought to assess the functional contribution of inputs along multiple stages of the current hierarchical model to a higher order area, the dorsal zone (DZ) of auditory cortex, in the anaesthetized cat. Cryoloops were placed over A1 and posterior auditory field (PAF). Multiunit neuronal responses to noise burst and tonal stimuli were recorded in DZ during cortical deactivation of each field individually and in concert. Deactivation of A1 suppressed peak neuronal responses in DZ regardless of stimulus and resulted in increased minimum thresholds and reduced absolute bandwidths for tone frequency receptive fields in DZ. PAF deactivation had less robust effects on DZ firing rates and receptive fields compared with A1 deactivation, and combined A1/PAF cooling was largely driven by the effects of A1 deactivation at the population level. These results provide physiological support for the current anatomically based model of both serial and parallel processing schemes in auditory cortical hierarchical organization.


2008 ◽  
Vol 99 (4) ◽  
pp. 1616-1627 ◽  
Author(s):  
Ben Scholl ◽  
Xiang Gao ◽  
Michael Wehr

Responses of cortical neurons to sensory stimuli within their receptive fields can be profoundly altered by the stimulus context. In visual and somatosensory cortex, contextual interactions have been shown to change sign from facilitation to suppression depending on stimulus strength. Contextual modulation of high-contrast stimuli tends to be suppressive, but for low-contrast stimuli tends to be facilitative. This trade-off may optimize contextual integration by cortical cells and has been suggested to be a general feature of cortical processing, but it remains unknown whether a similar phenomenon occurs in auditory cortex. Here we used whole cell and single-unit recordings to investigate how contextual interactions in auditory cortical neurons depend on the relative intensity of masker and probe stimuli in a two-tone stimulus paradigm. We tested the hypothesis that relatively low-level probes should show facilitation, whereas relatively high-level probes should show suppression. We found that contextual interactions were primarily suppressive across all probe levels, and that relatively low-level probes were subject to stronger suppression than high-level probes. These results were virtually identical for spiking and subthreshold responses. This suggests that, unlike visual cortical neurons, auditory cortical neurons show maximal suppression rather than facilitation for relatively weak stimuli.


2015 ◽  
Vol 6 (1) ◽  
Author(s):  
Anna Grosso ◽  
Marco Cambiaghi ◽  
Annamaria Renna ◽  
Luisella Milano ◽  
Giorgio Roberto Merlo ◽  
...  

2009 ◽  
Vol 102 (6) ◽  
pp. 3329-3339 ◽  
Author(s):  
Nima Mesgarani ◽  
Stephen V. David ◽  
Jonathan B. Fritz ◽  
Shihab A. Shamma

Population responses of cortical neurons encode considerable details about sensory stimuli, and the encoded information is likely to change with stimulus context and behavioral conditions. The details of encoding are difficult to discern across large sets of single neuron data because of the complexity of naturally occurring stimulus features and cortical receptive fields. To overcome this problem, we used the method of stimulus reconstruction to study how complex sounds are encoded in primary auditory cortex (AI). This method uses a linear spectro-temporal model to map neural population responses to an estimate of the stimulus spectrogram, thereby enabling a direct comparison between the original stimulus and its reconstruction. By assessing the fidelity of such reconstructions from responses to modulated noise stimuli, we estimated the range over which AI neurons can faithfully encode spectro-temporal features. For stimuli containing statistical regularities (typical of those found in complex natural sounds), we found that knowledge of these regularities substantially improves reconstruction accuracy over reconstructions that do not take advantage of this prior knowledge. Finally, contrasting stimulus reconstructions under different behavioral states showed a novel view of the rapid changes in spectro-temporal response properties induced by attentional and motivational state.


2004 ◽  
Vol 92 (4) ◽  
pp. 2520-2529 ◽  
Author(s):  
Yoriko Takikawa ◽  
Reiko Kawagoe ◽  
Okihide Hikosaka

Dopamine (DA) neurons respond to sensory stimuli that predict reward. To understand how DA neurons acquire such ability, we trained monkeys on a one-direction-rewarded version of memory-guided saccade task (1DR) only when we recorded from single DA neurons. In 1DR, position-reward mapping was changed across blocks of trials. In the early stage of training of 1DR, DA neurons responded to reward delivery; in the later stages, they responded predominantly to the visual cue that predicted reward or no reward (reward predictor) differentially. We found that such a shift of activity from reward to reward predictor also occurred within a block of trials after position-reward mapping was altered. A main effect of long-term training was to accelerate the within-block reward-to-predictor shift of DA neuronal responses. The within-block shift appeared first in the intermediate stage, but was slow, and DA neurons often responded to the cue that indicated reward in the preceding block. In the advanced stage, the reward-to-predictor shift occurred quickly such that the DA neurons' responses to visual cues faithfully matched the current position-reward mapping. Changes in the DA neuronal responses co-varied with the reward-predictive differentiation of saccade latency both in short-term (within-block) and long-term adaptation. DA neurons' response to the fixation point also underwent long-term changes until it occurred predominantly in the first trial within a block. This might trigger a switch between the learned sets. These results suggest that midbrain DA neurons play an essential role in adapting oculomotor behavior to frequent switches in position-reward mapping.


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