Arousal and locomotion make distinct contributions to cortical activity patterns and visual encoding

Vinck, Martin; Batista-Brito, Renata; Knoblich, Ulf; Cardin, Jessica A.

doi:10.1101/010751

Cited by 156 publications

(328 citation statements)

References 61 publications

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“…TDW/LMA uncoupling is consistent with rat studies showing that prominent hippocampal θ typically accompanies vigorous locomotion but can exist in the resting animal preceding or following a running bout (34,38) or under high motivational drive (29). Thus, TDW can occur in the absence of LMA, and LMA in the absence of TDW also likely occurs, as automatic locomotor activity such as wheel running was found to be associated with reduced cortical firing rates compared with exploration (39).…”

Section: Hcrt Is An Essential Regulator Of the Eeg Determinants Of Spsupporting

confidence: 63%

Hypocretin (orexin) is critical in sustaining theta/gamma-rich waking behaviors that drive sleep need

Vassalli

Franken

2017

Proc. Natl. Acad. Sci. U.S.A.

121

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Hcrt gene inactivation in mice leads to behavioral state instability, abnormal transitions to paradoxical sleep, and cataplexy, hallmarks of narcolepsy. Sleep homeostasis is, however, considered unimpaired in patients and narcoleptic mice. We find that whereas Hcrt ko/ko mice respond to 6-h sleep deprivation (SD) with a slowwave sleep (SWS) EEG δ (1.0 to 4.0 Hz) power rebound like WT littermates, spontaneous waking fails to induce a δ power reflecting prior waking duration. This correlates with impaired θ (6.0 to 9.5 Hz) and fast-γ (55 to 80 Hz) activity in prior waking. We algorithmically identify a theta-dominated wakefulness (TDW) substate underlying motivated behaviors and typically preceding cataplexy in Hcrt ko/ko mice. Hcrt ko/ko mice fully implement TDW when waking is enforced, but spontaneous TDW episode duration is greatly reduced. A reformulation of the classic sleep homeostasis model, where homeostatic pressure rises exclusively in TDW rather than all waking, predicts δ power dynamics both in Hcrt ko/ko and WT mouse baseline and recovery SWS. The low homeostatic impact of Hcrt ko/ko mouse spontaneous waking correlates with decreased cortical expression of neuronal activityrelated genes (notably Bdnf, Egr1/Zif268, and Per2). Thus, spontaneous TDW stability relies on Hcrt to sustain θ/fast-γ network activity and associated plasticity, whereas other arousal circuits sustain TDW during SD. We propose that TDW identifies a discrete global brain activity mode that is regulated by contextdependent neuromodulators and acts as a major driver of sleep homeostasis. Hcrt loss in Hcrt ko/ko mice causes impaired TDW maintenance in baseline wake and blunted δ power in SWS, reproducing, respectively, narcolepsy excessive daytime sleepiness and poor sleep quality.hypocretin/orexin | narcolepsy | sleep homeostasis | brain theta oscillations | waking substate W akefulness encompasses a wide spectrum of arousal levels, sensorimotor processing modes, and behaviors, reflected in the electroencephalogram (EEG) by a great variety of signal patterns (1). Fourier transform decomposes the signal into multiple frequency ranges, defining δ, θ (5 to 10 Hz), and γ (>30 Hz) oscillatory components. However, although the EEG has been used to define wakefulness and distinguish it from slow-wave and paradoxical sleep (SWS and PS) for decades, a formal cartography of waking substates, associated EEG features, and their significance for the animal is largely lacking. Likewise, definition of the relation between waking quality and subsequent sleep content has evolved little since enunciation of the twoprocess model of sleep regulation (2) in which a sleep/wakedependent homeostatic "process S," reflected in EEG δ power during SWS, regulates sleep propensity as a function of prior waking duration regardless of waking quality. Later studies described behaviors (3, 4) or EEG components (5, 6) that disproportionally affect the sleep homeostat. Different procedural, cognitive, or emotional experience differentially impacts subsequent SWS δ powe...

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Section: Hcrt Is An Essential Regulator Of the Eeg Determinants Of Spsupporting

confidence: 63%

Hypocretin (orexin) is critical in sustaining theta/gamma-rich waking behaviors that drive sleep need

Vassalli

Franken

2017

Proc. Natl. Acad. Sci. U.S.A.

121

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“…In our visual spatial task, monocular detection was more difficult than binocular detection, and this may have accentuated the effects of cortical state (Chen et al, 2008;McGinley et al, 2015;Spitzer et al, 1988). Our study isolated the effects of cortical state on perception in stationary conditions, minimizing complicated interactions between arousal, visual motion, and locomotion (Niell and Stryker, 2010;Poort et al, 2015;Saleem et al, 2013;Vaiceliunaite et al, 2013;Vinck et al, 2015). Understanding the effects of cortical states on perception across modalities, during a variety of behavioral contexts, remains an important topic for future study.…”

Section: Discussionmentioning

confidence: 99%

Cortical states control visual spatial perception

Speed

Rosario

Burgess

et al. 2018

Preprint

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SummaryMany factors modulate the state of cortical activity, but the importance of cortical states for sensory perception remains debated.We trained mice to detect spatially localized visual stimuli, and simultaneously measured local field potentials and excitatory and inhibitory neuron populations across layers of primary visual cortex (V1). Cortical states with low firing rates and correlations between excitatory neurons, and reduced oscillatory activity in Layer 4, accurately predicted single trials of visual spatial detection behavior. Our results show that cortical states exert strong effects at the initial stage of cortical processing in V1, and play a decisive role for visual spatial behavior in mice.

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“…However, some of these experiments were performed with anesthetized animals. One should be careful about comparing these results with those from human neuroimaging and psychophysics because responses of neurons in visual cortex depend on brain state (84)(85)(86). The dynamics of our model depend on multiple factors, stimulus strength, attentional modulation, and mutual inhibition (Fig.…”

Section: Discussionmentioning

confidence: 99%

Attention model of binocular rivalry

Rankin

Rinzel

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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When the corresponding retinal locations in the two eyes are presented with incompatible images, a stable percept gives way to perceptual alternations in which the two images compete for perceptual dominance. As perceptual experience evolves dynamically under constant external inputs, binocular rivalry has been used for studying intrinsic cortical computations and for understanding how the brain regulates competing inputs. Converging behavioral and EEG results have shown that binocular rivalry and attention are intertwined: binocular rivalry ceases when attention is diverted away from the rivalry stimuli. In addition, the competing image in one eye suppresses the target in the other eye through a pattern of gain changes similar to those induced by attention. These results require a revision of the current computational theories of binocular rivalry, in which the role of attention is ignored. Here, we provide a computational model of binocular rivalry. In the model, competition between two images in rivalry is driven by both attentional modulation and mutual inhibition, which have distinct selectivity (feature vs. eye of origin) and dynamics (relatively slow vs. relatively fast). The proposed model explains a wide range of phenomena reported in rivalry, including the three hallmarks: (i) binocular rivalry requires attention; (ii) various perceptual states emerge when the two images are swapped between the eyes multiple times per second; (iii) the dominance duration as a function of input strength follows Levelt's propositions. With a bifurcation analysis, we identified the parameter space in which the model's behavior was consistent with experimental results.B inocular rivalry is a visual phenomenon in which perception alternates between incompatible monocular images presented to the two eyes. During binocular rivalry, perceptual experience evolves dynamically while the external inputs are held constant. Binocular rivalry thereby provides an opportunity to gain insights about the intrinsic cortical computations underlying visual perception (1, 2).In conventional models of binocular rivalry, the competition between two percepts has been characterized as mutual inhibition between two populations of neurons selective for each of the two stimuli (3-11). Notwithstanding the differences in their details, these models consider the neural processing underlying binocular rivalry to be an automatic process. These models predict, therefore, that the dynamics of binocular rivalry are influenced mainly by bottom-up sensory inputs.Converging experimental evidence has shown, however, that binocular rivalry also depends on attention (for a review, see ref.12). First, EEG has been used to measure a neural correlate of the perceptual alternations during binocular rivalry when observers pay attention to the rival stimuli (13). However, this rivalry-induced modulation of the EEG signal is largely or entirely eliminated when attention is diverted away from the stimuli (14). Second, behavioral experiments comparing the perceptual cons...

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Arousal and locomotion make distinct contributions to cortical activity patterns and visual encoding

Cited by 156 publications

References 61 publications

Hypocretin (orexin) is critical in sustaining theta/gamma-rich waking behaviors that drive sleep need

Hypocretin (orexin) is critical in sustaining theta/gamma-rich waking behaviors that drive sleep need

Cortical states control visual spatial perception

Attention model of binocular rivalry

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