A disinhibitory circuit mechanism explains a general principle of peak performance during mid-level arousal

Proceedings of the National Academy of Sciences, Journal Year: 2024, Volume and Issue: 121(5)

Published: Jan. 26, 2024

Perceptual decision-making is highly dependent on the momentary arousal state of brain, which fluctuates over time a scale hours, minutes, and even seconds. The textbook relationship between task performance captured by an inverted U-shape, as put forward in Yerkes–Dodson law. This law suggests optimal at moderate levels impaired low or high levels. However, despite its popularity, evidence for this humans mixed best. Here, we use pupil-indexed data from various perceptual tasks to provide converging U-shaped spontaneous fluctuations across different decision types (discrimination, detection) sensory modalities (visual, auditory). To further understand relationship, built neurobiologically plausible mechanistic model show that it possible reproduce our findings incorporating two interneurons are both modulated signal. architecture produces dynamical regimes under influence arousal: one regime increases with another decreases arousal, together forming arousal–performance relationship. We conclude general robust property processing. It might be brought about act disinhibitory pathway neural populations encode available used decision.

Language: Английский

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Sensory processing in humans and mice fluctuates between external and internal modes

PLoS Biology, Journal Year: 2023, Volume and Issue: 21(12), P. e3002410 - e3002410

Published: Dec. 8, 2023

Perception is known to cycle through periods of enhanced and reduced sensitivity external information. Here, we asked whether such slow fluctuations arise as a noise-related epiphenomenon limited processing capacity or, alternatively, represent structured mechanism perceptual inference. Using 2 large-scale datasets, found that humans mice alternate between externally internally oriented modes sensory analysis. During mode, perception aligns more closely with the information, whereas internal mode characterized by biases toward history. Computational modeling indicated dynamic changes in are enabled interlinked factors: (i) integration subsequent inputs over time (ii) antiphase oscillations impact information versus predictions provided We propose between-mode generate unambiguous error signals enable optimal inference volatile environments.

Language: Английский

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Modulation of metastable ensemble dynamics explains optimal coding at moderate arousal in auditory cortex

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: April 5, 2024

Performance during perceptual decision-making exhibits an inverted-U relationship with arousal, but the underlying network mechanisms remain unclear. Here, we recorded from auditory cortex (A1) of behaving mice passive tone presentation, while tracking arousal via pupillometry. We found that discriminability in A1 ensembles was optimal at intermediate revealing a population-level neural correlate relationship. explained this arousal-dependent coding using spiking model clustered architecture. Specifically, show stimulus is achieved near transition between multi-attractor phase metastable cluster dynamics (low arousal) and single-attractor (high arousal). Additional signatures include arousal-induced reductions overall variability extent stimulus-induced quenching, which observed empirical data. Our results elucidate computational principles interactions pupil-linked sensory processing, variability, suggest role for transitions explaining nonlinear modulations cortical computations.

Language: Английский

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Distributed evidence accumulation across macaque large-scale neocortical networks during perceptual decision making

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Dec. 27, 2023

Despite the traditional view of parietal cortex as an important region for perceptual decision-making, recent evidence suggests that sensory accumulation occurs simultaneously across many cortical regions. We explored this hypothesis by integrating connectivity, cellular and receptor density datasets building a large-scale macaque model able to integrate conflicting signals perform decision-making task. Our results reveal supported distributed network temporal, frontal regions, with flexible sequential bottom-up or top-down modulation pathways depending on task difficulty. The replicates experimental lesioning effects reveals causal irrelevance areas like LIP decision performance is explained compensatory mechanisms within integration process. also reproduces observed temporal gating distractor timing during after Overall, our work hints at broad phenomenon, providing multiple testable predictions.

Language: Английский

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Strategic stabilization of arousal boosts sustained attention

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: March 6, 2022

Summary Changes in autonomic arousal, such as mounting sleep pressure, and changes motivation, fluctuating environmental reward statistics, both profoundly influence behavior. Our experience tells us that we have some capacity to control our arousal when doing so is important, staying awake while driving a motor vehicle. However, little known about how decision computations are jointly influenced by including whether animals, rodents, can adapt their state needs. Here, developed show results from an auditory feature-based sustained-attention task with intermittently shifting utility. We use pupil size estimate across wide range of states apply novel signal detection theoretic accumulation-to-bound modeling approaches large behavioral cohort. find pupil-linked utility major impacts on multiple aspects performance. Although substantial fluctuations persist conditions, mice partially stabilize near intermediate, optimal, level high. Behavioral analyses elements behavior improve during high influences some, but not all, them. Specifically, the likelihood timescale sensory evidence accumulation, quantity accumulated per time step attending. In sum, establish specific decision-computational signatures interaction, attention. So doing, provide experimental analysis framework for studying self-regulation neurotypical brains diseases attention-deficit/hyperactivity disorder.

Language: Английский

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Strategic stabilization of arousal boosts sustained attention

Current Biology, Journal Year: 2024, Volume and Issue: 34(18), P. 4114 - 4128.e6

Published: Aug. 15, 2024

Arousal and motivation interact to profoundly influence behavior. For example, experience tells us that we have some capacity control our arousal when appropriately motivated, such as staying awake while driving a motor vehicle. However, little is known about how jointly decision computations, including if animals, rodents, adapt their state needs. Here, developed show results from an auditory, feature-based, sustained-attention task with intermittently shifting utility. We use pupil size estimate across wide range of states apply tailored signal-detection theoretic, hazard function, accumulation-to-bound modeling approaches in large cohort mice. find pupil-linked utility both major impacts on multiple aspects performance. Although substantial fluctuations persist conditions, mice partially stabilize near intermediate optimal level high. Behavioral analyses elements behavior improve during high influences some, but not all, them. Specifically, the likelihood timescale sensory evidence accumulation quantity accumulated per time step attending. In sum, establish specific decision-computational signatures arousal, motivation, interaction attention. So doing, provide experimental analysis framework for studying self-regulation neurotypical brains diseases attention-deficit/hyperactivity disorder.

Language: Английский

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State modulation in spatial networks with three interneuron subtypes

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Aug. 24, 2024

Several inhibitory interneuron subtypes have been identified as critical in regulating sensory responses. However, the specific contribution of each subtype remains uncertain. In this work, we explore contributions cell-type activity and synaptic connections to dynamics a spatially organized spiking neuron network. We find that firing rates somatostatin (SOM) interneurons align closely with level network synchrony irrespective target modulatory input. Further analysis reveals inhibition from SOM parvalbumin (PV) must be limited allow gradual transitions asynchrony strength recurrent excitation onto neurons determines achievable Our results are consistent recent experimental findings on manipulations. Overall, our highlight common dynamic regimes achieved across modulations different cell populations identify cells main driver synchrony.

Language: Английский

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Strength of low-frequency EEG phase entrainment to external stimuli is associated with fluctuations in the brain’s internal state

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: May 23, 2024

Abstract The brain attends to environmental rhythms by aligning the phase of internal oscillations. However, factors underlying fluctuations in strength this entrainment remain largely unknown. In present study we examined whether low-frequency EEG rhythmic stimulus sequences varied with pupil size and posterior alpha-band power, thought reflect arousal level excitability cortical areas, respectively. We recorded scalp while participants carried out an intermodal selective attention task, which they were instructed attend a sequence visual or auditory stimuli ignore other perceptual modality. As expected, intertrial coherence (ITC), measure strength, was larger for task-relevant than task-irrelevant Across experiment, alpha power strongly linked each other. Interestingly, ITC tracked both variables: associated increase sequence, whereas decrease sequences. Exploratory analyses showed that temporal relation between emerged time periods around maxima minima. These results indicate endogenous sources contribute distinctly entrainment. Significance statement Fluctuations state powerfully shape perception external stimuli. Understanding physiological signatures is crucial understand how selectively switches content. Here studied two attentional state, pupil-linked band, activity Our reveal common dissociable influences these at slow scales. Furthermore, measuring including as covariates statistical models can help studies focusing on provides new evidence direct influence

Language: Английский

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