Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

eLife, Год журнала: 2022, Номер 11

Опубликована: Фев. 8, 2022

Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing. Yet, how arousal signals influence population activity detail has so far only been characterized a few selected brain regions. Traditional accounts conceptualize as homogeneous modulator of neural across the cerebral cortex. Recent insights, however, point to higher specificity effects on different components and Here, we provide comprehensive account relationships between fluctuations neuronal human brain. Exploiting established link pupil size central performed concurrent magnetoencephalographic (MEG) pupillographic recordings large number participants, pooled three laboratories. We found cascade relative peak timing spontaneous dilations: Decreases low-frequency (2–8 Hz) temporal lateral frontal cortex, followed increased high-frequency (>64 mid-frontal regions, monotonic inverted U intermediate frequency-range (8–32 occipito-parietal Pupil-linked also coincided widespread changes structure aperiodic component activity, indicative excitation-inhibition balance underlying microcircuits. Our results novel basis studying modulation cognitive computations circuits.

Язык: Английский

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Continuity fields enhance visual perception through positive serial dependence

Nature Reviews Psychology, Год журнала: 2024, Номер 3(5), С. 352 - 366

Опубликована: Апрель 8, 2024

Язык: Английский

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Neurobehavioral meaning of pupil size

Neuron, Год журнала: 2024, Номер 112(20), С. 3381 - 3395

Опубликована: Июнь 25, 2024

Pupil size is a widely used metric of brain state. It one the few signals originating from that can be readily monitored with low-cost devices in basic science, clinical, and home settings. is, therefore, important to investigate generate well-defined theories related specific interpretations this metric. What exactly does it tell us about brain? Pupils constrict response light dilate during darkness, but also controls pupil irrespective luminosity. fluctuations resulting ongoing "brain states" are as arousal, what pupil-linked arousal how should interpreted neural, cognitive, computational terms? Here, we discuss some recent findings these issues. We identify open questions propose answer them through combination tasks, neurocomputational models, neurophysiological probing interconnected loops causes consequences size.

Язык: Английский

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Adaptive History Biases Result from Confidence-Weighted Accumulation of past Choices

Journal of Neuroscience, Год журнала: 2018, Номер 38(10), С. 2418 - 2429

Опубликована: Янв. 25, 2018

Perceptual decision-making is biased by previous events, including the history of preceding choices: observers tend to repeat (or alternate) their judgments sensory environment more often than expected chance. Computational models postulate that these so-called choice biases result from accumulation internal decision signals across trials. Here, we provide psychophysical evidence for such a mechanism and its adaptive utility. Male female human performed different variants challenging visual motion discrimination task near threshold. In first experiment, decoupled categorical perceptual choices motor responses on trial-by-trial basis. Choice bias was explained choices, not responses, highlighting importance in action-independent formats. second stimulus environments containing levels autocorrelation providing no external feedback about correctness. Despite performing under overall high uncertainty, adjusted both strength sign environments. When sequences were dominated either repetitions or alternations, individual degree this adjustment as good predictor performance sensitivity. The scaled with two proxies observers' confidence (accuracy reaction time). Together, our results are consistent idea action-independent, confidence-modulated variables accumulated flexible manner depends decision-makers' model environment. SIGNIFICANCE STATEMENT Decisions based input influenced one's manifesting systematically choices. We here support arise context-dependent quantity referred variable: variable's dictates magnitude show an format manner, weighted This confidence-weighted enables decision-makers flexibly adjust behavior can be important optimizing sensitivity momentary input.

Язык: Английский

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Confirmation Bias through Selective Overweighting of Choice-Consistent Evidence

Current Biology, Год журнала: 2018, Номер 28(19), С. 3128 - 3135.e8

Опубликована: Сен. 13, 2018

People's assessments of the state world often deviate systematically from information available to them [1Tversky A. Kahneman D. Judgment under Uncertainty: Heuristics and Biases.Science. 1974; 185: 1124-1131Crossref PubMed Scopus (19190) Google Scholar]. Such biases can originate people's own decisions: committing a categorical proposition, or course action, subsequent judgment decision-making. This phenomenon, called confirmation bias [2Nickerson R.S. Confirmation bias: A ubiquitous phenomenon in many guises.Rev. Gen. Psychol. 1998; 2: 175-220Crossref (3702) Scholar], has been explained as suppression post-decisional dissonance [3Festinger L. theory cognitive dissonance. Stanford University Press, Stanford1957Crossref Scholar, 4Brehm J.W. Postdecision changes desirability alternatives.J. Abnorm. 1956; 52: 384-389Crossref (704) Here, we provide insights into underlying mechanism. It is commonly held that decisions result accumulation samples evidence informing about [5Gold J.I. Shadlen M.N. The neural basis decision making.Annu. Rev. Neurosci. 2007; 30: 535-574Crossref (2264) 6Bogacz R. Brown E. Moehlis J. Holmes P. Cohen J.D. physics optimal making: formal analysis models performance two-alternative forced-choice tasks.Psychol. 2006; 113: 700-765Crossref (1146) 7Liu F. Wang X.-J. common cortical circuit mechanism for perceptual discrimination veridical judgment.PLoS Comput. Biol. 2008; 4: e1000253Crossref (23) 8Wang Decision making recurrent neuronal circuits.Neuron. 60: 215-234Abstract Full Text PDF (424) We hypothesized choices process by selectively altering weighting (gain) evidence, akin selective attention. developed novel psychophysical task test this idea. Participants viewed two successive random dot motion stimuli made motion-direction judgments: after first stimulus continuous estimation overall direction across both second stimulus. Participants' sensitivity was enhanced when consistent with initial choice (compared both, choice-inconsistent stimuli). model entailing choice-dependent gain modulation effect better than several alternative mechanisms. Choice-dependent also established another averaging numerical values instead directions. conclude intermittent direct attention during evaluation possibly due decision-related feedback brain [9Wimmer K. Compte Roxin Peixoto Renart de la Rocha Sensory integration dynamics hierarchical network explains probabilities area MT.Nat. Commun. 2015; 6: 6177Crossref (88) Our results point interplay between decision-making

Язык: Английский

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The Confidence Database

Nature Human Behaviour, Год журнала: 2020, Номер 4(3), С. 317 - 325

Опубликована: Фев. 3, 2020

Язык: Английский

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Slow Drift of Neural Activity as a Signature of Impulsivity in Macaque Visual and Prefrontal Cortex

Neuron, Год журнала: 2020, Номер 108(3), С. 551 - 567.e8

Опубликована: Авг. 17, 2020

Язык: Английский

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Phasic Activation of Dorsal Raphe Serotonergic Neurons Increases Pupil Size

Current Biology, Год журнала: 2020, Номер 31(1), С. 192 - 197.e4

Опубликована: Ноя. 12, 2020

Transient variations in pupil size (PS) under constant luminance are coupled to rapid changes arousal state,1Reimer J. Froudarakis E. Cadwell C.R. Yatsenko D. Denfield G.H. Tolias A.S. Pupil fluctuations track fast switching of cortical states during quiet wakefulness.Neuron. 2014; 84: 355-362Abstract Full Text PDF PubMed Scopus (275) Google Scholar, 2McGinley M.J. David S.V. McCormick D.A. Cortical membrane potential signature optimal for sensory signal detection.Neuron. 2015; 87: 179-192Abstract (280) 3de Gee J.W. Colizoli O. Kloosterman N.A. Knapen T. Nieuwenhuis S. Donner T.H. Dynamic modulation decision biases by brainstem systems.eLife. 2017; 6: e23232Crossref (89) Scholar which have been interpreted as vigilance,4Yüzgeç Ö. Prsa M. Zimmermann R. Huber Size Coupling States Protects the Stability Deep Sleep via Parasympathetic Modulation.Curr. Biol. 2018; 28: 392-400.e3Abstract (35) salience,5Wang C.-A. Munoz D.P. A circuit orienting responses: implications cognitive size.Curr. Opin. Neurobiol. 33: 134-140Crossref (129) or a surprise signal.6Preuschoff K. 't Hart B.M. Einhäuser W. Dilation Signals Surprise: Evidence Noradrenaline's Role Decision Making.Front. Neurosci. 2011; 5: 115Crossref (226) 7Kloosterman Meindertsma van Loon A.M. Lamme V.A.F. Bonneh Y.S. tracks perceptual content and surprise.Eur. 41: 1068-1078Crossref (70) 8de Correa C. Weaver Gaal dilation P3 reflect subjective about outcome.bioRxiv. 2020; https://doi.org/10.1101/2020.06.25.164962Crossref (0) Neural control such presumably involves multiple brain regions5Wang Scholar,9Joshi Li Y. Kalwani R.M. Gold J.I. Relationships between Diameter Neuronal Activity Locus Coeruleus, Colliculi, Cingulate Cortex.Neuron. 2016; 89: 221-234Abstract (456) 10Nelson A. Mooney The Basal Forebrain Motor Cortex Provide Convergent yet Distinct Movement-Related Inputs Auditory 90: 635-648Abstract (68) 11Ebitz R.B. Platt M.L. activity primate dorsal anterior cingulate cortex signals task conflict predicts adjustments pupil-linked arousal.Neuron. 85: 628-640Abstract (101) neuromodulatory systems,3de Scholar,12Reimer McGinley Liu Rodenkirch Wang Q. adrenergic cholinergic cortex.Nat. Commun. 7: 13289Crossref (249) Scholar,13Joshi Window on Substrates Cognition.Trends Cogn. Sci. 24: 466-480Abstract (32) but it is often associated with phasic noradrenergic system.9Joshi Scholar,14Breton-Provencher V. Sur Active locus coeruleus GABAergic circuit.Nat. 2019; 22: 218-228Crossref (61) Scholar,15Aston-Jones G. Cohen J.D. An integrative theory coeruleus-norepinephrine function: adaptive gain performance.Annu. Rev. 2005; 403-450Crossref (2202) Serotonin (5-HT), neuromodulator also implicated aspects arousal16Frazer Hensler J.G. Involvement Physiological Function Behavior.in: Siegel G.J. Agranoff B.W. Albers R.W. Basic Neurochemistry: Molecular, cellular Medical Aspects. Lippincott-Raven, 1999: 264-268Google sleep-wake transitions,17Brown R.E. Basheer McKenna J.T. Strecker McCarley Control sleep wakefulness.Physiol. 2012; 92: 1087-1187Crossref (685) motivational state regulation,18Meyniel F. Goodwin G.M. Deakin Klinge MacFadyen Milligan H. Mullings Pessiglione Gaillard specific role serotonin overcoming effort cost.eLife. e17282Crossref (40) signaling unexpected events,19Matias Lottem Dugué G.P. Mainen Z.F. patterns neurons underlying flexibility.eLife. e20552Crossref (74) seems affect PS,20Prow M.R. Martin K.F. Heal D.J. 8-OH-DPAT-induced mydriasis mice: pharmacological characterisation.Eur. Pharmacol. 1996; 317: 21-28Crossref (22) 21Vitiello B. Hill Mack Molchan Martinez Murphy D.L. Sunderland Cognitive behavioral effects cholinergic, dopaminergic, serotonergic blockade humans.Neuropsychopharmacol. 1997; 16: 15-24Crossref (85) 22Schmid Enzler Gasser P. Grouzmann Preller K.H. Vollenweider F.X. Brenneisen Müller Borgwardt Liechti M.E. Acute Effects Lysergic Acid Diethylamide Healthy Subjects.Biol. Psychiatry. 78: 544-553Abstract (159) 23Weinberg-Wolf Fagan Anderson Tringides Dal Monte Chang S.W.C. 5-hydroxytryptophan attention central neurochemistry rhesus macaque.Neuropsychopharmacol. 43: 1589-1598Crossref (11) 24Yu Ramage A.G. Koss M.C. Pharmacological studies pupillary anesthetized rats.Eur. 2004; 489: 207-213Crossref (24) these not investigated detail. Here we show that 5-HT neuron stimulation causes transient PS changes. We used optogenetic activation raphe nucleus (DRN) head-fixed mice performing foraging task. 5-HT-driven modulations were maintained throughout photostimulation period sustained few seconds after end stimulation. found no evidence increase resulted from interactions variables, locomotion licking. Furthermore, observed effect depended level environmental uncertainty, consistent idea could report signal.19Matias These results advance our understanding PS, revealing tight relationship PS.

Язык: Английский

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Arousal-related adjustments of perceptual biases optimize perception in dynamic environments

Nature Human Behaviour, Год журнала: 2017, Номер 1(6)

Опубликована: Май 5, 2017

Язык: Английский

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A new comprehensive eye-tracking test battery concurrently evaluating the Pupil Labs glasses and the EyeLink 1000

PeerJ, Год журнала: 2019, Номер 7, С. e7086 - e7086

Опубликована: Июль 9, 2019

Eye-tracking experiments rely heavily on good data quality of eye-trackers. Unfortunately, it is often the case that only spatial accuracy and precision values are available from manufacturers. These two alone not sufficient to serve as a benchmark for an eye-tracker: deteriorates during experimental session due head movements, changing illumination or calibration decay. Additionally, different paradigms require analysis types eye movements; instance, smooth pursuit blinks microsaccades, which themselves cannot readily be evaluated by using alone. To obtain more comprehensive description properties, we developed extensive eye-tracking test battery. In 10 tasks, related measures such as: decay accuracy, fixation durations, pupil dilation, movement, microsaccade classification, blink influence motion. For some measures, true theoretical exist. others, relative comparison reference eye-tracker needed. Therefore, collected our gaze simultaneously remote EyeLink 1000 compared with mobile Pupil Labs glasses. As expected, average 0.57° was better than 0.82° glasses (N = 15). Furthermore, classified less fixations shorter saccade durations Similarly, found fewer microsaccades The over time decayed slightly 1000, but strongly Finally, observed measured diameters differed between eye-trackers individual subject level group level. conclude, battery offers tasks allow us many parameters interest in stereotypical situations addresses common source confounds measurement errors (e.g., yaw roll movements). All recorded (including Labs' videos), stimulus code battery, modular pipeline freely (https://github.com/behinger/etcomp).

Язык: Английский

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