Pupillary Dynamics Reflect the Impact of Temporal Expectation on Detection Strategy

Overview

Journal iScience

Publisher Cell Press

Date 2023 Feb 17

PMID 36798438

Authors

Jennifer Lawlor

Agnes Zagala

Sara Jamali

Yves Boubenec

Affiliations

Soon will be listed here.

Abstract

Everyday life's perceptual decision-making is informed by experience. In particular, temporal expectation can ease the detection of relevant events in noisy sensory streams. Here, we investigated if humans can extract hidden temporal cues from the occurrences of probabilistic targets and utilize them to inform target detection in a complex acoustic stream. To understand what neural mechanisms implement temporal expectation influence on decision-making, we used pupillometry as a proxy for underlying neuromodulatory activity. We found that participants' detection strategy was influenced by the hidden temporal context and correlated with sound-evoked pupil dilation. A model of urgency fitted on false alarms predicted detection reaction time. Altogether, these findings suggest that temporal expectation informs decision-making and could be implemented through neuromodulatory-mediated urgency signals.

Citing Articles

Pupillary responses to directional uncertainty while intercepting a moving target.

Marquez I, Trevino M R Soc Open Sci. 2024; 11(10):240606.

PMID: 39359460 PMC: 11444787. DOI: 10.1098/rsos.240606.

References

Thomaschke R, Wagener A, Kiesel A, Hoffmann J . The scope and precision of specific temporal expectancy: evidence from a variable foreperiod paradigm. Atten Percept Psychophys. 2011; 73(3):953-64. DOI: 10.3758/s13414-010-0079-1. View

Guo W, Robert B, Polley D . The Cholinergic Basal Forebrain Links Auditory Stimuli with Delayed Reinforcement to Support Learning. Neuron. 2019; 103(6):1164-1177.e6. PMC: 7927272. DOI: 10.1016/j.neuron.2019.06.024. View

Lakatos P, Musacchia G, OConnel M, Falchier A, Javitt D, Schroeder C . The spectrotemporal filter mechanism of auditory selective attention. Neuron. 2013; 77(4):750-61. PMC: 3583016. DOI: 10.1016/j.neuron.2012.11.034. View

Ossmy O, Moran R, Pfeffer T, Tsetsos K, Usher M, Donner T . The timescale of perceptual evidence integration can be adapted to the environment. Curr Biol. 2013; 23(11):981-6. DOI: 10.1016/j.cub.2013.04.039. View

Thura D, Cisek P . The Basal Ganglia Do Not Select Reach Targets but Control the Urgency of Commitment. Neuron. 2017; 95(5):1160-1170.e5. DOI: 10.1016/j.neuron.2017.07.039. View

Keung W, Hagen T, Wilson R . Regulation of evidence accumulation by pupil-linked arousal processes. Nat Hum Behav. 2019; 3(6):636-645. DOI: 10.1038/s41562-019-0551-4. View

Boubenec Y, Lawlor J, Gorska U, Shamma S, Englitz B . Detecting changes in dynamic and complex acoustic environments. Elife. 2017; 6. PMC: 5367897. DOI: 10.7554/eLife.24910. View

Steinemann N, OConnell R, Kelly S . Decisions are expedited through multiple neural adjustments spanning the sensorimotor hierarchy. Nat Commun. 2018; 9(1):3627. PMC: 6128824. DOI: 10.1038/s41467-018-06117-0. View

Murphy P, Vandekerckhove J, Nieuwenhuis S . Pupil-linked arousal determines variability in perceptual decision making. PLoS Comput Biol. 2014; 10(9):e1003854. PMC: 4168983. DOI: 10.1371/journal.pcbi.1003854. View

10.

Devine C, Gaffney C, Loughnane G, Kelly S, OConnell R . The role of premature evidence accumulation in making difficult perceptual decisions under temporal uncertainty. Elife. 2019; 8. PMC: 6904213. DOI: 10.7554/eLife.48526. View

11.

Yau Y, Hinault T, Taylor M, Cisek P, Fellows L, Dagher A . Evidence and Urgency Related EEG Signals during Dynamic Decision-Making in Humans. J Neurosci. 2021; 41(26):5711-5722. PMC: 8244970. DOI: 10.1523/JNEUROSCI.2551-20.2021. View

12.

de Gee J, Tsetsos K, Schwabe L, Urai A, McCormick D, McGinley M . Pupil-linked phasic arousal predicts a reduction of choice bias across species and decision domains. Elife. 2020; 9. PMC: 7297536. DOI: 10.7554/eLife.54014. View

13.

Murphy P, Boonstra E, Nieuwenhuis S . Global gain modulation generates time-dependent urgency during perceptual choice in humans. Nat Commun. 2016; 7:13526. PMC: 5123079. DOI: 10.1038/ncomms13526. View

14.

Jacob S, Nienborg H . Monoaminergic Neuromodulation of Sensory Processing. Front Neural Circuits. 2018; 12:51. PMC: 6048220. DOI: 10.3389/fncir.2018.00051. View

15.

Wang C, Munoz D . Coordination of Pupil and Saccade Responses by the Superior Colliculus. J Cogn Neurosci. 2021; 33(5):919-932. DOI: 10.1162/jocn_a_01688. View

16.

McDermott J, Simoncelli E . Sound texture perception via statistics of the auditory periphery: evidence from sound synthesis. Neuron. 2011; 71(5):926-40. PMC: 4143345. DOI: 10.1016/j.neuron.2011.06.032. View

17.

Thura D, Beauregard-Racine J, Fradet C, Cisek P . Decision making by urgency gating: theory and experimental support. J Neurophysiol. 2012; 108(11):2912-30. DOI: 10.1152/jn.01071.2011. View

18.

Thiele A, Bellgrove M . Neuromodulation of Attention. Neuron. 2018; 97(4):769-785. PMC: 6204752. DOI: 10.1016/j.neuron.2018.01.008. View

19.

Cazettes F, Reato D, P Morais J, Renart A, Mainen Z . Phasic Activation of Dorsal Raphe Serotonergic Neurons Increases Pupil Size. Curr Biol. 2020; 31(1):192-197.e4. PMC: 7808753. DOI: 10.1016/j.cub.2020.09.090. View

20.

Preuschoff K, Hart B, Einhauser W . Pupil Dilation Signals Surprise: Evidence for Noradrenaline's Role in Decision Making. Front Neurosci. 2011; 5:115. PMC: 3183372. DOI: 10.3389/fnins.2011.00115. View