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      Global gain modulation generates time-dependent urgency during perceptual choice in humans

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      a , 1 , 2 , 1 , 1
      Nature Communications
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          Abstract

          Decision-makers must often balance the desire to accumulate information with the costs of protracted deliberation. Optimal, reward-maximizing decision-making can require dynamic adjustment of this speed/accuracy trade-off over the course of a single decision. However, it is unclear whether humans are capable of such time-dependent adjustments. Here, we identify several signatures of time-dependency in human perceptual decision-making and highlight their possible neural source. Behavioural and model-based analyses reveal that subjects respond to deadline-induced speed pressure by lowering their criterion on accumulated perceptual evidence as the deadline approaches. In the brain, this effect is reflected in evidence-independent urgency that pushes decision-related motor preparation signals closer to a fixed threshold. Moreover, we show that global modulation of neural gain, as indexed by task-related fluctuations in pupil diameter, is a plausible biophysical mechanism for the generation of this urgency. These findings establish context-sensitive time-dependency as a critical feature of human decision-making.

          Abstract

          Decision-making balances the benefits of additional information with the cost of time, but it is unclear whether humans adjust this balance within individual decisions. Here, authors show that we do make such adjustments to suit contextual demands and suggest that these are driven by modulation of neural gain.

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          Most cited references30

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          The time course of perceptual choice: the leaky, competing accumulator model.

          The time course of perceptual choice is discussed in a model of gradual, leaky, stochastic, and competitive information accumulation in nonlinear decision units. Special cases of the model match a classical diffusion process, but leakage and competition work together to address several challenges to existing diffusion, random walk, and accumulator models. The model accounts for data from choice tasks using both time-controlled (e.g., response signal) and standard reaction time paradigms and its adequacy compares favorably with other approaches. A new paradigm that controls the time of arrival of information supporting different choice alternatives provides further support. The model captures choice behavior regardless of the number of alternatives, accounting for the log-linear relation between reaction time and number of alternatives (Hick's law) and explains a complex pattern of visual and contextual priming in visual word identification.
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            Probabilistic decision making by slow reverberation in cortical circuits.

            Recent physiological studies of alert primates have revealed cortical neural correlates of key steps in a perceptual decision-making process. To elucidate synaptic mechanisms of decision making, I investigated a biophysically realistic cortical network model for a visual discrimination experiment. In the model, slow recurrent excitation and feedback inhibition produce attractor dynamics that amplify the difference between conflicting inputs and generates a binary choice. The model is shown to account for salient characteristics of the observed decision-correlated neural activity, as well as the animal's psychometric function and reaction times. These results suggest that recurrent excitation mediated by NMDA receptors provides a candidate cellular mechanism for the slow time integration of sensory stimuli and the formation of categorical choices in a decision-making neocortical network.
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              The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes.

              Through a widespread efferent projection system, the locus coeruleus-noradrenergic system supplies norepinephrine throughout the central nervous system. Initial studies provided critical insight into the basic organization and properties of this system. More recent work identifies a complicated array of behavioral and electrophysiological actions that have in common the facilitation of processing of relevant, or salient, information. This involves two basic levels of action. First, the system contributes to the initiation and maintenance of behavioral and forebrain neuronal activity states appropriate for the collection of sensory information (e.g. waking). Second, within the waking state, this system modulates the collection and processing of salient sensory information through a diversity of concentration-dependent actions within cortical and subcortical sensory, attention, and memory circuits. Norepinephrine-dependent modulation of long-term alterations in synaptic strength, gene transcription and other processes suggest a potentially critical role of this neurotransmitter system in experience-dependent alterations in neural function and behavior. The ability of a given stimulus to increase locus coeruleus discharge activity appears independent of affective valence (appetitive vs. aversive). Combined, these observations suggest that the locus coeruleus-noradrenergic system is a critical component of the neural architecture supporting interaction with, and navigation through, a complex world. These observations further suggest that dysregulation of locus coeruleus-noradrenergic neurotransmission may contribute to cognitive and/or arousal dysfunction associated with a variety of psychiatric disorders, including attention-deficit hyperactivity disorder, sleep and arousal disorders, as well as certain affective disorders, including post-traumatic stress disorder. Independent of an etiological role in these disorders, the locus coeruleus-noradrenergic system represents an appropriate target for pharmacological treatment of specific attention, memory and/or arousal dysfunction associated with a variety of behavioral/cognitive disorders.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                24 November 2016
                2016
                : 7
                : 13526
                Affiliations
                [1 ]Institute of Psychology and Leiden Institute for Brain and Cognition, Leiden University , 2333 AK Leiden, The Netherlands
                [2 ]Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf , 20246 Hamburg, Germany
                Author notes
                Author information
                http://orcid.org/0000-0003-1963-185X
                Article
                ncomms13526
                10.1038/ncomms13526
                5123079
                27882927
                4140f981-7761-46e2-a09b-77ef72f887bb
                Copyright © 2016, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 09 May 2016
                : 12 October 2016
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