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Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed

The survival of animals depends critically on prioritizing responses to motivationally salient stimuli. While it is generally believed that motivational salience increases decision speed, the quantitative relationship between motivational salience and decision speed, measured by reaction time (RT),...

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Autores principales: Avila, Irene, Lin, Shih-Chieh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3958335/
https://www.ncbi.nlm.nih.gov/pubmed/24642480
http://dx.doi.org/10.1371/journal.pbio.1001811
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author Avila, Irene
Lin, Shih-Chieh
author_facet Avila, Irene
Lin, Shih-Chieh
author_sort Avila, Irene
collection PubMed
description The survival of animals depends critically on prioritizing responses to motivationally salient stimuli. While it is generally believed that motivational salience increases decision speed, the quantitative relationship between motivational salience and decision speed, measured by reaction time (RT), remains unclear. Here we show that the neural correlate of motivational salience in the basal forebrain (BF), defined independently of RT, is coupled with faster and also more precise decision speed. In rats performing a reward-biased simple RT task, motivational salience was encoded by BF bursting response that occurred before RT. We found that faster RTs were tightly coupled with stronger BF motivational salience signals. Furthermore, the fraction of RT variability reflecting the contribution of intrinsic noise in the decision-making process was actively suppressed in faster RT distributions with stronger BF motivational salience signals. Artificially augmenting the BF motivational salience signal via electrical stimulation led to faster and more precise RTs and supports a causal relationship. Together, these results not only describe for the first time, to our knowledge, the quantitative relationship between motivational salience and faster decision speed, they also reveal the quantitative coupling relationship between motivational salience and more precise RT. Our results further establish the existence of an early and previously unrecognized step in the decision-making process that determines both the RT speed and variability of the entire decision-making process and suggest that this novel decision step is dictated largely by the BF motivational salience signal. Finally, our study raises the hypothesis that the dysregulation of decision speed in conditions such as depression, schizophrenia, and cognitive aging may result from the functional impairment of the motivational salience signal encoded by the poorly understood noncholinergic BF neurons.
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spelling pubmed-39583352014-03-27 Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed Avila, Irene Lin, Shih-Chieh PLoS Biol Research Article The survival of animals depends critically on prioritizing responses to motivationally salient stimuli. While it is generally believed that motivational salience increases decision speed, the quantitative relationship between motivational salience and decision speed, measured by reaction time (RT), remains unclear. Here we show that the neural correlate of motivational salience in the basal forebrain (BF), defined independently of RT, is coupled with faster and also more precise decision speed. In rats performing a reward-biased simple RT task, motivational salience was encoded by BF bursting response that occurred before RT. We found that faster RTs were tightly coupled with stronger BF motivational salience signals. Furthermore, the fraction of RT variability reflecting the contribution of intrinsic noise in the decision-making process was actively suppressed in faster RT distributions with stronger BF motivational salience signals. Artificially augmenting the BF motivational salience signal via electrical stimulation led to faster and more precise RTs and supports a causal relationship. Together, these results not only describe for the first time, to our knowledge, the quantitative relationship between motivational salience and faster decision speed, they also reveal the quantitative coupling relationship between motivational salience and more precise RT. Our results further establish the existence of an early and previously unrecognized step in the decision-making process that determines both the RT speed and variability of the entire decision-making process and suggest that this novel decision step is dictated largely by the BF motivational salience signal. Finally, our study raises the hypothesis that the dysregulation of decision speed in conditions such as depression, schizophrenia, and cognitive aging may result from the functional impairment of the motivational salience signal encoded by the poorly understood noncholinergic BF neurons. Public Library of Science 2014-03-18 /pmc/articles/PMC3958335/ /pubmed/24642480 http://dx.doi.org/10.1371/journal.pbio.1001811 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
spellingShingle Research Article
Avila, Irene
Lin, Shih-Chieh
Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed
title Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed
title_full Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed
title_fullStr Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed
title_full_unstemmed Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed
title_short Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed
title_sort motivational salience signal in the basal forebrain is coupled with faster and more precise decision speed
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3958335/
https://www.ncbi.nlm.nih.gov/pubmed/24642480
http://dx.doi.org/10.1371/journal.pbio.1001811
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