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Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems

The neural bases of attention, a set of neural processes that promote behavioral selection, is a subject of intense investigation. In humans, rewarded cues influence attention, even when those cues are irrelevant to the current task. Because the amygdala plays a role in reward processing, and the ac...

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Autores principales: Kaskan, Peter M., Nicholas, Mark A., Dean, Aaron M., Murray, Elisabeth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9761678/
https://www.ncbi.nlm.nih.gov/pubmed/36319119
http://dx.doi.org/10.1523/JNEUROSCI.0925-22.2022
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author Kaskan, Peter M.
Nicholas, Mark A.
Dean, Aaron M.
Murray, Elisabeth A.
author_facet Kaskan, Peter M.
Nicholas, Mark A.
Dean, Aaron M.
Murray, Elisabeth A.
author_sort Kaskan, Peter M.
collection PubMed
description The neural bases of attention, a set of neural processes that promote behavioral selection, is a subject of intense investigation. In humans, rewarded cues influence attention, even when those cues are irrelevant to the current task. Because the amygdala plays a role in reward processing, and the activity of amygdala neurons has been linked to spatial attention, we reasoned that the amygdala may be essential for attending to rewarded images. To test this possibility, we used an attentional capture task, which provides a quantitative measure of attentional bias. Specifically, we compared reaction times (RTs) of adult male rhesus monkeys with bilateral amygdala lesions and unoperated controls as they made a saccade away from a high- or low-value rewarded image to a peripheral target. We predicted that: (1) RTs will be longer for high- compared with low-value images, revealing attentional capture by rewarded stimuli; and (2) relative to controls, monkeys with amygdala lesions would exhibit shorter RT for high-value images. For comparison, we assessed the same groups of monkeys for attentional capture by images of predators and conspecifics, categories thought to have innate biological value. In performing the attentional capture task, all monkeys were slowed more by high-value relative to low-value rewarded images. Contrary to our prediction, amygdala lesions failed to disrupt this effect. When presented with images of predators and conspecifics, however, monkeys with amygdala lesions showed significantly diminished attentional capture relative to controls. Thus, separate neural pathways are responsible for allocating attention to stimuli with learned versus innate value. SIGNIFICANCE STATEMENT Valuable objects attract attention. The amygdala is known to contribute to reward processing and the encoding of object reward value. We therefore examined whether the amygdala is necessary for allocating attention to rewarded objects. For comparison, we assessed the amygdala's contribution to attending to objects with innate biological value: predators and conspecifics. We found that the macaque amygdala is necessary for directing attention to images with innate biological value, but not for directing attention to recently learned reward-predictive images. These findings indicate that the amygdala makes selective contributions to attending to valuable objects. The data are relevant to mental health disorders, such as social anxiety disorders and small animal phobias, that arise from biased attention to select categories of objects.
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spelling pubmed-97616782022-12-19 Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems Kaskan, Peter M. Nicholas, Mark A. Dean, Aaron M. Murray, Elisabeth A. J Neurosci Research Articles The neural bases of attention, a set of neural processes that promote behavioral selection, is a subject of intense investigation. In humans, rewarded cues influence attention, even when those cues are irrelevant to the current task. Because the amygdala plays a role in reward processing, and the activity of amygdala neurons has been linked to spatial attention, we reasoned that the amygdala may be essential for attending to rewarded images. To test this possibility, we used an attentional capture task, which provides a quantitative measure of attentional bias. Specifically, we compared reaction times (RTs) of adult male rhesus monkeys with bilateral amygdala lesions and unoperated controls as they made a saccade away from a high- or low-value rewarded image to a peripheral target. We predicted that: (1) RTs will be longer for high- compared with low-value images, revealing attentional capture by rewarded stimuli; and (2) relative to controls, monkeys with amygdala lesions would exhibit shorter RT for high-value images. For comparison, we assessed the same groups of monkeys for attentional capture by images of predators and conspecifics, categories thought to have innate biological value. In performing the attentional capture task, all monkeys were slowed more by high-value relative to low-value rewarded images. Contrary to our prediction, amygdala lesions failed to disrupt this effect. When presented with images of predators and conspecifics, however, monkeys with amygdala lesions showed significantly diminished attentional capture relative to controls. Thus, separate neural pathways are responsible for allocating attention to stimuli with learned versus innate value. SIGNIFICANCE STATEMENT Valuable objects attract attention. The amygdala is known to contribute to reward processing and the encoding of object reward value. We therefore examined whether the amygdala is necessary for allocating attention to rewarded objects. For comparison, we assessed the amygdala's contribution to attending to objects with innate biological value: predators and conspecifics. We found that the macaque amygdala is necessary for directing attention to images with innate biological value, but not for directing attention to recently learned reward-predictive images. These findings indicate that the amygdala makes selective contributions to attending to valuable objects. The data are relevant to mental health disorders, such as social anxiety disorders and small animal phobias, that arise from biased attention to select categories of objects. Society for Neuroscience 2022-12-07 /pmc/articles/PMC9761678/ /pubmed/36319119 http://dx.doi.org/10.1523/JNEUROSCI.0925-22.2022 Text en Copyright © 2022 Kaskan, Nicholas et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Kaskan, Peter M.
Nicholas, Mark A.
Dean, Aaron M.
Murray, Elisabeth A.
Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems
title Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems
title_full Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems
title_fullStr Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems
title_full_unstemmed Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems
title_short Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems
title_sort attention to stimuli of learned versus innate biological value relies on separate neural systems
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9761678/
https://www.ncbi.nlm.nih.gov/pubmed/36319119
http://dx.doi.org/10.1523/JNEUROSCI.0925-22.2022
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