Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways

Patrik Wikman, Teemu Rinne, Christopher I. Petkov

Research output: Contribution to journalArticleScientificpeer-review

Abstract

In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task.

Original languageEnglish
Article number3055
JournalScientific Reports
Volume9
Number of pages17
ISSN2045-2322
DOIs
Publication statusPublished - 28 Feb 2019
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 515 Psychology
  • LONG-TERM-MEMORY
  • SELECTIVE ATTENTION
  • TASK ENGAGEMENT
  • DISCRIMINATION
  • SPECIFICITY
  • MOTIVATION
  • AMYGDALA
  • SYSTEM
  • MODEL

Cite this

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title = "Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways",
abstract = "In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task.",
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author = "Patrik Wikman and Teemu Rinne and Petkov, {Christopher I.}",
year = "2019",
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language = "English",
volume = "9",
journal = "Scientific Reports",
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T1 - Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways

AU - Wikman, Patrik

AU - Rinne, Teemu

AU - Petkov, Christopher I.

PY - 2019/2/28

Y1 - 2019/2/28

N2 - In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task.

AB - In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task.

KW - 515 Psychology

KW - LONG-TERM-MEMORY

KW - SELECTIVE ATTENTION

KW - TASK ENGAGEMENT

KW - DISCRIMINATION

KW - SPECIFICITY

KW - MOTIVATION

KW - AMYGDALA

KW - SYSTEM

KW - MODEL

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