Primary and secondary rewards differentially modulate neural activity dynamics during working memory

Stefanie M. Beck, Hannah S. Locke, Adam C. Savine, Koji Jimura, Todd S. Braver

Research output: Contribution to journalArticle

74 Citations (Scopus)

Abstract

Background: Cognitive control and working memory processes have been found to be influenced by changes in motivational state. Nevertheless, the impact of different motivational variables on behavior and brain activity remains unclear. Methodology/Principal Findings: The current study examined the impact of incentive category by varying on a withinsubjects basis whether performance during a working memory task was reinforced with either secondary (monetary) or primary (liquid) rewards. The temporal dynamics of motivation-cognition interactions were investigated by employing an experimental design that enabled isolation of sustained and transient effects. Performance was dramatically and equivalently enhanced in each incentive condition, whereas neural activity dynamics differed between incentive categories. The monetary reward condition was associated with a tonic activation increase in primarily right-lateralized cognitive control regions including anterior prefrontal cortex (PFC), dorsolateral PFC, and parietal cortex. In the liquid condition, the identical regions instead showed a shift in transient activation from a reactive control pattern (primary probe-based activation) during no-incentive trials to proactive control (primary cue-based activation) during rewarded trials. Additionally, liquid-specific tonic activation increases were found in subcortical regions (amygdala, dorsal striatum, nucleus accumbens), indicating an anatomical double dissociation in the locus of sustained activation. Conclusions/Significance: These different activation patterns suggest that primary and secondary rewards may produce similar behavioral changes through distinct neural mechanisms of reinforcement. Further, our results provide new evidence for the flexibility of cognitive control, in terms of the temporal dynamics of activation.

Original languageEnglish
Article numbere9251
JournalPLoS One
Volume5
Issue number2
DOIs
Publication statusPublished - 2010 Feb 16
Externally publishedYes

Fingerprint

Reward
Short-Term Memory
Motivation
Chemical activation
Data storage equipment
liquids
amygdala
Prefrontal Cortex
cognition
cortex
experimental design
Parietal Lobe
brain
Nucleus Accumbens
loci
Liquids
Amygdala
Cognition
Cues
Research Design

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Primary and secondary rewards differentially modulate neural activity dynamics during working memory. / Beck, Stefanie M.; Locke, Hannah S.; Savine, Adam C.; Jimura, Koji; Braver, Todd S.

In: PLoS One, Vol. 5, No. 2, e9251, 16.02.2010.

Research output: Contribution to journalArticle

Beck, Stefanie M. ; Locke, Hannah S. ; Savine, Adam C. ; Jimura, Koji ; Braver, Todd S. / Primary and secondary rewards differentially modulate neural activity dynamics during working memory. In: PLoS One. 2010 ; Vol. 5, No. 2.
@article{09d7ede6300940019087ac3fd42e9baa,
title = "Primary and secondary rewards differentially modulate neural activity dynamics during working memory",
abstract = "Background: Cognitive control and working memory processes have been found to be influenced by changes in motivational state. Nevertheless, the impact of different motivational variables on behavior and brain activity remains unclear. Methodology/Principal Findings: The current study examined the impact of incentive category by varying on a withinsubjects basis whether performance during a working memory task was reinforced with either secondary (monetary) or primary (liquid) rewards. The temporal dynamics of motivation-cognition interactions were investigated by employing an experimental design that enabled isolation of sustained and transient effects. Performance was dramatically and equivalently enhanced in each incentive condition, whereas neural activity dynamics differed between incentive categories. The monetary reward condition was associated with a tonic activation increase in primarily right-lateralized cognitive control regions including anterior prefrontal cortex (PFC), dorsolateral PFC, and parietal cortex. In the liquid condition, the identical regions instead showed a shift in transient activation from a reactive control pattern (primary probe-based activation) during no-incentive trials to proactive control (primary cue-based activation) during rewarded trials. Additionally, liquid-specific tonic activation increases were found in subcortical regions (amygdala, dorsal striatum, nucleus accumbens), indicating an anatomical double dissociation in the locus of sustained activation. Conclusions/Significance: These different activation patterns suggest that primary and secondary rewards may produce similar behavioral changes through distinct neural mechanisms of reinforcement. Further, our results provide new evidence for the flexibility of cognitive control, in terms of the temporal dynamics of activation.",
author = "Beck, {Stefanie M.} and Locke, {Hannah S.} and Savine, {Adam C.} and Koji Jimura and Braver, {Todd S.}",
year = "2010",
month = "2",
day = "16",
doi = "10.1371/journal.pone.0009251",
language = "English",
volume = "5",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - Primary and secondary rewards differentially modulate neural activity dynamics during working memory

AU - Beck, Stefanie M.

AU - Locke, Hannah S.

AU - Savine, Adam C.

AU - Jimura, Koji

AU - Braver, Todd S.

PY - 2010/2/16

Y1 - 2010/2/16

N2 - Background: Cognitive control and working memory processes have been found to be influenced by changes in motivational state. Nevertheless, the impact of different motivational variables on behavior and brain activity remains unclear. Methodology/Principal Findings: The current study examined the impact of incentive category by varying on a withinsubjects basis whether performance during a working memory task was reinforced with either secondary (monetary) or primary (liquid) rewards. The temporal dynamics of motivation-cognition interactions were investigated by employing an experimental design that enabled isolation of sustained and transient effects. Performance was dramatically and equivalently enhanced in each incentive condition, whereas neural activity dynamics differed between incentive categories. The monetary reward condition was associated with a tonic activation increase in primarily right-lateralized cognitive control regions including anterior prefrontal cortex (PFC), dorsolateral PFC, and parietal cortex. In the liquid condition, the identical regions instead showed a shift in transient activation from a reactive control pattern (primary probe-based activation) during no-incentive trials to proactive control (primary cue-based activation) during rewarded trials. Additionally, liquid-specific tonic activation increases were found in subcortical regions (amygdala, dorsal striatum, nucleus accumbens), indicating an anatomical double dissociation in the locus of sustained activation. Conclusions/Significance: These different activation patterns suggest that primary and secondary rewards may produce similar behavioral changes through distinct neural mechanisms of reinforcement. Further, our results provide new evidence for the flexibility of cognitive control, in terms of the temporal dynamics of activation.

AB - Background: Cognitive control and working memory processes have been found to be influenced by changes in motivational state. Nevertheless, the impact of different motivational variables on behavior and brain activity remains unclear. Methodology/Principal Findings: The current study examined the impact of incentive category by varying on a withinsubjects basis whether performance during a working memory task was reinforced with either secondary (monetary) or primary (liquid) rewards. The temporal dynamics of motivation-cognition interactions were investigated by employing an experimental design that enabled isolation of sustained and transient effects. Performance was dramatically and equivalently enhanced in each incentive condition, whereas neural activity dynamics differed between incentive categories. The monetary reward condition was associated with a tonic activation increase in primarily right-lateralized cognitive control regions including anterior prefrontal cortex (PFC), dorsolateral PFC, and parietal cortex. In the liquid condition, the identical regions instead showed a shift in transient activation from a reactive control pattern (primary probe-based activation) during no-incentive trials to proactive control (primary cue-based activation) during rewarded trials. Additionally, liquid-specific tonic activation increases were found in subcortical regions (amygdala, dorsal striatum, nucleus accumbens), indicating an anatomical double dissociation in the locus of sustained activation. Conclusions/Significance: These different activation patterns suggest that primary and secondary rewards may produce similar behavioral changes through distinct neural mechanisms of reinforcement. Further, our results provide new evidence for the flexibility of cognitive control, in terms of the temporal dynamics of activation.

UR - http://www.scopus.com/inward/record.url?scp=77949508331&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77949508331&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0009251

DO - 10.1371/journal.pone.0009251

M3 - Article

C2 - 20169080

AN - SCOPUS:77949508331

VL - 5

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 2

M1 - e9251

ER -