Valence processing in the PFC: Reconciling circuit-level and systems-level views

Austin A. Coley; Nancy Padilla-Coreano; Reesha Patel; Kay M. Tye

doi:10.1016/bs.irn.2020.12.002

Valence processing in the PFC: Reconciling circuit-level and systems-level views

Austin A. Coley, Nancy Padilla-Coreano, Reesha Patel, Kay M. Tye^*

^*Corresponding author for this work

Psychiatry and Behavioral Sciences

Research output: Chapter in Book/Report/Conference proceeding › Chapter

19 Scopus citations

Abstract

An essential component in animal behavior is the ability to process emotion and dissociate among positive and negative valence in response to a rewarding or aversive stimulus. The medial prefrontal cortex (mPFC)—responsible for higher order executive functions that include cognition, learning, and working memory; and is also involved in sociability—plays a major role in emotional processing and control. Although the amygdala is widely regarded as the “emotional hub,” the mPFC encodes for context-specific salience and elicits top-down control over limbic circuitry. The mPFC can then conduct behavioral responses, via cortico-striatal and cortico-brainstem pathways, that correspond to emotional stimuli. Evidence shows that abnormalities within the mPFC lead to sociability deficits, working memory impairments, and drug-seeking behavior that include addiction and compulsive disorders; as well as conditions such as anhedonia. Recent studies investigate the effects of aberrant salience processing on cortical circuitry and neuronal populations associated with these behaviors. In this chapter, we discuss mPFC valence processing, neuroanatomical connections, and physiological substrates involved in mPFC-associated behavior. We review neurocomputational and theoretical models such as “mixed selectivity,” that describe cognitive control, attentiveness, and motivational drives. Using this knowledge, we describe the effects of valence imbalances and its influence on mPFC neural pathways that contribute to deficits in social cognition, while understanding the effects in addiction/compulsive behaviors and anhedonia.

Original language	English (US)
Title of host publication	What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology
Editors	Adam T. Brockett, Adam T. Brockett, Linda M. Amarante, Mark Laubach, Matthew R. Roesch, Matthew R. Roesch
Publisher	Academic Press Inc
Pages	171-212
Number of pages	42
ISBN (Print)	9780323853361
DOIs	https://doi.org/10.1016/bs.irn.2020.12.002
State	Published - Jan 2021

Publication series

Name	International Review of Neurobiology
Volume	158
ISSN (Print)	0074-7742
ISSN (Electronic)	2162-5514

Funding

We thank Amy Cao for her illustration of Fig. 1. We thank Romy Wichmann and Gillian Matthews for comments on the manuscript, and Earl Miller for helpful discussion. We acknowledge funding sources K99 MH124435-01 (N.P.-C.), 8 K00 MH124182-03 (A.A.C.) and R01-MH115920 (NIMH; K.M.T.) Pioneer Award DP1-AT009925 (NCCIH; K.M.T.). The authors report no competing interest or biomedical financial interests. All authors contribute to conception, writing, figure making and editing/revising.

Keywords

Addiction
Anhedonia
Circuits
Context-modulated
Ensembles
Evolution
Mental health
Mixed selectivity
Prefrontal cortex
Social
Species
Valence

ASJC Scopus subject areas

Clinical Neurology
Cellular and Molecular Neuroscience

Access to Document

10.1016/bs.irn.2020.12.002

Cite this

Coley, A. A., Padilla-Coreano, N., Patel, R., & Tye, K. M. (2021). Valence processing in the PFC: Reconciling circuit-level and systems-level views. In A. T. Brockett, A. T. Brockett, L. M. Amarante, M. Laubach, M. R. Roesch, & M. R. Roesch (Eds.), What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology (pp. 171-212). (International Review of Neurobiology; Vol. 158). Academic Press Inc. https://doi.org/10.1016/bs.irn.2020.12.002

Coley, Austin A. ; Padilla-Coreano, Nancy ; Patel, Reesha et al. / Valence processing in the PFC : Reconciling circuit-level and systems-level views. What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology. editor / Adam T. Brockett ; Adam T. Brockett ; Linda M. Amarante ; Mark Laubach ; Matthew R. Roesch ; Matthew R. Roesch. Academic Press Inc, 2021. pp. 171-212 (International Review of Neurobiology).

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abstract = "An essential component in animal behavior is the ability to process emotion and dissociate among positive and negative valence in response to a rewarding or aversive stimulus. The medial prefrontal cortex (mPFC)—responsible for higher order executive functions that include cognition, learning, and working memory; and is also involved in sociability—plays a major role in emotional processing and control. Although the amygdala is widely regarded as the “emotional hub,” the mPFC encodes for context-specific salience and elicits top-down control over limbic circuitry. The mPFC can then conduct behavioral responses, via cortico-striatal and cortico-brainstem pathways, that correspond to emotional stimuli. Evidence shows that abnormalities within the mPFC lead to sociability deficits, working memory impairments, and drug-seeking behavior that include addiction and compulsive disorders; as well as conditions such as anhedonia. Recent studies investigate the effects of aberrant salience processing on cortical circuitry and neuronal populations associated with these behaviors. In this chapter, we discuss mPFC valence processing, neuroanatomical connections, and physiological substrates involved in mPFC-associated behavior. We review neurocomputational and theoretical models such as “mixed selectivity,” that describe cognitive control, attentiveness, and motivational drives. Using this knowledge, we describe the effects of valence imbalances and its influence on mPFC neural pathways that contribute to deficits in social cognition, while understanding the effects in addiction/compulsive behaviors and anhedonia.",

keywords = "Addiction, Anhedonia, Circuits, Context-modulated, Ensembles, Evolution, Mental health, Mixed selectivity, Prefrontal cortex, Social, Species, Valence",

author = "Coley, {Austin A.} and Nancy Padilla-Coreano and Reesha Patel and Tye, {Kay M.}",

note = "Funding Information: We thank Amy Cao for her illustration of Fig. 1. We thank Romy Wichmann and Gillian Matthews for comments on the manuscript, and Earl Miller for helpful discussion. We acknowledge funding sources K99 MH124435-01 (N.P.-C.), 8 K00 MH124182-03 (A.A.C.) and R01-MH115920 (NIMH; K.M.T.) Pioneer Award DP1-AT009925 (NCCIH; K.M.T.). The authors report no competing interest or biomedical financial interests. All authors contribute to conception, writing, figure making and editing/revising. Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",

year = "2021",

month = jan,

doi = "10.1016/bs.irn.2020.12.002",

language = "English (US)",

isbn = "9780323853361",

series = "International Review of Neurobiology",

publisher = "Academic Press Inc",

pages = "171--212",

editor = "Brockett, {Adam T.} and Brockett, {Adam T.} and Amarante, {Linda M.} and Mark Laubach and Roesch, {Matthew R.} and Roesch, {Matthew R.}",

booktitle = "What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology",

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Coley, AA, Padilla-Coreano, N, Patel, R & Tye, KM 2021, Valence processing in the PFC: Reconciling circuit-level and systems-level views. in AT Brockett, AT Brockett, LM Amarante, M Laubach, MR Roesch & MR Roesch (eds), What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology. International Review of Neurobiology, vol. 158, Academic Press Inc, pp. 171-212. https://doi.org/10.1016/bs.irn.2020.12.002

Valence processing in the PFC: Reconciling circuit-level and systems-level views. / Coley, Austin A.; Padilla-Coreano, Nancy; Patel, Reesha et al.
What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology. ed. / Adam T. Brockett; Adam T. Brockett; Linda M. Amarante; Mark Laubach; Matthew R. Roesch; Matthew R. Roesch. Academic Press Inc, 2021. p. 171-212 (International Review of Neurobiology; Vol. 158).

Research output: Chapter in Book/Report/Conference proceeding › Chapter

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AU - Padilla-Coreano, Nancy

AU - Patel, Reesha

AU - Tye, Kay M.

N1 - Funding Information: We thank Amy Cao for her illustration of Fig. 1. We thank Romy Wichmann and Gillian Matthews for comments on the manuscript, and Earl Miller for helpful discussion. We acknowledge funding sources K99 MH124435-01 (N.P.-C.), 8 K00 MH124182-03 (A.A.C.) and R01-MH115920 (NIMH; K.M.T.) Pioneer Award DP1-AT009925 (NCCIH; K.M.T.). The authors report no competing interest or biomedical financial interests. All authors contribute to conception, writing, figure making and editing/revising. Publisher Copyright: © 2021 Elsevier Inc.

PY - 2021/1

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N2 - An essential component in animal behavior is the ability to process emotion and dissociate among positive and negative valence in response to a rewarding or aversive stimulus. The medial prefrontal cortex (mPFC)—responsible for higher order executive functions that include cognition, learning, and working memory; and is also involved in sociability—plays a major role in emotional processing and control. Although the amygdala is widely regarded as the “emotional hub,” the mPFC encodes for context-specific salience and elicits top-down control over limbic circuitry. The mPFC can then conduct behavioral responses, via cortico-striatal and cortico-brainstem pathways, that correspond to emotional stimuli. Evidence shows that abnormalities within the mPFC lead to sociability deficits, working memory impairments, and drug-seeking behavior that include addiction and compulsive disorders; as well as conditions such as anhedonia. Recent studies investigate the effects of aberrant salience processing on cortical circuitry and neuronal populations associated with these behaviors. In this chapter, we discuss mPFC valence processing, neuroanatomical connections, and physiological substrates involved in mPFC-associated behavior. We review neurocomputational and theoretical models such as “mixed selectivity,” that describe cognitive control, attentiveness, and motivational drives. Using this knowledge, we describe the effects of valence imbalances and its influence on mPFC neural pathways that contribute to deficits in social cognition, while understanding the effects in addiction/compulsive behaviors and anhedonia.

AB - An essential component in animal behavior is the ability to process emotion and dissociate among positive and negative valence in response to a rewarding or aversive stimulus. The medial prefrontal cortex (mPFC)—responsible for higher order executive functions that include cognition, learning, and working memory; and is also involved in sociability—plays a major role in emotional processing and control. Although the amygdala is widely regarded as the “emotional hub,” the mPFC encodes for context-specific salience and elicits top-down control over limbic circuitry. The mPFC can then conduct behavioral responses, via cortico-striatal and cortico-brainstem pathways, that correspond to emotional stimuli. Evidence shows that abnormalities within the mPFC lead to sociability deficits, working memory impairments, and drug-seeking behavior that include addiction and compulsive disorders; as well as conditions such as anhedonia. Recent studies investigate the effects of aberrant salience processing on cortical circuitry and neuronal populations associated with these behaviors. In this chapter, we discuss mPFC valence processing, neuroanatomical connections, and physiological substrates involved in mPFC-associated behavior. We review neurocomputational and theoretical models such as “mixed selectivity,” that describe cognitive control, attentiveness, and motivational drives. Using this knowledge, we describe the effects of valence imbalances and its influence on mPFC neural pathways that contribute to deficits in social cognition, while understanding the effects in addiction/compulsive behaviors and anhedonia.

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KW - Circuits

KW - Context-modulated

KW - Ensembles

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KW - Social

KW - Species

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Coley AA, Padilla-Coreano N, Patel R, Tye KM. Valence processing in the PFC: Reconciling circuit-level and systems-level views. In Brockett AT, Brockett AT, Amarante LM, Laubach M, Roesch MR, Roesch MR, editors, What does Medial Frontal Cortex Signal During Behavior? Insights from Behavioral Neurophysiology. Academic Press Inc. 2021. p. 171-212. (International Review of Neurobiology). doi: 10.1016/bs.irn.2020.12.002

Valence processing in the PFC: Reconciling circuit-level and systems-level views

Abstract

Publication series

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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Cite this