Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding

Emily A. Boeke, Justin M. Moscarello, Joseph E. LeDoux, Elizabeth A. Phelps, Catherine A. Hartley

Research output: Contribution to journalArticle

Abstract

Patients with anxiety disorders often experience a relapse in symptoms after exposure therapy. Similarly, threat responses acquired during Pavlovian threat conditioning often return after extinction learning. Accordingly, there is a need for alternative methods to persistently reduce threat responding. Studies in rodents have suggested that exercising behavioral control over an aversive stimulus can persistently diminish threat responses, and that these effects are mediated by the amygdala, ventromedial prefrontal cortex, and striatum. In this fMRI study, we attempted to translate these findings to humans. Subjects first underwent threat conditioning. We then contrasted two forms of safety learning: active avoidance, in which participants could prevent the shock through an action, and yoked extinction, with shock presentation matched to the active condition, but without instrumental control. The following day, we assessed subjects’ threat responses (measured by skin conductance) to the conditioned stimuli without shock. Subjects next underwent threat conditioning with novel stimuli. Yoked extinction subjects showed an increase in conditioned response to stimuli from the previous day, but the active avoidance group did not. Additionally, active avoidance subjects showed reduced conditioned responding during novel threat conditioning, but the extinction group did not. We observed between-group differences in striatal BOLD responses to shock omission in Avoidance/Extinction. These findings suggest a differential role for the striatum in human active avoidance versus extinction learning, and indicate that active avoidance may be more effective than extinction in persistently diminishing threat responses.

Original languageEnglish (US)
Pages (from-to)4808-4818
Number of pages11
JournalJournal of Neuroscience
Volume37
Issue number18
DOIs
StatePublished - May 3 2017

Fingerprint

Psychological Extinction
Conditioning (Psychology)
Problem-Based Learning
Avoidance Learning
Corpus Striatum
Amygdala
Prefrontal Cortex
Anxiety Disorders
Rodentia
Magnetic Resonance Imaging
Learning
Safety
Recurrence
Skin

Keywords

  • Active avoidance
  • Anxiety
  • Coping
  • Instrumental learning
  • Resilience
  • Threat conditioning

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Active avoidance : Neural mechanisms and attenuation of pavlovian conditioned responding. / Boeke, Emily A.; Moscarello, Justin M.; LeDoux, Joseph E.; Phelps, Elizabeth A.; Hartley, Catherine A.

In: Journal of Neuroscience, Vol. 37, No. 18, 03.05.2017, p. 4808-4818.

Research output: Contribution to journalArticle

Boeke, Emily A.; Moscarello, Justin M.; LeDoux, Joseph E.; Phelps, Elizabeth A.; Hartley, Catherine A. / Active avoidance : Neural mechanisms and attenuation of pavlovian conditioned responding.

In: Journal of Neuroscience, Vol. 37, No. 18, 03.05.2017, p. 4808-4818.

Research output: Contribution to journalArticle

@article{012b49379e2745bea0ab007ca70905b5,
title = "Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding",
abstract = "Patients with anxiety disorders often experience a relapse in symptoms after exposure therapy. Similarly, threat responses acquired during Pavlovian threat conditioning often return after extinction learning. Accordingly, there is a need for alternative methods to persistently reduce threat responding. Studies in rodents have suggested that exercising behavioral control over an aversive stimulus can persistently diminish threat responses, and that these effects are mediated by the amygdala, ventromedial prefrontal cortex, and striatum. In this fMRI study, we attempted to translate these findings to humans. Subjects first underwent threat conditioning. We then contrasted two forms of safety learning: active avoidance, in which participants could prevent the shock through an action, and yoked extinction, with shock presentation matched to the active condition, but without instrumental control. The following day, we assessed subjects’ threat responses (measured by skin conductance) to the conditioned stimuli without shock. Subjects next underwent threat conditioning with novel stimuli. Yoked extinction subjects showed an increase in conditioned response to stimuli from the previous day, but the active avoidance group did not. Additionally, active avoidance subjects showed reduced conditioned responding during novel threat conditioning, but the extinction group did not. We observed between-group differences in striatal BOLD responses to shock omission in Avoidance/Extinction. These findings suggest a differential role for the striatum in human active avoidance versus extinction learning, and indicate that active avoidance may be more effective than extinction in persistently diminishing threat responses.",
keywords = "Active avoidance, Anxiety, Coping, Instrumental learning, Resilience, Threat conditioning",
author = "Boeke, {Emily A.} and Moscarello, {Justin M.} and LeDoux, {Joseph E.} and Phelps, {Elizabeth A.} and Hartley, {Catherine A.}",
year = "2017",
month = "5",
doi = "10.1523/JNEUROSCI.3261-16.2017",
volume = "37",
pages = "4808--4818",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "18",

}

TY - JOUR

T1 - Active avoidance

T2 - Journal of Neuroscience

AU - Boeke,Emily A.

AU - Moscarello,Justin M.

AU - LeDoux,Joseph E.

AU - Phelps,Elizabeth A.

AU - Hartley,Catherine A.

PY - 2017/5/3

Y1 - 2017/5/3

N2 - Patients with anxiety disorders often experience a relapse in symptoms after exposure therapy. Similarly, threat responses acquired during Pavlovian threat conditioning often return after extinction learning. Accordingly, there is a need for alternative methods to persistently reduce threat responding. Studies in rodents have suggested that exercising behavioral control over an aversive stimulus can persistently diminish threat responses, and that these effects are mediated by the amygdala, ventromedial prefrontal cortex, and striatum. In this fMRI study, we attempted to translate these findings to humans. Subjects first underwent threat conditioning. We then contrasted two forms of safety learning: active avoidance, in which participants could prevent the shock through an action, and yoked extinction, with shock presentation matched to the active condition, but without instrumental control. The following day, we assessed subjects’ threat responses (measured by skin conductance) to the conditioned stimuli without shock. Subjects next underwent threat conditioning with novel stimuli. Yoked extinction subjects showed an increase in conditioned response to stimuli from the previous day, but the active avoidance group did not. Additionally, active avoidance subjects showed reduced conditioned responding during novel threat conditioning, but the extinction group did not. We observed between-group differences in striatal BOLD responses to shock omission in Avoidance/Extinction. These findings suggest a differential role for the striatum in human active avoidance versus extinction learning, and indicate that active avoidance may be more effective than extinction in persistently diminishing threat responses.

AB - Patients with anxiety disorders often experience a relapse in symptoms after exposure therapy. Similarly, threat responses acquired during Pavlovian threat conditioning often return after extinction learning. Accordingly, there is a need for alternative methods to persistently reduce threat responding. Studies in rodents have suggested that exercising behavioral control over an aversive stimulus can persistently diminish threat responses, and that these effects are mediated by the amygdala, ventromedial prefrontal cortex, and striatum. In this fMRI study, we attempted to translate these findings to humans. Subjects first underwent threat conditioning. We then contrasted two forms of safety learning: active avoidance, in which participants could prevent the shock through an action, and yoked extinction, with shock presentation matched to the active condition, but without instrumental control. The following day, we assessed subjects’ threat responses (measured by skin conductance) to the conditioned stimuli without shock. Subjects next underwent threat conditioning with novel stimuli. Yoked extinction subjects showed an increase in conditioned response to stimuli from the previous day, but the active avoidance group did not. Additionally, active avoidance subjects showed reduced conditioned responding during novel threat conditioning, but the extinction group did not. We observed between-group differences in striatal BOLD responses to shock omission in Avoidance/Extinction. These findings suggest a differential role for the striatum in human active avoidance versus extinction learning, and indicate that active avoidance may be more effective than extinction in persistently diminishing threat responses.

KW - Active avoidance

KW - Anxiety

KW - Coping

KW - Instrumental learning

KW - Resilience

KW - Threat conditioning

UR - http://www.scopus.com/inward/record.url?scp=85018924739&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85018924739&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.3261-16.2017

DO - 10.1523/JNEUROSCI.3261-16.2017

M3 - Article

VL - 37

SP - 4808

EP - 4818

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 18

ER -