Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers

Money is a secondary reinforcer commonly used across a range of disciplines in experimental paradigms investigating reward learning and decision-making. The effectiveness of monetary reinforcers during aversive learning and its neural basis, however, remains a topic of debate. Specifically, it is u...

Full description

Bibliographic Details
Main Authors: Mauricio R Delgado, Rita L. Jou, Elizabeth A. Phelps
Format: Article
Language:English
Published: Frontiers Media S.A. 2011-05-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnins.2011.00071/full
_version_ 1818288281148719104
author Mauricio R Delgado
Rita L. Jou
Elizabeth A. Phelps
author_facet Mauricio R Delgado
Rita L. Jou
Elizabeth A. Phelps
author_sort Mauricio R Delgado
collection DOAJ
description Money is a secondary reinforcer commonly used across a range of disciplines in experimental paradigms investigating reward learning and decision-making. The effectiveness of monetary reinforcers during aversive learning and its neural basis, however, remains a topic of debate. Specifically, it is unclear if the initial acquisition of aversive representations of monetary losses depends on similar neural systems as more traditional aversive conditioning that involves primary reinforcers. This study contrasts the efficacy of a biologically defined primary reinforcer (shock) and a socially defined secondary reinforcer (money) during aversive learning and its associated neural circuitry. During a two-part experiment, participants first played a gambling game where wins and losses were based on performance to gain an experimental bank. Participants were then exposed to two separate aversive conditioning sessions. In one session, a primary reinforcer (mild shock) served as an unconditioned stimulus (US) and was paired with one of two colored squares, the conditioned stimuli (CS+ and CS-, respectively). In another session, a secondary reinforcer (loss of money) served as the US and was paired with one of two different CS. Skin conductance responses were greater for CS+ compared to CS- trials irrespective of type of reinforcer. Neuroimaging results revealed that the striatum, a region typically linked with reward-related processing, was found to be involved in the acquisition of aversive conditioned response irrespective of reinforcer type. In contrast, the amygdala was involved during aversive conditioning with primary reinforcers, as suggested by both an exploratory fMRI analysis and a follow-up case study with a patient with bilateral amygdala damage. Taken together, these results suggest that learning about potential monetary losses may depend on reinforcement learning related systems, rather than on typical structures involved in more biologically based fears.
first_indexed 2024-12-13T01:53:53Z
format Article
id doaj.art-1921cce0cc8b4be19213e7a80f2ed564
institution Directory Open Access Journal
issn 1662-453X
language English
last_indexed 2024-12-13T01:53:53Z
publishDate 2011-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neuroscience
spelling doaj.art-1921cce0cc8b4be19213e7a80f2ed5642022-12-22T00:03:26ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2011-05-01510.3389/fnins.2011.000719403Neural systems underlying aversive conditioning in humans with primary and secondary reinforcersMauricio R Delgado0Rita L. Jou1Elizabeth A. Phelps2Rutgers UniversityNew York UniversityNew York UniversityMoney is a secondary reinforcer commonly used across a range of disciplines in experimental paradigms investigating reward learning and decision-making. The effectiveness of monetary reinforcers during aversive learning and its neural basis, however, remains a topic of debate. Specifically, it is unclear if the initial acquisition of aversive representations of monetary losses depends on similar neural systems as more traditional aversive conditioning that involves primary reinforcers. This study contrasts the efficacy of a biologically defined primary reinforcer (shock) and a socially defined secondary reinforcer (money) during aversive learning and its associated neural circuitry. During a two-part experiment, participants first played a gambling game where wins and losses were based on performance to gain an experimental bank. Participants were then exposed to two separate aversive conditioning sessions. In one session, a primary reinforcer (mild shock) served as an unconditioned stimulus (US) and was paired with one of two colored squares, the conditioned stimuli (CS+ and CS-, respectively). In another session, a secondary reinforcer (loss of money) served as the US and was paired with one of two different CS. Skin conductance responses were greater for CS+ compared to CS- trials irrespective of type of reinforcer. Neuroimaging results revealed that the striatum, a region typically linked with reward-related processing, was found to be involved in the acquisition of aversive conditioned response irrespective of reinforcer type. In contrast, the amygdala was involved during aversive conditioning with primary reinforcers, as suggested by both an exploratory fMRI analysis and a follow-up case study with a patient with bilateral amygdala damage. Taken together, these results suggest that learning about potential monetary losses may depend on reinforcement learning related systems, rather than on typical structures involved in more biologically based fears.http://journal.frontiersin.org/Journal/10.3389/fnins.2011.00071/fullAmygdalaFear conditioningReinforcementRewardStriatuminsula
spellingShingle Mauricio R Delgado
Rita L. Jou
Elizabeth A. Phelps
Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
Frontiers in Neuroscience
Amygdala
Fear conditioning
Reinforcement
Reward
Striatum
insula
title Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
title_full Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
title_fullStr Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
title_full_unstemmed Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
title_short Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
title_sort neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
topic Amygdala
Fear conditioning
Reinforcement
Reward
Striatum
insula
url http://journal.frontiersin.org/Journal/10.3389/fnins.2011.00071/full
work_keys_str_mv AT mauriciordelgado neuralsystemsunderlyingaversiveconditioninginhumanswithprimaryandsecondaryreinforcers
AT ritaljou neuralsystemsunderlyingaversiveconditioninginhumanswithprimaryandsecondaryreinforcers
AT elizabethaphelps neuralsystemsunderlyingaversiveconditioninginhumanswithprimaryandsecondaryreinforcers