Striatal sensitivity to reward deliveries and omissions in substance dependent patients

Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specif...

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Published inNeuroImage (Orlando, Fla.) Vol. 42; no. 4; pp. 1609 - 1621
Main Authors Bjork, James M., Smith, Ashley R., Hommer, Daniel W.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.10.2008
Elsevier Limited
Subjects
Active avoidance
Adult
Alcohol dependence
Alcoholism
Alcoholism - physiopathology
Behavior disorders
Bias
Cocaine
Cocaine dependence
Comorbidity
Corpus Striatum - physiopathology
Decision making
Female
fMRI
Humans
Hypotheses
Impulsivity
Insula
Laboratories
Loss
Magnetic Resonance Imaging - methods
Male
Middle Aged
Monetary incentives
Motivation
Nucleus accumbens
Persistence
Recruitment
Respiratory distress syndrome
Reward
Studies
Ventral striatum
Young Adult
Nucleus accumbens
Persistence
Cocaine dependence
fMRI
Impulsivity
Loss
Active avoidance
Insula
Alcohol dependence
Ventral striatum
Reward
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Abstract Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specifically, with no requirement for altered nondrug incentive processing. We assessed whether individuals undergoing inpatient therapy for SD are characterized by altered recruitment of mesolimbic incentive neurocircuitry by cues and deliveries of nondrug rewards. During functional magnetic resonance imaging, substance-dependent patients (SDP) and controls performed a modified monetary incentive delay task featuring: a) anticipatory cues that signaled opportunities to respond to a target to either win money or avoid losing money, b) notifications of wins and losses, and c) unexpected replacement of reward trial outcomes with a demand to repeat the trial. Both anticipatory reward cues and loss cues elicited similar mood responses and VS activation between SDP and controls. However, in SDP (but not controls), reward notifications also activated VS and mesial frontal cortex, and loss notifications activated anterior insula. Finally, substitution of expected outcomes in reward trials with notifications to repeat the trial deactivated the VS in SDP but not in controls. These data do not suggest that SD is characterized by altered recruitment of VS circuitry by cues for nondrug incentives. Rather, SDP may instead have increased limbic system sensitivity to reward and loss delivery, consistent with the role of impulsivity in SD.
AbstractList Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specifically, with no requirement for altered nondrug incentive processing. We assessed whether individuals undergoing inpatient therapy for SD are characterized by altered recruitment of mesolimbic incentive neurocircuitry by cues and deliveries of nondrug rewards. During functional magnetic resonance imaging, substance-dependent patients (SDP) and controls performed a modified monetary incentive delay task featuring: a) anticipatory cues that signaled opportunities to respond to a target to either win money or avoid losing money, b) notifications of wins and losses, and c) unexpected replacement of reward trial outcomes with a demand to repeat the trial. Both anticipatory reward cues and loss cues elicited similar mood responses and VS activation between SDP and controls. However, in SDP (but not controls), reward notifications also activated VS and mesial frontal cortex, and loss notifications activated anterior insula. Finally, substitution of expected outcomes in reward trials with notifications to repeat the trial deactivated the VS in SDP but not in controls. These data do not suggest that SD is characterized by altered recruitment of VS circuitry by cues for nondrug incentives. Rather, SDP may instead have increased limbic system sensitivity to reward and loss delivery, consistent with the role of impulsivity in SD.Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specifically, with no requirement for altered nondrug incentive processing. We assessed whether individuals undergoing inpatient therapy for SD are characterized by altered recruitment of mesolimbic incentive neurocircuitry by cues and deliveries of nondrug rewards. During functional magnetic resonance imaging, substance-dependent patients (SDP) and controls performed a modified monetary incentive delay task featuring: a) anticipatory cues that signaled opportunities to respond to a target to either win money or avoid losing money, b) notifications of wins and losses, and c) unexpected replacement of reward trial outcomes with a demand to repeat the trial. Both anticipatory reward cues and loss cues elicited similar mood responses and VS activation between SDP and controls. However, in SDP (but not controls), reward notifications also activated VS and mesial frontal cortex, and loss notifications activated anterior insula. Finally, substitution of expected outcomes in reward trials with notifications to repeat the trial deactivated the VS in SDP but not in controls. These data do not suggest that SD is characterized by altered recruitment of VS circuitry by cues for nondrug incentives. Rather, SDP may instead have increased limbic system sensitivity to reward and loss delivery, consistent with the role of impulsivity in SD.
Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specifically, with no requirement for altered nondrug incentive processing. We assessed whether individuals undergoing inpatient therapy for SD are characterized by altered recruitment of mesolimbic incentive neurocircuitry by cues and deliveries of nondrug rewards. During functional magnetic resonance imaging, substance-dependent patients (SDP) and controls performed a modified monetary incentive delay task featuring: a) anticipatory cues that signaled opportunities to respond to a target to either win money or avoid losing money, b) notifications of wins and losses, and c) unexpected replacement of reward trial outcomes with a demand to repeat the trial. Both anticipatory reward cues and loss cues elicited similar mood responses and VS activation between SDP and controls. However, in SDP (but not controls), reward notifications also activated VS and mesial frontal cortex, and loss notifications activated anterior insula. Finally, substitution of expected outcomes in reward trials with notifications to repeat the trial deactivated the VS in SDP but not in controls. These data do not suggest that SD is characterized by altered recruitment of VS circuitry by cues for nondrug incentives. Rather, SDP may instead have increased limbic system sensitivity to reward and loss delivery, consistent with the role of impulsivity in SD.
Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specifically, with no requirement for altered nondrug incentive processing. We assessed whether individuals undergoing inpatient therapy for SD are characterized by altered recruitment of mesolimbic incentive neurocircuitry by cues and deliveries of nondrug rewards. During functional magnetic resonance imaging, substance-dependent patients (SDP) and controls performed a modified monetary incentive delay task featuring: a) anticipatory cues that signaled opportunities to respond to a target to either win money or avoid losing money, b) notifications of wins and losses, and c) unexpected replacement of reward trial outcomes with a demand to repeat the trial. Both anticipatory reward cues and loss cues elicited similar mood responses and VS activation between SDP and controls. However, in SDP (but not controls), reward notifications also activated VS and mesial frontal cortex, and loss notifications activated anterior insula. Finally, substitution of expected outcomes in reward trials with notifications to repeat the trial deactivated the VS in SDP but not in controls. These data do not suggest that SD is characterized by altered recruitment of VS circuitry by cues for nondrug incentives. Rather, SD may instead have increased limbic system sensitivity to reward and loss delivery, consistent with the role of impulsivity in SD.
Author Smith, Ashley R.
Hommer, Daniel W.
Bjork, James M.
AuthorAffiliation 1 Division of Clinical Neuroscience and Behavioral Research, National Institute on Drug Abuse, National Institutes of Health
2 Laboratory of Clinical and Translational Studies, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health
AuthorAffiliation_xml – name: 2 Laboratory of Clinical and Translational Studies, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health
– name: 1 Division of Clinical Neuroscience and Behavioral Research, National Institute on Drug Abuse, National Institutes of Health
Author_xml – sequence: 1
  givenname: James M.
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  email: jbjork@mail.nih.gov
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– sequence: 3
  givenname: Daniel W.
  surname: Hommer
  fullname: Hommer, Daniel W.
  organization: Laboratory of Clinical and Translational Studies, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/18672069$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords Nucleus accumbens
Persistence
Cocaine dependence
fMRI
Impulsivity
Loss
Active avoidance
Insula
Alcohol dependence
Ventral striatum
Reward
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Snippet Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for...
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SubjectTerms Active avoidance
Adult
Alcohol dependence
Alcoholism
Alcoholism - physiopathology
Behavior disorders
Bias
Cocaine
Cocaine dependence
Comorbidity
Corpus Striatum - physiopathology
Decision making
Female
fMRI
Humans
Hypotheses
Impulsivity
Insula
Laboratories
Loss
Magnetic Resonance Imaging - methods
Male
Middle Aged
Monetary incentives
Motivation
Nucleus accumbens
Persistence
Recruitment
Respiratory distress syndrome
Reward
Studies
Ventral striatum
Young Adult
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Title Striatal sensitivity to reward deliveries and omissions in substance dependent patients
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