Two Anatomically and Computationally Distinct Learning Signals Predict Changes to Stimulus-Outcome Associations in Hippocampus

Boorman, Erie D.; Rajendran, Vani G.; O’Reilly, Jill X.; Behrens, Timothy E.J.

doi:10.1016/j.neuron.2016.02.014

Cited by 103 publications

(152 citation statements)

References 65 publications

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“…In contrast to identity-specific signals in pOFC, we found that vmPFC represents different rewards using a general reward value code. This is in line with human imaging studies showing value processing in vmPFC (Plassmann et al, 2007;Chib et al, 2009;Lebreton et al, 2009;Levy and Glimcher, 2011;Howard et al, 2015), as well as studies showing that lesions to the vmPFC and adjacent OFC impair value-based choices (Bechara et al, 2000;Izquierdo et al, 2004;Fellows and Farah, 2007;Camille et al, 2011). However, to our knowledge no human or animal study has tested the effects of vmPFC lesions on behavior in a devaluation task, and it is therefore unclear whether vmPFC is necessary for goal-directed behavior.…”

Section: Discussionsupporting

confidence: 69%

“…Such signals have been identified in the OFC across species (Burke et al, 2008;Sescousse et al, 2010;Klein-Flügge et al, 2013;Howard et al, 2015;Boorman et al, 2016). Importantly, updating of these representations must occur on the fly, and thus without the need for additional stimulus-outcome learning (Dickinson and Balleine, 1994).…”

Section: Discussionmentioning

confidence: 99%

“…This specificity ensures that, for example, a decrease in the value of food after a meal does not affect the value of shelter or mates. Recent work in animals (Burke et al, 2008; and humans (Sescousse et al, 2010;Klein-Flügge et al, 2013;Howard et al, 2015;Boorman et al, 2016) has linked the OFC to the processing of such identity-specific reward signals (Rudebeck and Murray, 2014). These findings raise the possibility that identity-specific goal representations in OFC are altered to reflect changes in the value of a goal.…”

Section: Introductionmentioning

confidence: 99%

“…In contrast to OFC, activity in the vmPFC reflects decision values regardless of reward identity (Plassmann et al, 2007;Chib et al, 2009;Lebreton et al, 2009;Levy and Glimcher, 2011;Howard et al, 2015). Moreover, whereas identity-specific OFC signals are linked to reward expectations before a decision (Burke et al, 2008;Howard et al, 2015;Rich and Wallis, 2016), identity-general signals are typically observed at the time of choice (Daw et al, 2006;Padoa-Schioppa and Assad, 2006;Hampton and O'Doherty, 2007;Plassmann et al, 2007;Kennerley et al, 2011;Strait et al, 2014). Based on these findings, we hypothesized that identity-specific signals are directly updated in OFC and that they provide critical input to representations of decision values in vmPFC.…”

Section: Introductionmentioning

confidence: 99%

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Identity-Specific Reward Representations in Orbitofrontal Cortex Are Modulated by Selective Devaluation

2017

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Goal-directed behavior is sensitive to the current value of expected outcomes. This requires independent representations of specific rewards, which have been linked to orbitofrontal cortex (OFC) function. However, the mechanisms by which the human brain updates specific goals on the fly, and translates those updates into choices, have remained unknown. Here we implemented selective devaluation of appetizing food odors in combination with pattern-based neuroimaging and a decision-making task. We found that in a hungry state, participants chose to smell high-intensity versions of two value-matched food odor rewards. After eating a meal corresponding to one of the two odors, participants switched choices toward the low intensity of the sated odor but continued to choose the high intensity of the nonsated odor. This sensory-specific behavioral effect was mirrored by pattern-based changes in fMRI signal in lateral posterior OFC, where specific reward identity representations were altered after the meal for the sated food odor but retained for the nonsated counterpart. In addition, changes in functional connectivity between the OFC and general value coding in ventromedial prefrontal cortex (vmPFC) predicted individual differences in satiety-related choice behavior. These findings demonstrate how flexible representations of specific rewards in the OFC are updated by devaluation, and how functional connections to vmPFC reflect the current value of outcomes and guide goal-directed behavior.

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Section: Discussionsupporting

confidence: 69%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Identity-Specific Reward Representations in Orbitofrontal Cortex Are Modulated by Selective Devaluation

2017

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“…If every voxel contains 50 cells encoding stimulus A and 50 cells encoding stimulus B, it will be difficult to decode A versus B even using the most sensitive multivariate analysis [108]. fMRI adaptation bypasses this problem by relying on the sensitivity of individual neurons to repeated activation (Barron et al [107] in this issue), and has yielded a wealth of new insights in cognitive neuroscience [109][110][111][112].…”

Section: (D) Fmri Adaptationmentioning

confidence: 99%

Interpreting BOLD: towards a dialogue between cognitive and cellular neuroscience

Hall

Howarth

Kurth-Nelson

et al. 2016

Phil. Trans. R. Soc. B

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Cognitive neuroscience depends on the use of blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to probe brain function. Although commonly used as a surrogate measure of neuronal activity, BOLD signals actually reflect changes in brain blood oxygenation. Understanding the mechanisms linking neuronal activity to vascular perfusion is, therefore, critical in interpreting BOLD. Advances in cellular neuroscience demonstrating differences in this neurovascular relationship in different brain regions, conditions or pathologies are often not accounted for when interpreting BOLD. Meanwhile, within cognitive neuroscience, the increasing use of high magnetic field strengths and the development of model-based tasks and analyses have broadened the capability of BOLD signals to inform us about the underlying neuronal activity, but these methods are less well understood by cellular neuroscientists. In 2016, a Royal Society Theo Murphy Meeting brought scientists from the two communities together to discuss these issues. Here, we consolidate the main conclusions arising from that meeting. We discuss areas of consensus about what BOLD fMRI can tell us about underlying neuronal activity, and how advanced modelling techniques have improved our ability to use and interpret BOLD. We also highlight areas of controversy in understanding BOLD and suggest research directions required to resolve these issues. This article is part of the themed issue ‘Interpreting BOLD: a dialogue between cognitive and cellular neuroscience’.

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Anhedonia Reduction and the Association Between Left Ventral Striatal Reward Response and 6-Month Improvement in Life Satisfaction Among Young Adults

et al. 2019

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IMPORTANCE Anhedonia is a symptom of multiple psychiatric conditions in young adults that is associated with poorer mental health and psychosocial function and abnormal ventral striatum reward processing. Aberrant function of neural reward circuitry is well documented in anhedonia and other psychiatric disorders. Longitudinal studies to identify potential biomarkers associated with a reduction in anhedonia are necessary for the development of novel treatment targets. OBJECTIVE To identify neural reward-processing factors associated with improved psychiatric symptoms and psychosocial function in a naturalistic, observational context. DESIGN, SETTING, AND PARTICIPANTS A longitudinal cohort follow-up study was conducted from March 1, 2014, to June 5, 2018, at the University of Pittsburgh Medical Center after baseline functional magnetic resonance imaging in 52 participants between the ages of 18 and 25 years who were experiencing psychological distress. MAIN OUTCOMES AND MEASURES Participants were evaluated at baseline and 6 months. At baseline, participants underwent functional magnetic resonance imaging during a card-guessing monetary reward task. Participants completed measures of affective symptoms and psychosocial function at each visit. Neural activation during reward prediction error (RPE), a measure of reward learning, was determined using Statistical Parametric Mapping software. Neural reward regions with significant RPE activation were entered as regions associated with future symptoms in multiple linear regression models. RESULTS A total of 52 young adults (42 women and 10 men; mean [SD] age, 21.4 [2.2] years) completed the study. Greater RPE activation in the left ventral striatum was associated with a decrease in anhedonia symptoms during a 6-month period (β = −6.152; 95% CI,-11.870 to-0.433; P = .04). The decrease in anhedonia between baseline and 6 months mediated the association between left ventral striatum activation to RPE and improvement in life satisfaction between baseline and 6 months (total [c path] association: β = 0.245; P = .01; direct [c′ path] association: β = 0.133; P = .16; and indirect [ab path] association: 95% CI, 0.026-0.262). Results were not associated with psychotropic medication use. CONCLUSIONS AND RELEVANCE Greater left ventral striatum responsiveness to RPE may serve as a biomarker or potential target for novel treatments to improve the severity of anhedonia, overall mental health, and psychosocial function.

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Two Anatomically and Computationally Distinct Learning Signals Predict Changes to Stimulus-Outcome Associations in Hippocampus

Cited by 103 publications

References 65 publications

Identity-Specific Reward Representations in Orbitofrontal Cortex Are Modulated by Selective Devaluation

Identity-Specific Reward Representations in Orbitofrontal Cortex Are Modulated by Selective Devaluation

Interpreting BOLD: towards a dialogue between cognitive and cellular neuroscience

Anhedonia Reduction and the Association Between Left Ventral Striatal Reward Response and 6-Month Improvement in Life Satisfaction Among Young Adults

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