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Activation of Internal Correctness Monitoring Circuitry in Youth with Psychosis Spectrum Symptoms

  • Tess Levinson
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Lynch School of Education and Human Development, Boston College, Chestnut Hill, MA 02467, USA
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  • Greer Prettyman
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA
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  • Chloe Savage
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA
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  • Lauren White
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Penn-CHOP Lifespan Brain Institute, University of Pennsylvania, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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  • Tyler M. Moore
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Penn-CHOP Lifespan Brain Institute, University of Pennsylvania, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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  • Monica E. Calkins
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Penn-CHOP Lifespan Brain Institute, University of Pennsylvania, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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  • Kosha Ruparel
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA
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  • Raquel E. Gur
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Penn-CHOP Lifespan Brain Institute, University of Pennsylvania, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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  • Ruben C. Gur
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Penn-CHOP Lifespan Brain Institute, University of Pennsylvania, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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  • Theodore D. Satterthwaite
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA

    Penn-CHOP Lifespan Brain Institute, University of Pennsylvania, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA

    Lifespan Informatics and Neuroimaging Center (PennLINC), Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
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  • Daniel H. Wolf
    Correspondence
    Correspondence: Daniel H. Wolf M.D., Ph.D., 10th Floor Gates Bldg., 3400 Spruce St., Philadelphia, PA 19104. , Tele: (215) 662-3692, Fax: (215) 662-7903.
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia PA 19104, USA
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Published:January 31, 2023DOI:https://doi.org/10.1016/j.bpsc.2023.01.010

      ABSTRACT

      Background

      Self-directed performance monitoring is a critical contributor to cognitive performance and general functioning and is impacted by psychiatric symptoms and personality traits, but has been understudied in psychosis-risk states. We have shown that ventral striatum (VS) responds to correctness during cognitive tasks where no explicit feedback is required, and this “intrinsic reinforcement” response is reduced in schizophrenia.

      Methods

      Here we examined this phenomenon in youth (n=796, age 11-22) from the Philadelphia Neurodevelopmental Cohort (PNC) performing a working memory fMRI task. We hypothesized that VS would respond to internal correctness monitoring while classic “salience network” regions such as dorsal anterior cingulate cortex (ACC) and anterior insular cortex (AIC) would reflect internal error monitoring, and that these responses would increase with age. We expected that neurobehavioral measures of performance monitoring would be reduced in youth with subclinical psychosis spectrum (PS) features and correlate with amotivation severity.

      Results

      Supporting these hypotheses, we found correct>incorrect activation in VS, and incorrect>correct activation in ACC and AIC. Furthermore, VS activation was positively correlated with age, reduced in PS, and inversely correlated with amotivation. However, these patterns were not significant in ACC and AIC.

      Conclusions

      These findings advance our understanding of the neural underpinnings of performance monitoring and its impairment in adolescents with PS. Such understanding can facilitate investigation of the developmental trajectory of normative and aberrant performance monitoring, contribute to early identification of youth at elevated risk for poor academic, occupational, or psychiatric outcomes, and provide potential targets for therapeutic development.

      Keywords

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