Task-related neural mechanisms of persecutory ideation in schizophrenia and community monozygotic twin-pairs

Krista M. Wisner, Melissa K. Johnson, James N. Porter, Robert F. Krueger, Angus W. MacDonald

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Perceptions of spiteful behavior are common, distinct from rational fear, and may undergird persecutory ideation. To test this hypothesis and investigate neural mechanisms of persecutory ideation, we employed a novel economic social decision-making task, the Minnesota Trust Game (MTG), during neuroimaging in patients with schizophrenia (n = 30) and community monozygotic (MZ) twins (n = 38; 19 pairs). We examined distinct forms of mistrust, task-related brain activation and connectivity, and investigated relationships with persecutory ideation. We tested whether co-twin discordance on these measurements was correlated to reflect a common source of underlying variance. Across samples persecutory ideation was associated with reduced trust only during the suspiciousness condition, which assessed spite sensitivity given partners had no monetary incentive to betray. Task-based activation contrasts for specific forms of mistrust were limited and unrelated to persecutory ideation. However, task-based connectivity contrasts revealed a dorsal cingulate anterior insula network sensitive to suspicious mistrust, a left frontal–parietal (lF-P) network sensitive to rational mistrust, and a ventral medial/orbital prefrontal (vmPFC/OFC) network that was sensitive to the difference between these forms of mistrust (all p <.005). Higher persecutory ideation was predicted only by reduced connectivity between the vmPFC/OFC and lF-P networks (p =.005), which was only observed when the intentions of the other player were relevant. Moreover, co-twin differences in persecutory ideation predicted co-twin differences in both spite sensitivity and in vmPFC/OFC–lF-P connectivity. This work found that interconnectivity may be particularly important to the complex neurobiology underlying persecutory ideation, and that unique environmental variance causally linked persecutory ideation, decision-making, and brain connectivity.

Original languageEnglish (US)
Pages (from-to)5244-5263
Number of pages20
JournalHuman Brain Mapping
Volume42
Issue number16
Early online dateJul 31 2021
DOIs
StatePublished - Nov 2021

Bibliographical note

Funding Information:
This work was supported by funding from National Association Research in Schizophrenia and Depression/Brain Behavior Research Foundation awards to AWM and National Institute of Mental Health grants R21MH112918 to AWM and F31MH102997 to KMW. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the Brain Behavior Research Foundation. We thank the participants for their time and effort involved in the study. We also thank the Minnesota Center for Twin and Family Research, the Minnesota Supercomputer Institute, and the Center for Magnetic Resonance Research at the University of Minnesota, each for resources or support during different phases of the study.

Funding Information:
National Association Research in Schizophrenia and Depression/Brain Behavior Research Foundation's Francoeur Investigator Award; National Institute of Mental Health, Grant/Award Numbers: F31MH102997, R21MH112918 Funding information

Funding Information:
This work was supported by funding from National Association Research in Schizophrenia and Depression/Brain Behavior Research Foundation awards to AWM and National Institute of Mental Health grants R21MH112918 to AWM and F31MH102997 to KMW. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the Brain Behavior Research Foundation. We thank the participants for their time and effort involved in the study. We also thank the Minnesota Center for Twin and Family Research, the Minnesota Supercomputer Institute, and the Center for Magnetic Resonance Research at the University of Minnesota, each for resources or support during different phases of the study.

Publisher Copyright:
© 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

Keywords

  • decision-making
  • functional connectivity
  • monozygotic twins
  • persecutory ideation
  • schizophrenia
  • trust

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