Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment
Recent evidence suggests that the aberrant signaling of salience is associated with psychotic illness. Salience, however, can take many forms in task environments. For example, salience may refer to any of the following: (1) the valence of an outcome, (2) outcomes that are unexpected, called reward...
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| Format: | Article |
| Language: | English |
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MDPI AG
2021-12-01
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| Series: | Brain Sciences |
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| Online Access: | https://www.mdpi.com/2076-3425/11/12/1610 |
| _version_ | 1797506460154855424 |
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| author | Adam J. Culbreth Zuzana Kasanova Thomas J. Ross Betty J. Salmeron James M. Gold Elliot A. Stein James A. Waltz |
| author_facet | Adam J. Culbreth Zuzana Kasanova Thomas J. Ross Betty J. Salmeron James M. Gold Elliot A. Stein James A. Waltz |
| author_sort | Adam J. Culbreth |
| collection | DOAJ |
| description | Recent evidence suggests that the aberrant signaling of salience is associated with psychotic illness. Salience, however, can take many forms in task environments. For example, salience may refer to any of the following: (1) the valence of an outcome, (2) outcomes that are unexpected, called reward prediction errors (PEs), or (3) cues associated with uncertain outcomes. Here, we measure brain responses to different forms of salience in the context of a passive PE-signaling task, testing whether patients with schizophrenia (SZ) showed aberrant signaling of particular types of salience. We acquired event-related MRI data from 29 SZ patients and 23 controls during the performance of a passive outcome prediction task. Across groups, we found that the anterior insula and posterior parietal cortices were activated to multiple different types of salience, including PE magnitude and heightened levels of uncertainty. However, BOLD activation to salient events was not significantly different between patients and controls in many regions, including the insula, posterior parietal cortices, and default mode network nodes. Such results suggest that deficiencies in salience processing in SZ may not result from an impaired ability to signal salience <i>per se</i>, but instead the ability to use such signals to guide future actions. Notably, no between-group differences were observed in BOLD signal changes associated with PE-signaling in the striatum. However, positive symptom severity was found to significantly correlate with the magnitudes of salience contrasts in default mode network nodes. Our results suggest that, in an observational environment, SZ patients may show an intact ability to activate striatal and cortical regions to rewarding and non-rewarding salient events. Furthermore, reduced deactivation of a hypothesized default mode network node for SZ participants with high levels of positive symptoms, following salient events, point to abnormalities in interactions of the salience network with other brain networks, and their potential importance to positive symptoms. |
| first_indexed | 2024-03-10T04:32:58Z |
| format | Article |
| id | doaj.art-a141d437f2644a05a55684b994861609 |
| institution | Directory Open Access Journal |
| issn | 2076-3425 |
| language | English |
| last_indexed | 2024-03-10T04:32:58Z |
| publishDate | 2021-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Brain Sciences |
| spelling | doaj.art-a141d437f2644a05a55684b9948616092023-11-23T04:02:03ZengMDPI AGBrain Sciences2076-34252021-12-011112161010.3390/brainsci11121610Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task EnvironmentAdam J. Culbreth0Zuzana Kasanova1Thomas J. Ross2Betty J. Salmeron3James M. Gold4Elliot A. Stein5James A. Waltz6Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD 21228, USALeuven Research & Development Spin-off & Innovation Unit, KU Leuven, Waaistraat 6-Box 5105, 3000 Leuven, BelgiumNeuroimaging Research Branch, National Institute on Drug Abuse-Intramural Research Program, Baltimore, MD 21224, USANeuroimaging Research Branch, National Institute on Drug Abuse-Intramural Research Program, Baltimore, MD 21224, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD 21228, USANeuroimaging Research Branch, National Institute on Drug Abuse-Intramural Research Program, Baltimore, MD 21224, USAMaryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD 21228, USARecent evidence suggests that the aberrant signaling of salience is associated with psychotic illness. Salience, however, can take many forms in task environments. For example, salience may refer to any of the following: (1) the valence of an outcome, (2) outcomes that are unexpected, called reward prediction errors (PEs), or (3) cues associated with uncertain outcomes. Here, we measure brain responses to different forms of salience in the context of a passive PE-signaling task, testing whether patients with schizophrenia (SZ) showed aberrant signaling of particular types of salience. We acquired event-related MRI data from 29 SZ patients and 23 controls during the performance of a passive outcome prediction task. Across groups, we found that the anterior insula and posterior parietal cortices were activated to multiple different types of salience, including PE magnitude and heightened levels of uncertainty. However, BOLD activation to salient events was not significantly different between patients and controls in many regions, including the insula, posterior parietal cortices, and default mode network nodes. Such results suggest that deficiencies in salience processing in SZ may not result from an impaired ability to signal salience <i>per se</i>, but instead the ability to use such signals to guide future actions. Notably, no between-group differences were observed in BOLD signal changes associated with PE-signaling in the striatum. However, positive symptom severity was found to significantly correlate with the magnitudes of salience contrasts in default mode network nodes. Our results suggest that, in an observational environment, SZ patients may show an intact ability to activate striatal and cortical regions to rewarding and non-rewarding salient events. Furthermore, reduced deactivation of a hypothesized default mode network node for SZ participants with high levels of positive symptoms, following salient events, point to abnormalities in interactions of the salience network with other brain networks, and their potential importance to positive symptoms.https://www.mdpi.com/2076-3425/11/12/1610schizophreniadopaminereinforcementbasal gangliaventromedial prefrontal cortex |
| spellingShingle | Adam J. Culbreth Zuzana Kasanova Thomas J. Ross Betty J. Salmeron James M. Gold Elliot A. Stein James A. Waltz Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment Brain Sciences schizophrenia dopamine reinforcement basal ganglia ventromedial prefrontal cortex |
| title | Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment |
| title_full | Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment |
| title_fullStr | Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment |
| title_full_unstemmed | Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment |
| title_short | Schizophrenia Patients Show Largely Similar Salience Signaling Compared to Healthy Controls in an Observational Task Environment |
| title_sort | schizophrenia patients show largely similar salience signaling compared to healthy controls in an observational task environment |
| topic | schizophrenia dopamine reinforcement basal ganglia ventromedial prefrontal cortex |
| url | https://www.mdpi.com/2076-3425/11/12/1610 |
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