Modulation of motivational salience processing during the early stages of psychosis

Smieskova, Renata; Roiser, Jonathan P.; Chaddock, Christopher; Schmidt, André; Harrisberger, Fabienne; Bendfeldt, Kerstin; Simon, Andor E.; Walter, Anna; Fusar‐Poli, Paolo; McGuire, Philip; Lang, Undine E.; Riecher-Rössler, Anita; Borgwardt, Stefan

doi:10.1016/j.schres.2015.04.036

Cited by 54 publications

(71 citation statements)

References 65 publications

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“…[15][16][17][18] Other studies including patients with broadly defined first-episode psychosis (not restricted to schizophrenia and schizophreniform disorder) or individuals at-risk for psychosis did not report any group differences, but focused more on the relationship with symptom expression. [19][20][21][22][23] This work supports the idea that on a group level reduced activation of the striatum may be more strongly related to schizophrenia or chronic forms of psychosis than to psychotic disorders in general. Importantly, these divergent findings highlight the importance of using dimensional approaches to investigate the neural basis of psychosis rather than restricting research to group differences.…”

Section: Introductionsupporting

confidence: 80%

“…19,53 At the group level, we found no differences between HCs and individuals with SPT or first-episode psychosis in VS activation, which is consistent with previous results in broadly defined FEP patients and individuals at-risk for psychosis. [19][20][21][22] In contrast, there is now meta-analytic support for reduced VS activation in patients with established schizophrenia, 24 but results on the individual study level are very inconsistent. 15,16,23,25,31,35,59,62,63 These mixed findings support the notion that striatal alterations in psychosis do not solely consist of hypo-activation but vary between different stages (early vs chronic) and different forms of psychosis (schizophrenia vs non-schizophrenia).…”

Section: Discussionmentioning

confidence: 99%

“…Only recently, researchers have begun to shed light on this important question, but data are still very limited. 22,[32][33][34] Importantly, with respect to individuals with schizotypal traits no study has ever investigated reward anticipation to identify neural correlates of symptom expression.…”

Section: Introductionmentioning

confidence: 99%

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Ventral Striatal Dysfunction and Symptom Expression in Individuals With Schizotypal Personality Traits and Early Psychosis

Kirschner

Hager

Muff

et al. 2016

SCHBUL

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Striatal abnormalities play a crucial role in the pathophysiology of schizophrenia. Growing evidence suggests an association between aberrant striatal activity during reward anticipation and symptom dimensions in schizophrenia. However, it is not clear whether this holds across the psychosis continuum. The aim of the present study was to investigate alterations of ventral striatal activation during reward anticipation and its relationship to symptom expression in persons with schizotypal personality traits (SPT) and first-episode psychosis. Twenty-six individuals with high SPT, 26 patients with non-affective first-episode psychosis (including 13 with brief psychotic disorder (FEP-BPD) and 13 with first-episode schizophrenia [FEP-SZ]) and 25 healthy controls underwent event-related functional magnetic resonance imaging while performing a variant of the Monetary Incentive Delay task. Ventral striatal activation was positively correlated with total symptom severity, in particular with levels of positive symptoms. This association was observed across the psychosis continuum and within each subgroup. Patients with FEP-SZ showed the strongest elevation of striatal activation during reward anticipation, although symptom levels did not differ between groups in the psychosis continuum. While our results provide evidence that variance in striatal activation is mainly explained by dimensional symptom expression, patients with schizophrenia show an additional dysregulation of striatal activation. Trans-diagnostic approaches are promising in order to disentangle dimensional and categorical neural mechanisms in the psychosis continuum.

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Section: Introductionsupporting

confidence: 80%

Section: Discussionmentioning

confidence: 99%

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Ventral Striatal Dysfunction and Symptom Expression in Individuals With Schizotypal Personality Traits and Early Psychosis

Kirschner

Hager

Muff

et al. 2016

SCHBUL

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“…14 These 3 fMRI studies together show local activity changes mainly in the VS, insula and ACC in patients with FEP during reward prediction 4,5,14 as well as alterations in these regions induced by antipsychotic medication. 11,14 One previous fMRI study in unmedicated patients with schizophrenia showed reduced connectivity between the prefrontal cortex and the VS during reward processing.…”

Section: Introductionmentioning

confidence: 93%

“…11 Although not speci cally during reward processing, a recent resting-state fMRI study in patients J Psychiatry Neurosci 2016;41 (6) with FEP also showed that atypical antipsychotics increased functional connectivity between striatal regions, the ACC and right anterior insula, 12 which correlated positively with symptom improvement. Using the Salience Attribution Task (SAT), 13 Smieskova and colleagues 14 recently reported that compared with controls patients with FEP showed reduced right insula activity in response to high-versus low-probability reward cues. Furthermore, the right insula and ACC activity was negatively correlated with the severity of hallucinations in unmedi cated patients.…”

Section: Introductionmentioning

confidence: 99%

Dysfunctional insular connectivity during reward prediction in patients with first-episode psychosis

Schmidt

Palaniyappan

Smieskova

et al. 2016

jpn

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IntroductionOur brain is constantly exposed to a wide variety of stimuli, which compete for limited cognitive resources. External stimu li are processed depending on their salience so as to ignore predictable, state and task-irrelevant events while enhancing resource allocation in order to process unexpected or state-and task-relevant events. Efficient prediction of salient stimuli, such as those of rewards, is thus essential for adapting ongoing behaviour. This process requires the ability to learn that a neutral stimulus becomes emotionally endowed owing to its association with primary reinforcement. 1 Behavioural and fMRI studies have demonstrated impairments in patients with psychosis when anticipating reward.2 Relative to controls, behavioural evidence indicated that patients with rst-episode psychosis (FEP) exhibited less reactivity to reward-predicting cues.3 Functional MRI studies during reward prediction have reported reduced activity in diverse brain regions, including the ventral striatum (VS), 4,5 anterior cingulate cortex (ACC), midbrain, thalamus and cerebellum, of unmedicated patients with FEP compared with controls. 5 It has further been shown that VS activation during reward prediction was negatively related to positive psychotic symptoms in patients with FEP. 4,5 Reward processing is critically mediated by dopamine, 6,7 and the VS response to reward-predicting cues is likely triggered by dopamine activity. 8,9 A previous fMRI study in patients with chronic schizophrenia showed that the VS response during reward prediction was reduced only in patients treated with typical antipsychotics, whereas no difference was observed between healthy controls and patients treated with atypical medication. 10 In line with this nding in patients with chronic schizophrenia, the reduced baseline VS activation during reward prediction seen in patients with FEP relative to healthy controls has been reported to be normalized after 6 weeks of monotherapy with atypical antipsychotics.11 The largest improvement in positive symptoms was seen in patients with the highest VS signal increase.11 Although not speci cally during reward processing, a recent resting-state fMRI study in patients Background: Increasing evidence indicates that psychosis is associated with abnormal reward processing. Imaging studies in patients with first-episode psychosis (FEP) have revealed reduced activity in diverse brain regions, including the ventral striatum, insula and anterior cingulate cortex (ACC), during reward prediction. However, whether these reductions in local brain activity are due to altered connectivity has rarely been explored. Methods: We applied dynamic causal modelling and Bayesian model selection to fMRI data during the Salience Attribution Task to investigate whether patients with FEP showed abnormal modulation of connectivity between the ventral striatum, insula and ACC induced by rewarding cues and whether these changes were related to positive psychotic symptoms and atypical antipsychotic medication. Results: The model...

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Ventral Striatal Activation During Reward Processing in Psychosis

et al. 2015

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IMPORTANCE Abnormal reward processing is suggested to underlie the formation of psychotic symptoms, likely driven by elevated ventral striatal (VS) dopamine levels. Functional magnetic resonance imaging studies reveal alterations of VS activity during reward processing in patients with chronic psychosis and first episode of psychosis, as well as individuals at high risk for psychosis, but findings are inconclusive, conflicting, and difficult to subject to meta-analysis without introducing bias because several studies reported that findings were not statistically significant but did not report statistics. OBJECTIVE To assess the differences between patients with schizophrenia spectrum disorders and healthy controls in VS activation during reward processing. DATA SOURCES Web of Knowledge database (incorporating Web of Science and MEDLINE) until July 2015, including references of eligible articles and reviews. STUDY SELECTION Functional magnetic resonance imaging studies comparing VS activity during monetary reward processing between patients with schizophrenia spectrum disorders or clinical or genetic high-risk state for psychosis and healthy controls. DATA EXTRACTION AND SYNTHESIS Statistics and thresholds related to the main outcome measures and potential moderators were independently retrieved by 2 investigators. Effect sizes were analyzed using MetaNSUE, a random-effects method that enables the unbiased inclusion of nonstatistically significant unreported effects. MAIN OUTCOMES AND MEASURES Effect size of the group differences in VS activity, and correlation between VS activity and negative and positive symptom scores in patients. RESULTS The meta-analysis included 23 studies (917 patients) for reward anticipation, 9 studies (358 patients) for reward feedback, and 8 studies (314 patients) for reward prediction error. We found significant bilateral VS hypoactivation during reward anticipation (23 studies, n = 917) in patients compared with healthy controls (left/right Cohen d, −0.50/−0.70; P< .001). Left VS abnormality was more severe in patients with high scores of negative symptoms during reward anticipation (r=−0.41; P< .001). Patients also showed hypoactivation during reward feedback (left/right d, −0.57/−0.56; P< .001). Simulations showed that exclusion of studies with nonstatistically significant unreported effects was associated with a strong bias (d bias=0.22), whereas estimations using MetaNSUE were unbiased even when statistics were seldom reported (d bias < 0.001). CONCLUSIONS AND RELEVANCE This meta-analysis provides evidence that patients with psychosis demonstrate VS hypoactivation during reward anticipation. The assessment of VS prediction errors seems to be promising, but more studies are needed to draw valid conclusions.

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Modulation of motivational salience processing during the early stages of psychosis

Abstract: The changes in adaptive motivational salience processing during psychosis development reveal neurofunctional abnormalities in the somatosensory and premotor cortex. Antipsychotic medication seems to modify hemodynamic responses in the anterior cingulate and insula.

Cited by 54 publications

References 65 publications

Ventral Striatal Dysfunction and Symptom Expression in Individuals With Schizotypal Personality Traits and Early Psychosis

Ventral Striatal Dysfunction and Symptom Expression in Individuals With Schizotypal Personality Traits and Early Psychosis

Dysfunctional insular connectivity during reward prediction in patients with first-episode psychosis

Ventral Striatal Activation During Reward Processing in Psychosis

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