Abstract
Disrupted striatal functional connectivity is proposed to play a critical role in the development of psychotic symptoms. Previous resting-state functional magnetic resonance imaging (rs-fMRI) studies typically reported disrupted striatal connectivity in patients with psychosis and in individuals at clinical and genetic high risk of the disorder relative to healthy controls. This has not been widely studied in healthy individuals with subclinical psychotic-like experiences (schizotypy). Here we applied the emerging technology of multi-echo rs-fMRI to examine corticostriatal connectivity in this group, which is thought to drastically maximize physiological noise removal and increase BOLD contrast-to-noise ratio. Multi-echo rs-fMRI data (echo times, 12, 28, 44, 60 ms) were acquired from healthy individuals with low (LS, n = 20) and high (HS, n = 19) positive schizotypy as determined with the Oxford-Liverpool Inventory of Feelings and Experiences (O-LIFE). After preprocessing to ensure optimal contrast and removal of non-BOLD signal components, whole-brain functional connectivity from six striatal seeds was compared between the HS and LS groups. Effects were considered significant at cluster-level p < .05 family-wise error correction. Compared to LS, HS subjects showed lower rs-fMRI connectivity between ventromedial prefrontal regions and ventral striatal regions. Lower connectivity was also observed between the dorsal putamen and the hippocampus, occipital regions, as well as the cerebellum. These results demonstrate that subclinical positive psychotic-like experiences in healthy individuals are associated with striatal hypoconnectivity as detected using multi-echo rs-fMRI. Further application of this approach may aid in characterizing functional connectivity abnormalities across the extended psychosis phenotype.
Highlights
Over the last two decades, the dysconnection hypothesis of schizophrenia (Friston et al, 2016; Friston and Frith, 1995; McGuire and Frith, 1996) has gained growing neurobiological support due to technical advances in structural and functional magnetic resonance imaging (Pettersson-Yeo et al, 2011)
NeuroImage: Clinical 21 (2019) 101603 patients with a full-blown psychotic disorder (Boehme et al, 2015; Diaconescu et al, 2010; Pankow et al, 2016; Roiser et al, 2013; Schlagenhauf et al, 2009; Winton-Brown et al, 2017, 2014). Such evidence aligns well with predictions based on animal models of psychosis (Lodge and Grace, 2011) which show that striatal dysfunction may result from increased hippocampal activity, which may in turn be related to prefrontal cortex (PFC) abnormalities (Gomes and Grace, 2017), and propose that disrupted interactions within this corticostriatal circuit contribute to the development of aberrant salience processing and positive symptoms (Grace, 2016)
Two hundred and fifty potential participants who had responded to online advertising via the Research Volunteer Recruitment Webpage of King's College London were pre-screened using the short version of the Oxford-Liverpool Inventory of Feelings and Experiences (O-LIFE) (Mason and Claridge, 2006)
Summary
Over the last two decades, the dysconnection hypothesis of schizophrenia (Friston et al, 2016; Friston and Frith, 1995; McGuire and Frith, 1996) has gained growing neurobiological support due to technical advances in structural and functional magnetic resonance imaging (Pettersson-Yeo et al, 2011). There is evidence to suggest that positive symptoms may be associated with disrupted task-related striatal activation and connectivity during the attribution of aberrant salience to otherwise irrelevant stimuli in healthy individuals, CHR subjects, and NeuroImage: Clinical 21 (2019) 101603 patients with a full-blown psychotic disorder (Boehme et al, 2015; Diaconescu et al, 2010; Pankow et al, 2016; Roiser et al, 2013; Schlagenhauf et al, 2009; Winton-Brown et al, 2017, 2014). Such evidence aligns well with predictions based on animal models of psychosis (Lodge and Grace, 2011) which show that striatal dysfunction may result from increased hippocampal activity, which may in turn be related to prefrontal cortex (PFC) abnormalities (Gomes and Grace, 2017), and propose that disrupted interactions within this corticostriatal circuit contribute to the development of aberrant salience processing and positive symptoms (Grace, 2016)
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