Resting-State Functional Connectivity of the Nucleus Accumbens in Auditory and Visual Hallucinations in Schizophrenia

Abstract

Both auditory hallucinations (AH) and visual hallucinations may occur in schizophrenia. One of the main hypotheses underlying their occurrence involves the increased activity of the mesolimbic pathway, which links the ventral tegmental area (VTA) and the nucleus accumbens (NAcc). However, the precise contribution of the mesolimbic pathway in hallucinations across various sensory modalities has not yet been explored. We compared the resting-state functional connectivity (rs-FC) of the NAcc among 16 schizophrenia patients with pure AH, 15 with both visuoauditory hallucinations (VAH), and 14 without hallucinations (NoH). A betweengroup comparison was performed using random-effects ANCOVA (rs-FC of the bilateral NAcc as the dependent variable, groups as the between-subjects factor, age and Positive and Negative Syndrome Scale scores as covariates; q(false discovery rate [FDR]) < .05). Compared to the NoH group, the AH group exhibited significantly enhanced NAcc rs-FC with the left temporal superior gyrus, the cingulate gyri, and the VTA, whereas the VAH group, compared to the AH group, exhibited significantly enhanced NAcc rs-FC with the bilateral insula, putamen, parahippocampal gyri, and VTA. The strength in rs-FC between the NAcc and the VTA appeared to be positively associated with the presence of hallucinations, but the NAcc FC patterns changed with the complexity of these experiences (ie, 0, 1, or 2 sensory modalities), rather than with severity. This might support the aberrant salience hypothesis of schizophrenia. Moreover, these findings suggest that future clinical and neurobiological studies of hallucinations should evaluate not only the global severity of symptoms but also their sensorial features.

Modality-Dependent Impact of Hallucinations on Low-Frequency Fluctuations in Schizophrenia

“…12 Rolland et al 12 found that mesolimbic connectivity patterns changed with escalating sensory complexity of the experiences (eg, 0, 1, or 2 modalities). Relative to patients that did not endorse hallucinations in any sensory domain and those that endorsed hallucinations solely in the auditory domain, Sz patients that endorsed both VH and AH had significantly elevated parahippocampal, insular and striatal connectivity with the nucleus accumbens, while significant differences in hippocampal connectivity were not found between the pure AH group and NH.…”

“…Due to AH prevalence in Sz, these studies are designed to assess FC differences across patient groups that endorse both VH and AH vs patients that endorse only AH. Relative to patients that endorsed only AH, patients that endorse VH and AH show functional hyperconnectivity with subcortical structures including caudate, 11 putamen, 12 amygdala, 13 nucleus accumbens, 12 parahippocampus, 12 and hippocampus. 11,13 We posit that Sz patients that endorse AH will have distinct, dynamic patterns of rs-activity in comparison to patients that endorse both VH and AH.…”

Les neurosciences computationnelles en psychiatrie : peut-on modéliser les symptômes psychotiques ?

“…En effet, le signal codant pour une erreur de pré diction dans une structure dopaminergique sous-corticale, le striatum, augmente le couplage de structures corticales distantes [11], et pourrait ainsi renforcer leur association sous-tendant l'idé e dé lirante. De maniè re inté -ressante et en parfaite continuité avec ces hypothè ses, des anomalies de connectivité fonctionnelle du striatum ventral ont ré cemment pu être mises en é vidence dans la schizophré nie, recrutant des ré seaux neuronaux variables en fonction de la complexité hallucinatoire des sujets [37].…”

Response to “Cortico-accumbens circuitry in schizophrenia: Merely a reward system?” by Rolland and Jardri (SCHRES-14-D-00731)

“…In their recent publication, Rolland and colleagues (Rolland et al, 2014) linked hallucinations in patients with schizophrenia to connectivity between the nucleus accumbens (NAc), ventral tegmental area (VTA), and a number of other regions generally consistent with what we referred to as the brain reward circuit. Moreover, they noted in their letter that the circuitry that we found to be affected by THC and smoked cannabis has also been implicated in psychosis in schizophrenia, and that cannabis smoking can increase positive symptoms in these patients.…”