Action simulation in hallucination-prone adolescents

Abstract

Theoretical and empirical accounts suggest that impairments in self-other discrimination processes are likely to promote the expression of hallucinations. Studies using a variety of paradigms involving self-performed actions argue in favor of perspective taking confusion in hallucination-prone subjects. However, our understanding of such processes during adolescence is still at an early stage. The present study thus aims (1) to delineate the neural correlates sustaining mental simulation of actions involving self-performed actions (first-person perspective; 1PP) and other-performed actions (third-person perspective; 3PP) during adolescence (2) to identify atypical activation patterns during 1PP/3PP mental simulation of actions in hallucination-prone adolescents (3) to examine whether differential risk for schizophrenia (clinical vs. genetic) is also associated with differential impairments in the 1PP/3PP mental simulation of actions during adolescence. Twenty-two typically developing controls (Control group; 6 females), 12 hallucination-prone adolescents [auditory hallucination (AH) group; 7 females] and 13 adolescents with 22q11.2 Deletion Syndrome (22q11.2DS group; 4 females) were included in the study. During the fMRI task, subjects were presented with a cue (self-other priming cues) indicating to perform the task using either a first person perspective (“you”-1PP) or a third person perspective (“best friend”-3PP) and then they were asked to mentally simulate actions based on the type of cue. Hallucination-proneness was assessed using a self-report questionnaire [Cardiff Anomalous Perception Scale (CAPS)]. Our results indicated that atypical patterns of cerebral activation, particularly in the key areas of self-other distinction, were found in both groups at risk for auditory hallucinations (AHs and 22q11.2DS). More precisely, adolescents in the AH group presented decreased activations in the right middle occipital gyrus BA19, left cingulate gyrus BA31, and right precuneus BA31 for the 3PP > 1PP contrast. Adolescents in the 22q11.2DS group presented decreased activations in the right superior occipital gyrus BA19, left caudate tail and left precuneus BA7 for the 3PP > 1PP contrast. In comparison to the Control group, only the 22q11.2DS adolescents showed a decreased activation for other-related cues (prime other > prime self contrast) in areas of visual imagery, episodic memory and social cognition. This study characterizes the neural correlates of mental imagery for actions during adolescence, and suggests that a differential risk for hallucination-proneness (clinical vs. genetic) is associated to similar patterns of atypical activations in key areas sustaining self-other discrimination processes. These observations may provide relevant information for future research and prevention strategies with regards to hallucination-proneness during adolescence.

Functional connectivity mapping of regions associated with self‐ and other‐processing

“…Furthermore, the vMPFC may play a crucial role in interpersonal processing, particularly social cognition [Bzdok et al, ], the representation of social value [Ruff and Fehr, ], and approach/avoidance‐modulating processing [Bzdok et al, ]. Moreover, reduced PCC/PC functioning may relate to impaired discrimination of third‐ from first‐person agency representations in hallucination‐prone individuals [Dahoun et al, ]. Two very recent meta‐analyses demonstrated the AG/TPJ to underlie higher order executive functioning associated with attention orientation and social cognition, particularly theory of mind [Bzdok et al, , Krall et al, in press].…”

Schizotypy From a Developmental Perspective

“…In a recent fMRI study on perspective-taking, comparable patterns of atypical neural activation during a 1p-3p perspective-taking task were observed for both typical adolescents reporting transient auditory verbal hallucinations and adolescents at ultrahigh risk for schizophrenia because of 22q11.2 deletion syndrome. 39 Together, these studies would suggest that high schizotypy appears to accompany the different endophenotypical risk markers during early risk for schizophrenia spectrum disorders. In other words, and from a clinical standpoint, the significant association between valid endophenotypes and early high schizotypy may signify the establishment of early risk progress for subclinical schizotypal youths.…”

“…Finally, social cognitive impairments associated with schizophrenia also relate to schizotypal expression during adolescence. [37][38][39] When this triad of observations is considered conjointly with the predictive value of schizotypy for the development of schizophrenia spectrum disorders, it positions this risk trait as a potent transactional agent, a developmental vehicle linking early endophenotypes to growing propensity of developing psychopathology. In other words, schizotypy might constitute a measurable intermediate mediator in the developmental cascade of schizophrenic disorders.…”

Current perspectives on the mechanisms of auditory hallucinations: introduction to the special research topic

“…In strong contrast, no attentional modulation of this area could be observed in schizophrenia patients with AH. Further similarities as well as differences in mechanisms underlying AH are shown by i Dahoun et al (2013) who compared neural correlates of mentally simulated actions (e.g., “open a window”) between hallucination-prone adolescents and a group with a genetic risk for schizophrenia (22q11.2 deletion syndrome). While both groups exhibited decreased activation in regions related to self-other distinction when imagining a close friend performing an action, individuals with a genetic risk for schizophrenia displayed additional decreased activations in areas associated with visual imagery, episodic memory and social cognition when “simply” seeing a cue that said either “you” or “best friend” earlier on in the task.…”