Fronto-Temporal Disconnection Within the Presence Hallucination Network in Psychotic Patients With Passivity Experiences

Abstract

Psychosis, characterized by hallucinations and delusions, is a common feature of psychiatric disease, especially schizophrenia. One prominent theory posits that psychosis is driven by abnormal sensorimotor predictions leading to the misattribution of self-related events. This misattribution has been linked to passivity experiences (PE), such as loss of agency and, more recently, to presence hallucinations (PH), defined as the conscious experience of the presence of an alien agent while no person is actually present. PH has been observed in schizophrenia, Parkinson’s disease, and neurological patients with brain lesions and, recently, the brain mechanisms of PH (PH-network) have been determined comprising bilateral posterior middle temporal gyrus (pMTG), inferior frontal gyrus (IFG), and ventral premotor cortex (vPMC). Given that the experience of an alien agent is a common feature of PE, we here analyzed the functional connectivity within the PH-network in psychotic patients with (N = 39) vs without PE (N = 26). We observed reduced fronto-temporal functional connectivity in patients with PE compared to patients without PE between the right pMTG and the right and left IFG of the PH-network. Moreover, when seeding from these altered regions, we observed specific alterations with brain regions commonly linked to auditory-verbal hallucinations (such as Heschl’s gyrus). The present connectivity findings within the PH-network extend the disconnection hypothesis for hallucinations to the specific case of PH and associates the PH-network with key brain regions for frequent psychotic symptoms such as auditory-verbal hallucinations, showing that PH are relevant to the study of the brain mechanisms of psychosis and PE.

The Felt Presence experience: From cognition to the clinic

“…They tested whether PE experiences were associated with the same FP network map that had been previously identified. Post-hoc connectivity analysis demonstrated that reductions in strength between the right MTG and IFG bilaterally was reduced in patients with passivity experiences [65]. Taken together, impaired multisensory integration may lead to difficulties in determining the source and identity of sensorimotor, proprioceptive, and interoceptive signals, and thus, weakening bodily-self processing.…”

“…Experimenters also identified in patients that weaker connectivity within this network was associated with greater cognitive decline and more FP experiences during the experimental task [66]. In a further study [65], experimenters acquired fMRI data from individuals diagnosed with psychosis who did or not did report passivity experiences. They tested whether PE experiences were associated with the same FP network map that had been previously identified.…”

“…Neuropsychological models of felt presence implicate abnormalities of a cortical network that includes the temporoparietal junction (TPJ), the insula, and the frontoparietal cortex associated with multisensory integration, bodily self-processing, self-other distinction, self-awareness, and mental imagery [4,16,48,65,66] (Figure 2A). There is some evidence to indicate that the 'presence' arises from a misattribution of one's own body perception; a (mis)projection of mental representation of the body schema including the postural, tactile, and kinaesthetic components [4].…”

Linking Agent Detection of Invisible Presences to the Self: Relevance for Religious and Spiritual Experiences

“…The feeling of presence has long interested psychologists (James, 1902 ), psychiatrists (Jaspers, 1913 ), and neurologists (Critchley, 1979 ), and has recently also been investigated as a clinical symptom. PH has been reported to co-occur with temporoparietal tumors (Brugger et al, 1996 ), epilepsy (Critchley, 1979 ; Brugger et al, 1996 ), stroke (Blanke et al, 2014 ), or schizophrenia (Llorca et al, 2016 ; Stripeikyte et al, 2021 ). Lately, PH has been classified as a frequent early hallucination in Parkinson's disease (Fénelon et al, 2011 ; Bernasconi et al, 2021 ) and Lewy Body dementia (Nagahama et al, 2010 ).…”

Abnormal interhemispheric and intrahemispheric functional connectivity dynamics in drug‐naïve first‐episode schizophrenia patients with auditory verbal hallucinations

“…AVHs are defined as hearing and perceiving voices in the absence of an external auditory stimulus. Based on the technology of functional magnetic resonance imaging (fMRI), recent findings suggested that AVHs might be traced back to abnormally intrinsic functional organizations involving multiple brain regions and networks (Cui et al, 2017 ; Hoffman et al, 2007 ; Kumari et al, 2010 ; Northoff & Qin, 2011 ; Scheinost et al, 2019 ; Silbersweig et al, 1995 ; Simons et al, 2010 ; Stripeikyte et al, 2021 ). Although multiple existing conceptual models of AVHs, such as top‐down and bottom‐up (Hugdahl, 2009 ), corollary discharge (Ford et al, 2007 ), nondominant language intrusion (Sommer et al, 2008 ; van Lutterveld et al, 2014 ), and interhemispheric miscommunication (Curcic‐Blake et al, 2013 ; Gavrilescu et al, 2010 ), were indicated by the previous studies, it is unclear which model is the most relevant for AVHs.…”