Robot-induced hallucinations in Parkinson’s disease depend on altered sensorimotor processing in fronto-temporal network

Abstract

Hallucinations in Parkinson’s disease (PD) are disturbing and frequent non-motor symptoms and constitute a major risk factor for psychosis and dementia. We report a robotics-based approach applying conflicting sensorimotor stimulation, enabling the induction of presence hallucinations (PHs) and the characterization of a subgroup of patients with PD with enhanced sensitivity for conflicting sensorimotor stimulation and robot-induced PH. We next identify the fronto-temporal network of PH by combining MR-compatible robotics (and sensorimotor stimulation in healthy participants) and lesion network mapping (neurological patients without PD). This PH-network was selectively disrupted in an additional and independent cohort of patients with PD, predicted the presence of symptomatic PH, and associated with cognitive decline. These robotics-neuroimaging findings extend existing sensorimotor hallucination models to PD and reveal the pathological cortical sensorimotor processes of PH in PD, potentially indicating a more severe form of PD that has been associated with psychosis and cognitive decline.

Presence Hallucinations during Locomotion in Patients with Parkinson's Disease

“…[1][2][3] Recently, we have induced PHs safely in patients with PD by generating sensorimotor conflicts while patients repeatedly actuated a robotic device providing tactile feedback. 4 Patients with symptomatic PHs were more sensitive to such sensorimotor stimulation than those without. We also identified abnormal sensorimotor processes predictive for the occurrence of PHs.…”

“…Here, we describe the case of two patients with PD who reported PHs after PD onset only when they were involved in repetitive locomotor activities in daily life-clinical evidence in favor of the importance of sensorimotor signals in PHs in PD, compatible with repetitive robotic sensorimotor stimulation inducing PH in PD. 4 A 73-year old patient experienced PHs repeatedly, but only when walking outside his home. PHs are frequent and enduring, occurring several times per week: "I'm walking, then I feel that someone is just behind me, a bit on my right, wanting to overtake me, bending over my shoulder.…”

“…We argue that for some patients with PD, locomotion-a highly procedural motor activity associated with tactile and proprioceptive feedback-facilitates PHs by interfering with sensorimotor processes. 4 A widespread network including cerebellum, cortical and sub-cortical structures is involved in locomotion and integration of related sensorimotor signals, for which the role of the basal ganglia has particularly been emphasized. 5 Partly similar brain regions were recruited in robot-induced PHs, 4 suggesting a neural overlap between gait control and PHs.…”

“…4 A widespread network including cerebellum, cortical and sub-cortical structures is involved in locomotion and integration of related sensorimotor signals, for which the role of the basal ganglia has particularly been emphasized. 5 Partly similar brain regions were recruited in robot-induced PHs, 4 suggesting a neural overlap between gait control and PHs. We note that both patients did not suffer from dementia, nor delusions (Table 1).…”

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

“…In brief, Guthrie's anthropomorphism account (Guthrie, 1980(Guthrie, , 1989(Guthrie, , 2001) linked agent-detection to supernatural beliefs, arguing for a low-level perceptual tendency anthropomorphizing the environment and detecting the presence of humans in environments devoid of others. Generating such false-positive agent perceptions may be adaptive in human evolution, because FIGURE 1 | Experimental induction of PH using sensorimotor stimulation (modified after Bernasconi et al, 2021). (A) The robotic set-up used for induction of invisible presences in patients with Parkinsons' disease in a sitting position.…”