Neuroscience robotics for controlled induction and real-time assessment of hallucinations

Abstract

Although hallucinations are important and frequent symptoms in major psychiatric and neurological diseases, little is known about their brain mechanisms. Hallucinations are unpredictable and private experiences, making their investigation, quantification and assessment highly challenging. A major shortcoming in hallucination research is the absence of methods able to induce specific and short-lasting hallucinations, which resemble clinical hallucinations, can be elicited repeatedly and vary across experimental conditions. By integrating clinical observations and recent advances in cognitive neuroscience with robotics, we have designed a novel device and sensorimotor method able to repeatedly induce a specific, clinically relevant hallucination: presence hallucination. Presence hallucinations are induced by applying specific conflicting (spatiotemporal) sensorimotor stimulation including an upper extremity and the torso of the participant. Another, MRI-compatible, robotic device using similar sensorimotor stimulation permitted the identification of the brain mechanisms of these hallucinations. Enabling the identification of behavioral and a frontotemporal neural biomarkers of hallucinations, under fully controlled experimental conditions and in real-time, this method can be applied in healthy participants as well as patients with schizophrenia, neurodegenerative disease or other hallucinations. The execution of these protocols requires intermediate-level skills in cognitive neuroscience and MRI processing, as well as minimal coding experience to control the robotic device. These protocols take ~3 h to be completed.

Robotically-induced auditory-verbal hallucinations: combining self-monitoring and strong perceptual priors

“…Extending our sensorimotor procedure that has been shown to induce PH in healthy subjects (Bernasconi et al, 2022; Blanke et al, 2014; Dhanis et al, 2022; Orepic et al, 2021; Serino et al, 2021) and patients with Parkinson’s disease (Bernasconi et al, 2021), we here demonstrate a new experimental paradigm able to induce controlled AVH-like phenomena (manifested as specific false alarms) in healthy, non-hallucinating individuals. Previous methods of inducing hallucinations in healthy individuals – such as through psychedelic medications (Preller and Vollenweider, 2018) or by automatized visual stimulations (e.g., Flicker-induced (Allefeld et al, 2011; Pearson et al, 2016)) – have identified many important challenges present in hallucination engineering.…”

“…In our two studies with two independent cohorts, our participants detected voices (either their own or someone else's) presented at individual hearing thresholds in pink noise, while simultaneously experiencing robotic sensorimotor stimulation. We hypothesized that conflicting sensorimotor stimulation leading to a PH (Bernasconi et al, 2022(Bernasconi et al, , 2021Blanke et al, 2014) would lead to an increase in vocal false alarms (i.e., reporting hearing voices in trials with no physical voice present in noise), compared to the stimulation with a weaker sensorimotor conflict, thereby relating our findings with the self-monitoring account. Moreover, we hypothesized that this increase would be modulated by the voice task they are involved in (other-voice detection vs self-voice detection), being especially prominent when performing other-voice detection.…”

“…We used a robotic procedure that can create impairments in self-monitoring as well as elicit the sensations that there is another (alien) person close by (i.e., presence hallucination, PH) (Bernasconi et al, 2021;Blanke et al, 2014;Salomon et al, 2020;Serino et al, 2021). Specifically, we designed a robotic setup that exposes participants to sensorimotor conflicts of various degree between repeated upper-limb poking movements and the corresponding tactile sensations on the back (Hara et al, 2011), linked to the misperception of the source and identity of sensorimotor signals of one's own body (Bernasconi et al, 2022(Bernasconi et al, , 2021Blanke et al, 2014;Salomon et al, 2020;Serino et al, 2021). Thus, our robotic setup applies sensorimotor conflicts of various degree (i.e., self-monitoring perturbations) and induces a perceptual prior about the presence of an external non-existing agent.…”

“…Despite this clinical relevance, hallucination research, and the understanding of the underling brain mechanisms, has been hampered by methodological shortcomings to investigate hallucinations in real-time under controlled experimental settings. A major shortcoming is the absence of controlled procedures allowing to induce hallucinations in laboratory and/or clinical settings (Bernasconi et al, 2022; Pearson et al, 2016). Moreover, hallucination research has predominantly been conducted in clinical populations, and is therefore confounded by comorbidities existing in the tested populations.…”

“…We recently described a robotic procedure able to repeatedly induce a specific, highly-controllable and clinically-relevant sensorimotor hallucination – presence hallucination – the sensation that someone is nearby when no-one is actually present, and cannot be seen or heard (Bernasconi et al, 2022, 2021; Blanke et al, 2014). Merging techniques from engineering and neuroscience, this procedure has been used to induce and understand clinically-relevant hallucinations (Bernasconi et al, 2022) under controlled experimental conditions in healthy individuals (Blanke et al, 2014; Dhanis et al, 2022; Orepic et al, 2022, 2021; Serino et al, 2021) as well as in patients with Parkinson’s disease (Bernasconi et al, 2021) and early psychosis patients (Salomon et al, 2020). This method, when combined with auditory-verbal tasks that are carried out during robotic stimulation, is able to induce deficits in auditory-verbal self-monitoring in psychosis patients (Salomon et al, 2020) and induce changes in voice perception in healthy participants (Orepic et al, 2021).…”