Conscious vision: investigating visual hallucination awareness in Lewy body disease

Visual awareness includes the ability to distinguish internally generated sensory experience from veridical percepts derived from the external world. Visual hallucinations (VHs) are an example of internally generated experience with important clinical implications and are common in Lewy body disease (LBD), with some patients aware of their hallucinations and others not. The awareness difference between LBD patients provides an opportunity to study the neural and neuropsychological mechanisms of hallucination awareness (VH-awareness). We hypothesized that VH-awareness would be associated with functional brain alterations in terms of resting-state functional connectivity (rs-FC) within and between cerebral systems involved in VH (intra-/inter-network rs-FC). In this cross-sectional study, we focused on visual association areas and networks (VIS) engaged in prediction errors (PEs) and reality monitoring, comparing LBD patients with preserved awareness of VH (VH-aware) to those with impaired awareness of VH (VH-unaware). Compared to the VH-aware group, the VH-unaware group showed reduced rs-FC between the VIS and PE in the right hemisphere, with no differences in rs-FC within each individual system. This suggests that VH-unawareness in LBD might reflect disruptions in implicit, online awareness processes and, specifically, may depend on impaired functional coupling between the brain regions providing perceptual contents to the hallucinatory experience and those evaluating its congruency with internal predictions. Furthermore, VH-unaware patients exhibited deficits in executive functioning, aligning with altered PE mechanisms and visuoperceptual abilities, which may represent the primary dysfunction defining VH content. Although preliminary, our findings provide a foundation for further investigations into VH-awareness in LBD and a model of visual awareness set within a general framework of perception, hallucination and consciousness. Future research will need to explore the proposed awareness model in diverse clinical populations to further unveil the mechanisms and wider clinical implications of one of the most distinctive aspects of brain function.