Mind-wandering in Parkinson’s disease hallucinations reflects primary visual and default network coupling

Abstract

A mismatch between top-down expectations and incoming sensory information is thought to be associated with hallucinations across a range of neuropsychiatric disorders. In Parkinsons disease with visual hallucinations, abnormal activity within the default network, and its pattern of connectivity with early visual regions, has been identified as a potential pathological source of the internally generated expectations that override incoming sensory input. In the context of attention deficits and visual dysfunction, mental imagery and perceptual expectancies generated across the default network are suggested to exert excessive influence over earlier visual regions, leading to aberrant perceptual experiences. Whilst converging neuroimaging evidence has identified unconstrained default network activity in Parkinsons disease with hallucinations, to date there has been a lack of behavioural evidence to confirm the consequences of an over-engaged default mode network - therefore the contributions it might make to hallucination phenomenology remain speculative. To address this, we administered a validated thought-sampling task to 38 Parkinsons disease patients (18 with hallucinations; 20 without) and 40 controls, to test the hypothesis that individuals with hallucinations experience an increased frequency of mind-wandering - a form of spontaneous cognition strongly associated with mental imagery and default network activity. The neural correlates of mind-wandering frequency were examined in relation to resting-state functional connectivity. Our results showed that patients with hallucinations exhibited significantly higher mind-wandering frequencies compared to non-hallucinators, who in turn had reduced levels of mind-wandering relative to controls. Inter-network connectivity and seed-to-voxel analyses confirmed that increased mind-wandering in the hallucinating vs. non-hallucinating group was associated with greater coupling between the primary visual cortex and dorsal default network. Taken together, both elevated mind-wandering and increased default-visual network coupling emerged as a distinguishing feature of the hallucinatory phenotype. We propose that the finding of increased mind-wandering reflects unconstrained spontaneous thought and mental imagery, which in turn furnish the content of visual hallucinations. Our findings suggest that primary visual cortex to dorsal default network coupling may provide a neural substrate by which regions of the default network exert disproportionate influence over ongoing visual perception. These findings refine current models of visual hallucinations by identifying a specific cognitive phenomenon and neural substrate consistent with the top-down influences over perception that have been implicated in visual hallucinations.