Oris Shenyan: Reduced susceptibility to experimentally-induced complex visual hallucinations with age

Percepts without corresponding external stimuli - are associated with various clinical conditions including schizophrenia (Silverstein & Lai, 2021), Parkinson’s disease (Barnes & David, 2001), dementia (Zarkali, Adams, et al., 2019), epilepsy (Kasper et al., 2010) and vision impairment (Jan & del Castillo, 2012). Many of these conditions are particularly prevalent in older adults. Though hallucinations are commonly experienced in these pathological states, they can also be experienced within the general population - both spontaneously (Johns et al., 2014; McGrath et al., 2015; Tien, 1991) and induced through experimental methods, for example using alterations in light and sound (Allefeld et al., 2011; Reeder, 2022; Wackermann et al., 2002). Across all of these states, the hallucinations that are experienced can range from simple (i.e. abstract, geometric forms) to more complex, (i.e. objects, human figures, or scenes) (Barnes & David, 2001; Jan & del Castillo, 2012; Kasper et al., 2010; Shenyan et al., 2024; Silverstein & Lai, 2021). However, it is unclear how susceptibility to phenomenologically distinct types of hallucinations changes across the lifespan in healthy adults.

Among the few studies that explore hallucination frequency in typical ageing, findings are inconsistent (Badcock et al., 2017, 2020a; Larøi et al., 2019; Shenyan et al., 2024; Soulas et al., 2016; Thompson et al., 2021). Though some studies report an increase in hallucinatory prevalence with age (Shenyan et al., 2024; Tien, 1991; Turvey et al., 2001), many report a decrease (Larøi et al., 2005, 2019; Maijer et al., 2018; Thompson et al., 2021). These studies often rely on self-report questionnaires, which may be prone to various biases: for example, older individuals may retrospectively under-report hallucinations due to stigma (Badcock et al., 2017, 2020a). We sought to resolve this discrepancy by measuring changes in hallucinatory proneness in a healthy ageing population using more objective, experimental measures (Shenyan et al., 2024). If hallucinations are rare in older people, their presence could provide a strong indicator of underlying pathological processes (Compton et al., 2012; Pagonabarraga et al., 2016; Zarkali, Adams, et al., 2019). Alternatively, an increase in hallucinations may simply be a normal aspect of ageing, and thus, we would observe a corresponding increase in a healthy, ageing population (Baumeister et al., 2017).

1.1 Age-related mechanisms of hallucinatory proneness

Ageing also offers a unique opportunity to test existing hypotheses about the multiple interrelated factors which have been shown to promote hallucinatory experiences. One key factor is an overreliance on prior expectations (Teufel et al., 2015; Zarkali, Adams, et al., 2019), which may act to increase the tendency to experience hallucinations when paired with an independent, pathological mechanism, for instance, in Lewy body disease (Zarkali, Adams, et al., 2019) or psychosis (Teufel et al., 2015). Alternatively, prior expectations may become overweighted to compensate for age-related declines in visual function, which reduce the reliability of sensory input (Collerton et al., 2023; Occelli et al., 2017). Given that visual function diminishes with age (Pitts, 1982), increased hallucinatory proneness in older adults may stem from the interaction between sensory deficits and stronger reliance on prior knowledge (Chan et al., 2021). We therefore predicted that both visual impairments and the weighting of prior expectations would increase with age, and that these factors would be associated with a heightened tendency to experience complex hallucinatory imagery in later life. Similarly, the strength and vividness of mental imagery - a predominantly top-down process (Dijkstra et al., 2017, 2019, 2022), may also influence hallucinatory proneness (Königsmark et al., 2021; Reeder, 2022). However, as mental imagery vividness tends to decline across the lifespan (Gulyás et al., 2022), this could alternatively predict a reduction in hallucinatory experiences in older age.

Another contributing factor to hallucinatory proneness is a reduced ability to suppress irrelevant signals—a cognitive process related to inhibitory control—which has been associated with increased auditory hallucinations (Alderson-Day et al., 2019; Badcock & Hugdahl, 2014; Swyer & Powers, 2020). This tendency can be measured through intentional memory inhibition tasks, which require participants to suppress responses to irrelevant memories (Alderson-Day et al., 2019; Paulik et al., 2007). Performance on tasks measuring inhibitory control and memory suppression correlate with the severity of hallucinations both in individuals with psychosis (Badcock et al., 2005; Waters et al., 2003) and in healthy controls, as measured via self-reported questionnaire (Alderson-Day et al., 2019). While most research on intentional memory inhibition and hallucinations has predominantly focused on the auditory domain, here we test the relationship between inhibition and visual hallucinations. Prior research suggests that the ability to intentionally suppress unwanted memories diminishes with age, with older adults’ performing poorer than younger adults in similar tasks (Anderson et al., 2011; Collette et al., 2009). This led us to hypothesise that age-related declines in intentional memory inhibition could also increase the tendency to experience hallucinatory experiences in older age.

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