8 Sulfaro et al. subjective ratings of imagery 'vividness'. If so, this would justify why vividness ratings are generally only investigated concern-ing imagined, not veridical, experiences: veridical percepts are maximally sensory by default. Hallucinations Our model also delineates conditions for hallucinations. Visually, a hallucination entails seeing a non-veridical sensory percept in a given region of the visual field instead of a percept that reflects external reality. Under our model, for any modality, the most per-ceptually compelling hallucinations would then be those where a non-veridical stimulus dominates most, if not all, low-level rep-resentations. The notion of non-veridical information penetrating sensory systems top-down to cause hallucinations has been pre-viously explored in depth under a predictive coding framework (Powers et al. 2016). In our model, it can occur from overweighting top-down information relative to bottom-up information. How-ever, hallucinations could also occur simply if aberrant low-level activity is fed through an otherwise normal perceptual system (Hahamy et al. 2021). Note that, in both cases, our model only accounts for the perceptual experience of imagery, hallucinated or otherwise, and not whether it was induced voluntarily (as imagery tends to be) or involuntarily (as hallucinations tend to be). In the first suggested route to hallucinations, top-down infor-mation becomes overweighted such that non-veridical thoughts can permeate low-level areas to nearly the same extent as uncontested bottom-up veridical input. In this case, hallucina-tions are modelled as an anomalous case of mental imagery with an extremely low representational equilibrium point, sim-ilar to hyperphantasia. If our model is correct, then individu-als with hallucinatory disorders should tend to have improved mental imagery abilities. Accordingly, Parkinson's hallucinators tend to have stronger mental imagery priming effects than non-hallucinating controls, with the degree of imagery-induced priming predicting hallucination frequency (Shine et al. 2015 ). Parkinson's hallucinators also mind-wander more than non-hallucinators, corresponding to increased connectivity to the early visual cortex from default network regions (Walpola et al. 2020 ). Additionally, although individuals with schizophrenia can have impaired memory, their abilities on visuospatial mental imagery manipulation tasks are enhanced compared to neurotypical con-trols ( Benson and Park 2013 ; Matthews et al. 2014 ). However, note that some individuals are able to complete mental imagery manipulation tasks while reporting no visual mental imagery (Zeman et al. 2010 ). Hallucinations should also occur when sensory input is dis-connected altogether such that internally generated percepts are entirely uncontested. If feedforward information is downweighted completely (wl-1=0) to any layer, then that layer and any layer above it are free to be commandeered by any high-level inter-nally generated stimulus present. Representations at such layers will then inevitably converge towards the internally generated stimulus representation (Figs 2b, e, and 3d). This could con-tribute to hallucinations in disorders of afferent visual processing (e. g. Charles Bonnet syndrome; Reichert et al. 2013 ). Hallucina-tions are reasonably common following cortical blindness (Aldrich et al. 1987), and in one such reported case, hallucinations could be induced directly from attempting voluntary mental imagery (Wunderlich et al. 2000 ). Dampening external sensory input might also contribute to hypnagogic hallucinations, which occur during sleep onset. When falling asleep, the cortex remains active sev-eral minutes after the thalamus begins silencing external sensory information (Magnin et al. 2010), potentially providing a window of time in which internally generated cortical activity has reduced competition from the external environment. Top-down effects are probably not solely responsible for hal-lucinatory perception, however. Hallucinations can be visually detailed and sometimes reportedly even clearer than veridical per-cepts (Teunisse et al. 1996; Ffytche et al. 1998; Manford and Ander-mann 1998). This implies that hallucinations may not be a purely top-down phenomenon given that retrohierarchically extrapolat-ing high-level information into low-level regions should result in a degradation of visual information (Breedlove et al. 2020). Many hallucinations are therefore likely to also involve aberrant low-level cortical activity ( Manford and Andermann 1998 ; Hahamy et al. 2021) perhaps independent of, or in tandem with, amplified feedback signals. Eyes-open versus eyes-closed imagery We note that the model proposed in this paper does not presume any difference between an eyes-closed and eyes-open state apart from the change to the content of the sensory input each act pro-duces. Although closing one's eyes might be ostensibly interpreted as disconnecting external sensory input to the visual system, if this were the case, our model would predict that closing one's eyes would rapidly result in hallucinations. While hallucinations can happen when the eyes are deprived of light, such phenomena gen-erally require either drugs (Fisher 1991) or multiple hours (if not days) of light deprivation to manifest (Merabet et al. 2004). It could be that darkness constitutes a genuine sensory disconnection, yet with neural activity adapting to a lack of competition on slow timescales, or it could be that sensory deprivation alone does not equate to a true sensory disconnection. A formal disconnection or downweighting of sensory input could instead require large-scale neurochemical or neurophysiological changes, such as those which occur when shifting between different states of arousal (see the following section, 'Serotonin and acetylcholine: neuro-logically plausible bottom-up and top-down weighting agents', for details). This may be why eye closure (or darkness) is not sufficient for hallucinations in neurotypical individuals during normal wak-ing states, but does co-occur with hallucinations during altered neurochemical states, such as during sleep onset and offset (i. e. hypnagogic and hypnopompic hallucinations) and during sleep itself (i. e. dreaming). Even in blind individuals who cannot per-ceive environmental light levels, hallucinations are not ubiquitous and tend to occur later in the day when drowsy (Manford and Andermann 1998), suggesting that darkness alone is not a form of sensory disconnection. Closing one's eyes (at least on short time scales) might then be most aptly interpreted as changing sensory input to a dif-fuse, dark, and generally unremarkable stimulus image rather than disconnecting it altogether. Still, visual mental imagery is more likely to be reported when eyes are closed rather than open (Sulfaro et al. 2023). However, while eye closure tends to aid the recall of fine-grained sensory information, potentially by improv-ing mental imagery, recall is not significantly improved compared to merely looking at blank space ( Vredeveldt et al. 2011 ). Yet, we acknowledge that our conceptualization of eye closure may be a simplification given that neural activity patterns between eyes-closed and eyes-open states can differ substantially even when both occur in darkness ( Marx et al. 2003, 2004). Even so, an eyes-closed state could still improve mental imagery simply due to the signal-to-noise ratio advantage gained by pitting an imagined stimulus representation against a homogenous closed-eye scene, with the additional benefit of hiding attentional distractors. Downloaded from https://academic. oup. com/nc/article/2023/1/niad018/7248966 by guest on 25 August 2024 