Susceptibility to auditory hallucinations is associated with spontaneous but not directed modulation of top-down expectations for speech.

Ben Alderson-Day,Alena D Oncel,Ivy Yi Ting Leong,Sophie Denton,Jamie Moffatt,Sophie K Scott,Charles Fernyhough,Saloni Krishnan,Samuel Evans,Yu-Lin Wu,Zehra Gurbuz,César F Lima

doi:10.1093/nc/niac002

Abstract

Auditory verbal hallucinations (AVHs)—or hearing voices—occur in clinical and non-clinical populations, but their mechanisms remain unclear. Predictive processing models of psychosis have proposed that hallucinations arise from an over-weighting of prior expectations in perception. It is unknown, however, whether this reflects (i) a sensitivity to explicit modulation of prior knowledge or (ii) a pre-existing tendency to spontaneously use such knowledge in ambiguous contexts. Four experiments were conducted to examine this question in healthy participants listening to ambiguous speech stimuli. In experiments 1a (n = 60) and 1b (n = 60), participants discriminated intelligible and unintelligible sine-wave speech before and after exposure to the original language templates (i.e. a modulation of expectation). No relationship was observed between top-down modulation and two common measures of hallucination-proneness. Experiment 2 (n = 99) confirmed this pattern with a different stimulus—sine-vocoded speech (SVS)—that was designed to minimize ceiling effects in discrimination and more closely model previous top-down effects reported in psychosis. In Experiment 3 (n = 134), participants were exposed to SVS without prior knowledge that it contained speech (i.e. naïve listening). AVH-proneness significantly predicted both pre-exposure identification of speech and successful recall for words hidden in SVS, indicating that participants could actually decode the hidden signal spontaneously. Altogether, these findings support a pre-existing tendency to spontaneously draw upon prior knowledge in healthy people prone to AVH, rather than a sensitivity to temporary modulations of expectation. We propose a model of clinical and non-clinical hallucinations, across auditory and visual modalities, with testable predictions for future research.

Highlights

Hallucinations have long been considered a product of top-down processes: what the mind brings to our perception of the world, not the other way round (Esquirol 1832)
Performance significantly improved following exposure to the original sentences, as indicated by an increase in d′
Bias significantly increased, with participants being more likely to say that speech was present after template exposure [before hits M(SD)% = 67.9% (21.1%), false alarms M(SD) = 20.6% (12.3%); after hits M(SD)% = 88.6% (14.2%), false alarms = 26% (14.9%)]

Summary

Introduction

Hallucinations have long been considered a product of top-down processes: what the mind brings to our perception of the world, not the other way round (Esquirol 1832). Under the predictive processing framework (PPF), all of perception and cognition is the result of a trade-off between generative models of the world, shaped by prior expectations and prediction error, i.e. the gap between expectation and sensory input (Clark 2013; Hohwy 2014). Hallucinations have been posited as an imbalance between prior expectation and prediction error (Fletcher and Frith 2009; Jardri and Denève 2013; Powers et al 2016). Such accounts have been argued to be consistent with source-monitoring theories (Wilkinson 2014; Griffin and Fletcher 2017; Corlett et al 2019)

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