Spontaneous Activity Patterns in Primary Visual Cortex Predispose to Visual Hallucinations

Abstract

According to theoretical frameworks casting perception as inference, vision results from the integration of bottom-up visual input with top-down expectations. Under conditions of strongly degraded sensory input, this may occasionally result in false perceptions in the absence of a sensory signal, also termed "hallucinations." Here, we investigated whether spontaneous prestimulus activity patterns in sensory circuits, which may embody a participant's prior expectations, predispose the observer toward false perceptions. Specifically, we used fMRI to investigate whether the representational content of prestimulus activity in early visual cortex is linked to subsequent perception during a challenging detection task. Human participants were asked to detect oriented gratings of a particular orientation that were embedded in noise. We found two characteristics of prestimulus activity that predisposed participants to hallucinations: overall lower prestimulus activity and a bias in the prestimulus activity patterns toward the to-be-detected (expected) grating. These results suggest that perceptual hallucinations may be due to an imprecise and biased state of sensory circuits preceding sensory evidence collection.

Significance statement: When sensory stimulation is strongly degraded, we occasionally misperceive a stimulus when only noise is present: a perceptual hallucination. Using fMRI in healthy participants, we investigated whether the state of early visual cortex preceding stimulus onset predisposes an observer to hallucinations. We found two characteristics of prestimulus activity that predisposed participants to hallucinations: overall lower prestimulus activity and a bias in the prestimulus activity patterns toward the expected grating. These results suggest that perceptual hallucinations are due to an imprecise and biased state of sensory circuits preceding sensation.

Keywords: expectation; fMRI; hallucination; perception; spontaneous fluctuations.

Figure 1.

A, Experimental paradigm. Each trial started with a cue indicating the beginning of the trial. On 80% of the trials, participants were presented with dynamic noise alone; on the remaining 20%, a Gabor pattern at detection threshold was embedded in the noise. Participants performed a detection task and were then asked to provide a confidence judgment about their answer. Crucially, participants were informed that Gabor orientation was constant within a block, promoting the formation of orientation-specific stimulus expectation. B, Mean proportion of correct (CRs and hits) and incorrect (FAs and misses) responses within signal absent (left) and signal present (right) trials. Error bars indicate SEM. Numbers above bars indicate the median number of trials across participants.

Figure 2.

A, Time course of BOLD signal in V1 time locked to onset of visual stimulus. Data were averaged across 19 participants. Error bars indicate SEM. B, Amplitude of BOLD activity in V1 voxels preferring the orientation displayed in the current block (filled bars) or the orthogonal orientation (hatched bars) separately for FAs, CRs, and hits during the first (t = −2 s, top panel) and second (t = 0 s, bottom panel) time points before stimulus onset (see x-axis on A). Error bars indicate SEM.