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Pavlovian conditioning-induced hallucinations result from overweighting of perceptual priors.

Powers AR, Mathys C, Corlett PR
Science. 2017 Aug 11; 357(6351):596-600. PMID: 28798131. Pubmed

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Submitted by Kenneth Hugdahl on

An often replicated finding in psychology is that what we see and hear of the world around us is colored by what we expect to see and hear, such that the actual perception of an object or a sound is the combination of the sensory input and our stored memories and prior expectations. Another way of expressing this is to say that our perceptions are the sum of bottom-up sensory input and top-down cognitive modulations. In perceptual and cognitive psychology, the expectations that people carry with them and which shape their perceptions are called “priors,” which can be more or less salient. Perceptual errors, like visual illusions, may then be seen as a mismatch between the sensory input and these “priors,” for example, the illusion that the fishing rod is broken if it is dipped into the water.

In their study of hallucinations, Powers et al. found that strong “priors” can induce beliefs about perceptual experience in the absence of a corresponding sensory input. In other words, strong priors can induce a conviction that a perceptual experience has an external cause, although there is none, as when individuals are convinced that they “hear a voice” although there is no one speaking to them. This is an auditory hallucination, and one of the most debilitating symptoms in schizophrenia. The advent of modern brain imaging techniques, and especially functional magnetic resonance imaging (fMRI), made it possible to record blood flow in the brain when subjects solved various cognitive tasks, or when they were hallucinating (see Kompus et al., 2011; Hugdahl, 2015; Sommer et al., 2008). A typical brain activation pattern in the temporal lobe language area during auditory hallucinations is seen in Figure 1.

Auditory Cortex 250

Although previous fMRI studies have shown how the brain is involved in hallucinations, it has not been known how the brain constructs such non-real percepts, and if they are caused by misinterpreted inner speech or by a perceptual mismatch between bottom-up perceptual and top-down cognitive influences.

The study by Powers et al. is, in this respect, an important contribution to a better understanding of the underlying mechanisms, with implications for more individualized treatments. The authors recruited four groups: patients with a diagnosis of psychosis who experienced “hearing voices”; patients who did not have such experiences; individuals without a diagnosis who “heard voices”; and individuals without a diagnosis who did not hear voices. In order to reveal the effect of priors on hallucinatory experiences, Powers et al. used an ingenious experimental paradigm based on Pavlovian, or classical, conditioning where they paired weak tones at sensory threshold concurrent on the presentation of a visual stimulus while they recorded blood flow changes in the brain with fMRI. Pairing the tones and the visual stimuli would then establish a conditioned, or learned, association between the two stimulus events. They then sometimes presented only the visual stimulus, and sometimes together with tones that were so weak that they could not be heard, and tested whether the subjects nevertheless believed that they had perceived a tone. If the subjects responded that they heard a tone and described how convinced they were, this constituted the foundation for the experience of an auditory hallucination (in the absence of a real perceptual stimulus).

The results showed that subjects in the groups that had previous experiences of auditory hallucinations, independent of a diagnosis, more often reported that they heard a tone, and were more convinced than the other two groups of their experience, and their brain responses also showed activation in networks that have previously been found in hallucinating individuals (see Figure 2 of Powers et al.). Thus, the results of the study by Powers et al. show how prior beliefs and expectations of a perceptual phenomenon, in this case an audio-visual association, can cause the experience of actually “hearing a voice” that does not exist. In this respect, the results also shed light on the ongoing discussion of theoretical models for auditory hallucinations, by providing strong arguments for the perceptual nature of the very strange phenomenon of being convinced of experiencing something that is simply not there.