Background
Auditory verbal hallucinations (AVH) are one of the most prominent symptoms of schizophrenia but have also been reported in the general population. Several cognitive models have tried to elucidate the mechanism behind auditory verbal hallucinations, among which a top-down model. According to this model, perception is biased towards top-down information (e.g., expectations), reducing the influence of bottom-up information coming from the sense organs. This bias predisposes to false perceptions, i.e., hallucinations.
Methods
The current study investigated this hypothesis in non-psychotic individuals with frequent AVH, psychotic patients with AVH and healthy control subjects by applying a semantic top-down task. In this task, top-down processes are manipulated through the semantic context of a sentence. In addition, the association between hallucination proneness and semantic top-down errors was investigated.
Results
Non-psychotic individuals with AVH made significantly more top-down errors compared to healthy controls, while overall accuracy was similar. The number of top-down errors, corrected for overall accuracy, in the patient group was in between those of the other two groups and did not differ significantly from either the non-psychotic individuals with AVH or the healthy controls. The severity of hallucination proneness correlated with the number of top-down errors.
Discussion
These findings confirm that non-psychotic individuals with AVH are stronger influenced by top-down processing (i.e., perceptual expectations) than healthy controls. In contrast, our data suggest that in psychotic patients semantic expectations do not play a role in the etiology of AVH. This finding may point towards different cognitive mechanisms for pathological and nonpathological hallucinations.
Auditory verbal hallucinations (AVH) are among the most prominent symptoms of schizophrenia but have also been reported in other psychiatric disorders as well as in a significant minority of the general population (for reviews, see Beavan et al., 2011 and Aleman and Larøi, 2008). AVH have been suggested to lie on a continuum (Verdoux and van Os, 2002), ranging from non-psychotic and otherwise healthy individuals with AVH on one end to psychotic patients on the other. On the phenomenological level, some differences between AVH in these groups were reported, mostly related to the emotional valence and associated distress (Daalman et al., 2011a), but there is also a substantial overlap in AVH on both ends of this continuum: loudness, number of voices, personification and location of voices were rather similar.
On the neurobiological level, brain activation during AVH measured with fMRI was found to be similar in non-psychotic and psychotic individuals (Diederen et al., 2011). However, increased striatal dopamine, known to play a key role in AVH in psychosis, was absent in non-psychotic individuals with frequent AVH (Howes et al., 2012). It so far remains unclear if similar or different processes underlie hallucinations at either ends of the continuum.
Different cognitive models have tried to explain the mechanism(s) behind AVH. A possible mechanism accounting for the vulnerability to hallucinate is increased reliance on top-down processing. In normal perception, bottom-up information coming from the senses is combined with top-down information that regards implicit prior knowledge based on previously encountered situations, leading to perceptual expectations (Behrendt, 1998 and Meyer, 2011). The balance between bottom-up and top-down processing can be distorted in such a way, that it is influenced to a higher degree by top-down factors, which may trigger perceptual experiences in the absence of corresponding external stimulation, i.e., hallucinations (Behrendt, 1998 and Grossberg, 2000).
The aim of this study was to investigate whether both psychotic and non-psychotic individuals with AVH indeed make more top-down errors, compared to healthy controls. A previous study revealed an increased number of top-down errors in university students selected for hallucination-proneness compared to students without a proneness towards hallucination (Vercammen and Aleman, 2010). That is, subjects with higher levels of hallucination proneness were more likely to report hearing a word that fitted the sentence context, when it was not actually presented. The present study investigated whether such a finding would extend to a sample of people from the general population who experience AVH and to patients with schizophrenia and AVH. Investigating this effect in non-psychotic individuals with AVH as well as in patients with AVH would provide further evidence for the top-down model in AVH. To this end, three groups of participants were included: 40 healthy control subjects, 40 non-psychotic individuals with AVH and 40 psychotic patients with AVH. Patients are hypothesized to make more top-down errors than non-psychotic individuals with AVH, since they experience AVH more frequently (Daalman et al., 2011a). In addition, the Launay-Slade Hallucination Scale (LSHS; Larøi et al., 2004) was used to measure whether hallucination proneness would be associated with more top-down errors in the non-psychotic groups. For the patient group, the association between number of top-down errors and hallucinatory behavior (item P3 of the Positive and Negative Syndrome Scale; PANSS, Kay et al., 1987) was determined.
