Attentional modulation of external speech attribution in patients with hallucinations and delusions

Abstract

A range of psychological theories have been proposed to account for the experience of auditory hallucinations and delusions in schizophrenic patients. Most influential theories are those implicating the defective self-monitoring of inner speech. Some recent studies measured response bias independently of self-monitoring and found the results inconsistent with the defective self-monitoring model, but explained by an externalizing response bias. We aimed to investigate the role of attentional bias in external misattribution of source by modulating participant's endogenous expectancies. Comparisons were made between patients with paranoid schizophrenia (N = 23) and matched healthy controls (N = 23) who participated in two different versions of an audio–visual task, which differed based upon level of the cue predictiveness. The acoustic characteristic of voice was altered in half of the trials by shifting the pitch (distortion). Participants passively listened to recordings of single adjectives spoken in their own and another person's voice (alien) preceded by their own or another person's (alien) face and made self/non self judgments about the source. The patients showed increased error rates comparing to controls, when listening to the distorted self spoken words, misidentifying their own speech as produced by others. Importantly, patients made significantly more errors across all the invalid cue conditions. This suggests not only the presence of pathological misattribution bias, but also an inadequate balance between top-down and bottom-up attentional processes in the patients, which could be responsible for misattribution of the ambiguous sensory material.

Introduction

Auditory verbal hallucinations (AVH) are one of the most common symptoms experienced by patients with schizophrenia (Slade & Bentall, 1988) and are usually associated with delusions (Liddle, 1987). A range of cognitive models have been proposed to account for AVH and delusions in schizophrenic patients (Allen et al., 2007, Seal et al., 2004). One such model proposes that AVH arise because of the defective monitoring of inner speech (Frith, 1987, Frith, 1992). According to this model AVH result from defective monitoring of thoughts/inner speech, as they are generated, leading to misidentification of self-generated thoughts as external ‚alien’ voices. Frith's model is supported by data from studies that have engaged verbal self-monitoring by experimentally manipulating auditory verbal feedback while patients with AVH spoke aloud (Cahill et al., 1996, Johns et al., 2001). Altering the acoustic characteristics of their speech introduced a disparity between what subjects expected to hear and what they actually perceived. In both studies patients with hallucinations and delusions were more likely than controls to make misattribution errors and misidentify their own speech as alien when it is distorted. However, a later study found that the misattribution of self speech to an external source was not specific to patients with AVH and that patients with delusions but no hallucinations also demonstrate a significant tendency to misattribute their own speech (Johns, Gregg, Allen, & McGuire, 2006). The specificity of such a deficit to AVH is therefore equivocal as most studies report that patients with delusions also tend to make external misattributions when listening to their own distorted speech (Allen et al., 2007). However, the tendency to make misattribution errors in patients currently experiencing AVH in the context of an affective psychosis was not identical to the one that was seen in patients experiencing AVH in the context of schizophrenia. Namely, they did not misattribute their own speech when it was distorted, but they tended to be unsure about the speech source. Hence, the misattribution bias was not observed in patients who had a history of hallucinations but were hallucination-free for a month.

It has also been suggested that positive symptoms, e.g. hallucinations and delusions, are related to a deficit in reality and/or source monitoring leading to confusion between imagined and perceived items (Bentall et al., 1991, Blakemore et al., 2000, Blakemore et al., 2002, Brébion et al., 2000). Much of the experimental evidence is consistent with this idea as patients with hallucinations and delusions (H/D patients) in general tend to misattribute items they produced themselves to an external source on a variety of experimental tasks (Allen et al., 2004, Bentall et al., 1991, Bentall et al., 1994, Brébion et al., 2000, Brébion et al., 2002, Brébion et al., 1997, Johns et al., 2001, Johns et al., 2006). Allen et al. (2004) adapted the paradigm used by Johns et al., 2001, Johns et al., 2006, such that participants made judgments about the source of pre-recorded speech rather than speech that was generated online. As participants were simply required to indicate when they recognized their own voice, the putative self-monitoring of self-generated speech was bypassed. Despite this H/D patients were still more likely to claim their own distorted voice was that of another person than patients without hallucinations (and significantly lower levels of delusions) and healthy volunteers. This finding suggests that the external misattribution of source may reflect impairment in not only verbal self-monitoring, but also in the appraisal of ambiguous sensory material (Allen et al., 2007). Recent event-related brain potentials studies (Ford and Mathalon, 2005, Maldonado-Heinks et al., 2007) found that hallucinators performed poorly both during self-monitoring their own speech and when the putative self-monitoring of self-generated speech was bypassed. Thus they suggested that the self-monitoring of speech may have failed to develop appropriately resulting in uncertainty about the source of current perceptions. According to these studies, misattributions therefore may result from a “coping” strategy learned over time to navigate through life.

We argue that misattribution of speech in patients with positive symptoms suggests more than a “coping strategy”. It is our view that impairment of attention, that has been cited as a fundamental clinical feature of schizophrenia (Kraepelin, 1919, Posner et al., 1988) plays an important role in the misattribution of external speech in patients with positive symptoms. Abnormalities of visual (Danckert et al., 2003, Maruff et al., 1998, Sereno and Holzman, 1996) and auditory (Mathalon et al., 2004) attention processing are frequently reported in patients with schizophrenia. In particular, attention deficit had been previously shown to correlate with positive symptoms of schizophrenia (Rocca et al., 2006). Specifically, cognitive deficits in both bottom-up and top-down processing have been reported in patients with schizophrenia (Fuller et al., 2006, Gold et al., 2007).

Interestingly, the neural deficits underlying impaired cognitive performance support bottom-up dysregulation more than the top-down cortical dysregulation (Butler et al., 2007, Leavitt et al., 2007). Bottom-up or exogenous attentional control is stimulus driven, i.e. attention is spontaneously oriented towards an oncoming stimulus. Top-down or endogenous control, by contrast, is intentionally and cognitively driven, i.e. directed by knowledge, expectation and current goals (Desimone and Duncan, 1995, Egeth and Yantis, 1997). Importantly, top-down and bottom-up processes represent overlapping organizational principles rather than dichotomous constructs, and in most situations, top-down and bottom-up processes interact to optimize attentional performance (Sarter, Givens, & Bruno, 2001). Deficits in magnocelullar visual processing in schizophrenia suggest a dysfunction even within the early regions of the visual pathway, which may lead to bottom-up driven dysregulation of higher cortical function (Butler et al., 2007). A recent study in auditory processing in schizophrenia reflects analogous findings that the earliest afferent input to the primary auditory cortex, which arrives from subcortical regions, already show evidence of dysfunction in patients with schizophrenia consistent with a bottom-up model of auditory processing deficits (Leavitt et al., 2007). Although there have been few investigations of top-down and bottom-up attentional processes in patients with positive symptoms, one study by Aleman, Böcker, Hijman, De Haan, and Kahn (2003) observed a correlation between the severity of hallucination ratings and top-down influences on auditory perception. This is consistent with the notion that hallucinations may result from an increased influence of top-down sensory expectations on conscious perception (Aleman et al., 2003). It has been also shown in previous studies that when bottom-up and top-down processes conflict, patients with schizophrenia exhibit significantly worse performance than healthy controls (Maruff et al., 1998).

The aim of the present study is to examine the effect of attentional modulation on source decisions for pre-recorded speech in patients with schizophrenia and in healthy control group. In the previous versions of the paradigm (Allen et al., 2004, Johns et al., 2001) distortion of participant's voice was used to manipulate what they expected to hear and what they actually perceived. As well as distortion of participants voice we also manipulated the validity of cues in a speech appraisal task (Allen et al., 2004) in order to modulate the participant's expectancies about the source of speech that they heard.

Our hypothesis were:

• when top-down (cue preceding the voice stimuli) and bottom-up (source of the voice stimuli) mechanisms are placed in conflict (e.g. during invalid trials) patients with hallucinations and delusion will demonstrate impaired performance relative to controls. This is because patients with hallucinations and delusions are allowing top-down information to guide them at the expense of bottom-up information,

• the patients will demonstrate a significant externalizing response bias (misidentifying their own speech as alien) that will be particularly evident on invalid cue trials when their own voice is preceded by an alien cue. Misattribution errors should be more evident in the predictive cue condition (80% valid cues and 20% invalid cues), as the high informative power of the cue should guide source attributions stronger than the unpredictive cue condition (50% valid cues and 50% invalid cues),

• finally, in the patient group, errors associated with invalid trials should correlate with severity of positive symptoms.