Article

Synch Before You Speak: Auditory Hallucinations in Schizophrenia

Stanford University, Palo Alto, California, United States
American Journal of Psychiatry (Impact Factor: 13.56). 04/2007; 164(3):458-66. DOI: 10.1176/appi.ajp.164.3.458
Source: PubMed

ABSTRACT Synchronization of neural activity preceding self-generated actions may reflect the operation of the forward model, which acts to dampen sensations resulting from those actions. If this is true, pre-action synchrony should be related to subsequent sensory suppression. Deficits in this mechanism may be characteristic of schizophrenia and related to positive symptoms, such as auditory hallucinations. If so, schizophrenia patients should have reduced neural synchrony preceding movements, especially patients with severe hallucinations.
In 24 patients with schizophrenia or schizoaffective disorder and 25 healthy comparison subjects, the authors related prespeech neural synchrony to subsequent auditory cortical responsiveness to the spoken sound, compared prespeech neural synchrony in schizophrenia patients and healthy comparison subjects, and related prespeech neural synchrony to auditory hallucination severity in patients. To assess neural synchrony, phase coherence of single-trial EEG preceding talking was calculated at a single site across repeated trials. To assess auditory cortical suppression, the N1 event-related brain potentials to speech sound onset during talking and listening were compared.
In healthy comparison subjects, prespeech neural synchrony was related to subsequent suppression of responsiveness to the spoken sound, as reflected in reduction of N1 during talking relative to listening. There was greater prespeech synchrony in comparison subjects than in patients, especially those with severe auditory hallucinations.
These data suggest that EEG synchrony preceding speech reflects the action of a forward model system, which dampens auditory responsiveness to self-generated speech and is deficient in patients who hallucinate.

Download full-text

Full-text

Available from: Daniel H Mathalon, Aug 29, 2015
0 Followers
 · 
152 Views
  • Source
    • "They have been related to several brain functions, such as perception, attention, memory, consciousness and synaptic plasticity (Uhlhaas et al 2008). In agreement with previous studies, our findings suggest that SCH patients decrease their γ-coupling activity between response and baseline (Slewa-Younan et al 2004), whereas controls exhibit a γ-coupling increase (Ford et al 2007). Abnormal γ-band activity has also been related to disturbed corollary modulation of sensory processes (Uhlhaas et al 2008). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Objective. The aim of this research is to explore the coupling patterns of brain dynamics during an auditory oddball task in schizophrenia (SCH). Approach. Event-related electroencephalographic (ERP) activity was recorded from 20 SCH patients and 20 healthy controls. The coupling changes between auditory response and pre-stimulus baseline were calculated in conventional EEG frequency bands (theta, alpha, beta-1, beta-2 and gamma), using three coupling measures: coherence, phase-locking value and Euclidean distance. Main results. Our results showed a statistically significant increase from baseline to response in theta coupling and a statistically significant decrease in beta-2 coupling in controls. No statistically significant changes were observed in SCH patients. Significance. Our findings support the aberrant salience hypothesis, since SCH patients failed to change their coupling dynamics between stimulus response and baseline when performing an auditory cognitive task. This result may reflect an impaired communication among neural areas, which may be related to abnormal cognitive functions.
    Journal of Neural Engineering 12/2014; 12(1):016007. DOI:10.1088/1741-2560/12/1/016007 · 3.42 Impact Factor
  • Source
    • "Functional neural networks, such as the language processing network, are mostly investigated using two different approaches: (1) through assessment of activity patterns during experimental tasks (Meyer-Lindenberg et al., 2001; Lawrie et al., 2002; Calhoun et al., 2004; Ford et al., 2007; Garrity et al., 2007) or (2) through restingstate functional imaging (e.g. resting-state fMRI). "
    [Show abstract] [Hide abstract]
    ABSTRACT: We have previously reported altered functional asymmetry of the primary auditory cortex (Heschl's gyrus) of patients with schizophrenia (SZ) and their relatives during auditory processing. In this study, we investigated whether schizophrenia patients have altered intrinsic functional organization of Heschl's gyrus (HG) during rest. Using functional magnetic resonance imaging (fMRI), we measured functional connectivity between bilateral HG and the whole brain in 24 SZ patients, 22 unaffected first-degree relatives and 24 matched healthy controls.SZ patients and relatives showed altered functional asymmetry in HG and altered connectivity between temporal and limbic areas in the auditory network during resting-state in comparison with healthy controls. These changes in functional connectivity correlated with predisposition towards hallucinations in patients and relatives and with acute positive symptoms in patients.The results are in line with the results from task-related and symptom-mapping studies that investigated the neural correlates of positive symptoms, and suggest that individual psychopathology is associated with aberrant intrinsic organization of auditory regions in schizophrenia. This might be evidence that reduced hemispheric lateralization and reduced functional connectivity of the auditory network are trait markers of schizophrenia.
    Schizophrenia Research 11/2014; 160(1-3). DOI:10.1016/j.schres.2014.10.036 · 4.43 Impact Factor
  • Source
    • "A primary aim of this research was to test the predictions of the comparator account as it applied to misattributed inner speech. Overall, the results have been interpreted as suggesting that inner speech is normally attenuated, and that there is a failure of attenuation of inner speech in patients with a diagnosis of schizophrenia (Ford et al., 2001a,b,c, 2007; Ford and Mathalon, 2004, 2005, 2012; Heinks-Maldonado et al., 2007). As such, the results appear to provide key evidence in favor of the current comparator account of misattributed inner speech. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The comparator account holds that processes of motor prediction contribute to the sense of agency by attenuating incoming sensory information and that disruptions to this process contribute to misattributions of agency in schizophrenia. Over the last 25 years this simple and powerful model has gained widespread support not only as it relates to bodily actions but also as an account of misattributions of agency for inner speech, potentially explaining the etiology of auditory verbal hallucination (AVH). In this paper we provide a detailed analysis of the traditional comparator account for inner speech, pointing out serious problems with the specification of inner speech on which it is based and highlighting inconsistencies in the interpretation of the electrophysiological evidence commonly cited in its favor. In light of these analyses we propose a new comparator account of misattributed inner speech. The new account follows leading models of motor imagery in proposing that inner speech is not attenuated by motor prediction, but rather derived directly from it. We describe how failures of motor prediction would therefore directly affect the phenomenology of inner speech and trigger a mismatch in the comparison between motor prediction and motor intention, contributing to abnormal feelings of agency. We argue that the new account fits with the emerging phenomenological evidence that AVHs are both distinct from ordinary inner speech and heterogeneous. Finally, we explore the possibility that the new comparator account may extend to explain disruptions across a range of imagistic modalities, and outline avenues for future research.
    Frontiers in Human Neuroscience 08/2014; 8:675. DOI:10.3389/fnhum.2014.00675 · 2.90 Impact Factor
Show more