Corollary discharge dysfunction in schizophrenia: Can it explain auditory hallucinations?

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Abstract

Failure of corollary discharge, a mechanism for distinguishing self-generated from externally generated percepts, has been posited to underlie certain positive symptoms of schizophrenia, including auditory hallucinations. Although originally described in the visual system, corollary discharge may exist in the auditory system, whereby signals from motor speech commands prepare auditory cortex for self-generated speech. While associated with sensorimotor systems, it might also apply to inner speech or thought, regarded as our most complex motor act. In this paper, we describe the results of a series of studies in which we have shown that: (1) event-related brain potentials (ERPs) can be used to demonstrate the corollary discharge phenomenon during talking, (2) corollary discharge is abnormal in patients with schizophrenia, (3) EEG gamma band coherence between frontal and temporal lobes is greater during talking than listening and is disrupted by distorted feedback during talking in normals, and (4) patients with schizophrenia do not show this pattern for EEG gamma coherence. While these studies have identified ERPs and EEG gamma coherence indices of the efference copy/corollary discharge system and documented abnormalities in these systems in patients with schizophrenia, we have so far had limited success in establishing a relationship between these neurobiologic indicators of corollary discharge abnormality and reports of hallucinations in patients.

Introduction

Auditory hallucinations are a cardinal symptom of schizophrenia, occurring in about 75% of schizophrenic patients (Nayani and David, 1996). They are experienced as voices even though no one is speaking. With hemodynamic and electrophysiological brain imaging, we have the opportunity to understand the neural mechanisms underlying this perplexing symptom. One approach to understanding auditory hallucinations is “symptom capture”, a naturalist approach which attempts to image the brain, using electroencephalography (EEG), functional magnetic resonance imaging (fMRI), or positron emission tomography (PET), as patients are experiencing hallucinations. While this approach is conceptually simple, it is extremely difficult in practice because it relies not only on the timely occurrence of an illusive subjective experience but also on the ability of the patient to reliably report its initiation and completion. Symptom capture requires patience from the research team and cooperation and insight from the patient. Nevertheless, a number of investigators have used it successfully, variously reporting that auditory hallucinations are associated with activation of speech production areas (Dierks et al., 1999), primary (Dierks et al., 1999) and secondary auditory cortices, and various polymodal association cortices (Dierks et al., 1999, Shergill et al., 2000, Silbersweig and Stern, 1996).

A more mechanistic approach that does not rely on timing, patience, cooperation and endurance is the “fundamental deficit” approach (see Silbersweig and Stern, 1996). The first step in this approach is to identify a fundamental psychological mechanism that when disrupted could cause auditory hallucinations. The second step is to identify the neurobiological process underlying the psychological process, and the third step is to assess the integrity of this neurobiological mechanism. First, following a suggestion of Frith (1987), we identified the self-monitoring deficit as the fundamental dysfunctional psychological mechanism responsible for auditory hallucinations. The underlying assumption is that if voices that come from inside the head (i.e., thoughts) are not identified as self-generated through a failure of self-monitoring, they will be experienced as coming from an external source (i.e., hallucinations). Next, we adopted the proposal of Feinberg (1978) who suggested that self-monitoring deficits in schizophrenia reflect dysfunction of the efference copy/corollary discharge mechanism. Then we sought a neurobiological assay of this efference copy/corollary discharge mechanism. And finally, we attempted to relate abnormalities in this assay to auditory hallucinations.

Section snippets

Efference copy/corollary discharge

Von Holst and Mittelstaedt (1950) and Sperry (1950) suggested that motor actions are accompanied by an efference copy of the action which sends a “corollary discharge” signal to sensory cortex, signaling that impending sensations are self-initiated or self-generated. In the visual system, this system may serve to stabilize the visual image during eye movements, maintaining visuo-spatial constancy. In the somatosensory system, it may explain why we cannot tickle ourselves (Blakemore et al., 1998

Efference copy/corollary discharge in the auditory system

A similar mechanism may exist in the auditory system: corollary discharges from motor speech producing regions in the frontal lobes prepare the auditory cortex for perceiving resulting speech as self-generated (Creutzfeldt et al., 1989). Support for this mechanism comes from a study (Creutzfeldt et al., 1989) in which recordings were made during a pre-surgical planning procedure from the exposed surface of the right and left temporal cortices while patients talked and listened to others

Efference copy/corollary discharge in schizophrenia

These early studies of cortical activation and deactivation in monkey and human, using direct recordings of neuronal activity, are consistent with more recent, non-invasive, hemodynamic brain imaging studies. Studies of healthy volunteers comparing hemodynamic activation when subjects generate words to activation when they simply repeat words have shown that word generation results in relatively more activation of frontal lobe structures and relatively less activation (relative “deactivation”)

Subjects

Eight medicated patients with schizophrenia (DSM-IV (SCID1) (First et al., 1995) and 8 healthy adult comparison subjects (SCID screened for any significant history of Axis

Subjects

Data from 20 patients with schizophrenia (20 men, 1 woman) are added to the analysis described above.

Aim 5: relate efference copy/corollary discharge abnormalities in patients to auditory hallucinations

In the ERP experiment described above, for which we had only 8 subjects, we attempted to relate the severity of auditory hallucinations to the amplitude of N1 during talking and to the difference in N1 during talking and listening. We also classified patients as those with almost no experience of hallucinations and those who had moderately severe hallucinatory experiences. Neither approach produced relationships between hallucinations and our N1 measures of corollary discharge dysfunction.

In

Acknowledgements

Invited Keynote Lecture delivered at the 12th World Congress of Psychophysiology, The Olympics of the Brain, International Organization of Psychophysiology, associated with the United Nations (New York), September 18–23, 2004, Porto Carras, Halkidiki, Greece.

We acknowledge the help and support of our co-authors on the four papers summarized in this article: Max Gray, William O. Faustman, PhD, and Theda Heinks. We thank Mark Rothrock, MD for helping us recruit patient volunteers to our studies,

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