Elsevier

Biological Psychiatry

Volume 49, Issue 8, 15 April 2001, Pages 694-703
Biological Psychiatry

Original article
Altered hemispheric asymmetry of auditory magnetic fields to tones and syllables in schizophrenia

https://doi.org/10.1016/S0006-3223(00)01023-4Get rights and content

Abstract

Background: A growing body of literature suggests that schizophrenic patients often do not show the normal brain hemispheric asymmetry. We have found this for simple tones presented to the right ear in a previous study. In this study we extended this investigation to left ear stimulation and verbal stimuli.

Methods: With a whole-head neuromagnetometer, contra- and ipsilateral auditory-evoked magnetic fields in response to tones (1000 Hz) and to the syllables (“ba”) delivered to the left and right ears in separate runs were compared between schizophrenic patients (n = 17) and healthy control subjects (n = 15).

Results: In response to tones, all control subjects showed the expected asymmetry (contralateral predominance) of the auditory-evoked magnetic N100m (dipole moment). In the patient sample asymmetry was reversed following tones presented to the left ear in 47% and following tones to the right ear in 24%. In response to syllables, the asymmetry was similar between groups. In patients compared with control subjects the N100m was located more anterior without asymmetry between hemispheres.

Conclusions: Results suggest that deviation from the normal functional lateralization in schizophrenia appears in a proportion of patients at a basic stage of auditory processing, but may be compensated for at higher levels such as the processing of syllables.

Introduction

Many studies have shown an altered hemispheric asymmetry in schizophrenic patients in terms of structure and in terms of function Bilder et al 1999, DeLisi 1999, Flor-Henry 1989, Galderisi et al 1999, Pearlson and Marsh 1999, Rockstroh et al 1997. Morphometric data indicate reduced or reversed asymmetry, particularly of temporal lobe structures (i.e., planum temporale) of the left hemisphere Barta et al 1997, Falkai et al 1995, Petty et al 1995, a brain region strongly involved in language processing (Geschwind and Levitzky 1968). Nonetheless, gross structural deviations occur only in a minority of patients, which may be a result of different ways of assessing the anomalies. Moreover, the relation between structural deviations in cerebral asymmetry and functional lateralization is still unclear. Studies investigating functional lateralization complement structural findings and should validate hypotheses of abnormal asymmetry underlying basic schizophrenic symptoms, as postulated, for instance, by Crow 1990, Crow 1997a, Crow 1998). Alterations in the functional lateralization were, for instance, reported by Gur (1978), indicating a left hemispheric deficit when schizophrenic patients had to process visually presented syllables. In a magnetic resonance imaging (MRI) study, Woodruff and colleagues (Woodruff et al 1997) compared activation during listening to external speech with activation during blank intervals and found greater right temporal and less left posterior activation in schizophrenic patients relative to control subjects. However, other studies found normal patterns of functional asymmetry in schizophrenic patients during language processing Magaro and Chamrad 1983, Mohr et al in press. Noninvasive imaging techniques such as functional MRI, electroencephalography (EEG), and magnetoencephalography (MEG) have substantiated the knowledge of functional hemispheric asymmetry. In this respect, the auditory modality has been favored, as various acoustic stimuli elicit auditory-evoked magnetic fields (AEFs) in the supratemporal auditory cortex in the temporal lobes, which display distinct hemispheric asymmetries Makela et al 1993, Reite et al 1999. Lateralized AEFs have been found for the processing of tones Makela et al 1993, Pantev et al 1998 and phonetic stimuli Eulitz et al 1995, Gootjes et al 1999, with the larger evoked magnetic responses in temporal areas contralateral to the stimulated ear. In schizophrenic patients, MEG studies revealed reversed (Tiihonen et al 1998) or reduced Reite et al 1997, Reite et al 1999, Rockstroh et al 1998, Sauer et al 1998 functional asymmetry of the N100m, the magnetic auditory-evoked response peaking around 100 msec following monaural stimulation with simple tones. The commonly reported gender difference, with more pronounced functional hemispheric asymmetry in male subjects than in female subjects Geschwind and Levitsky 1968, Hellige 1993, Kanno et al 1998, Witelson and Kigar 1992, seems to affect the alteration of lateralization in schizophrenic patients. For instance, Reite and colleagues (Reite et al 1997) reported a reduced asymmetry of the N100m component only in male schizophrenic patients. Sauer and colleagues (Sauer et al 1998) found dipole deviations in the N100m in the left hemisphere for male subjects and in the right hemisphere for female subjects (see also Hajek et al 1997, Kreitschmann-Andermahr et al 1999).

Until now, studies with schizophrenic patients looking at hemispheric differences have been restricted to the level of simple tone processing. As language processing is known to be predominant in the left hemisphere in most right-handed healthy subjects and has been shown to evoke left lateralized brain responses in the N100m component in MEG (Rinne et al 1999), it is of interest to examine whether this is true also for schizophrenic patients. Theories of abnormal lateralization in schizophrenia are based on the assumption that language processes are involved in the development of laterality per se as well as in the development of schizophrenic disorders Crow 1997b, Crow et al 1989. Thus, language processes should be incorporated in experiments aiming at testing these theories. It still seems not sufficiently clear at which processing level altered asymmetry emerges in schizophrenia and for which processing levels or domains schizophrenic patients exhibit deviant or normal functional asymmetry. Is it only evident during passive processing of simple tones or is it also visible at higher processing stages like syllable processing or even word or sentence comprehension?

With this background, we examined hemispheric lateralization during a nonverbal (tone processing) and verbal (syllable processing) task. Auditory-evoked magnetic fields were measured in schizophrenic patients and healthy control subjects in response to tones and syllables delivered monaurally to the right or the left ear. These measurements should substantiate our previous results (Rockstroh et al 1998) and specify hemispheric asymmetry patterns in schizophrenic patients by looking at different processing levels including simple tones and acoustically more complex material like syllables.

Section snippets

Subjects

Seventeen inpatients (five female, mean age 32.2 ± 6.2 years, education 11.0 ± 2.4 years) of the university research ward at the local center of psychiatry were recruited for this study. Data of the patients were compared to those of 15 healthy subjects comparable to the patient group with respect to gender, age, and educational degree (six female, mean age 31.3 ± 5.8 years, education 11.6 ± 2.0 years). All subjects were paid (about $10) for participation in the experiment, which lasted for

Results

Figure 1 provides examples of typical auditory magnetic responses as evoked by tones and syllables in the ispilateral and contralateral hemisphere for two representative subjects, a schizophrenic patient and a control subject. Peaks around 100 msec following stimulus onset are evident for tones and syllables, as are differences in peak latencies between tones and syllables. Larger contralateral than ipsilateral amplitudes are more obvious at distinct sensors for the control subject than for the

Discussion

The two main goals of this study were 1) to substantiate the reduced hemispheric asymmetry of the AEFs to 1000-Hz tones in schizophrenic patients (Rockstroh et al 1998) by comparing right and left ear stimulation in a larger sample of patients and control subjects and 2) to explore the range of hemispheric asymmetry in schizophrenia by comparing laterality measures in response to simple tones and to verbal material (syllables).

Single ECDs could be fitted in all subjects and for all conditions.

Acknowledgements

Research was supported by the Deutsche Forschungsgemeinschaft (Ro 805/11) and the Volkswagen-Stiftung.

The authors gratefully acknowledge the assistance of Drs. H. Watzl and K. Pröpster in establishing the diagnostics and clinical status of the patients, and of Dr. E. Diesch and S. Heim inr generating the syllable stimuli.

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