Lack of asymmetrical transfer for linguistic stimuli in schizophrenia: an ERP study
Introduction
Differences in the structural asymmetry of language regions, especially lack of asymmetry of the planum temporale are often cited in schizophrenia (Petty et al., 1995, Barta et al., 1997, Saugstad, 1999, Shapleske et al., 1999). In accordance, behavioural studies commonly cite loss of the normal RVF/left hemisphere advantage for language in schizophrenia (Gur, 1978, Sommer et al., 2001). Characteristic language disturbances in schizophrenia include poverty of speech, poverty of content, repetition, illogicality, derailment, perseveration, and the use of neologisms (invented words) (Andreasen and Grove, 1986, Maher, 1991). Yet, while left hemisphere dysfunction may provide a parsimonious explanation for language symptoms in schizophrenia there are reports of normal left hemisphere lateralization of language in this population (Mohr et al., 2000, Mohr et al., 2001, Endrass et al., 2002).
Further evidence suggests that individuals with schizophrenia have difficulty integrating information between the hemispheres. There are reports of deficits when either the same (Mohr et al., 2000) or different stimuli (Beaumont and Dimond, 1973, Eaton et al., 1979) are presented to both hemispheres simultaneously. The accuracy advantage usually reported when stimuli are presented to both hemispheres simultaneously (bilateral gain) is not observed in schizophrenia (Mohr et al., 2000). (paragraph shortened).
Finally there is evidence to suggest that interhemispheric transfer times (IHTT) differ in schizophrenia. Evidence from both reaction time studies (Marzi et al., 1991) and visual evoked potentials (EPs) (Brown and Jeeves, 1993, Brown et al., 1994) finds that, in healthy controls, information transfer is faster from the right hemisphere to the left (R-to-L) than from the left to the right (L-to-R). There has been one previous study of IHTT in schizophrenia using a direct EP method. Endrass et al. (2002) used a lateralized lexical-decision task and presented words and non-words to the LVF or RVF, and measured IHTT using 65-channel EEG. While controls had significantly faster IHTT from the R-to-L hemisphere for words, this directional asymmetry was not present in the schizophrenia group. The lack of bilateral gain (Mohr et al., 2000) and the differences in IHTT (Endrass et al., 2002) in schizophrenia have been attributed to dysfunctional information transfer via the corpus callosum. In accordance meta-analysis finds an overall reduction in the area of the corpus callosum in schizophrenia (Woodruff et al., 1995).
Because callosal dysfunction should influence information transfer in both directions we suggest that impairments in callosal transfer may not provide the best explanation for differences interhemispheric transfer in schizophrenia. We suggest that asymmetry of transfer results from increased activation in the hemisphere that is the source of the faster transfer. Since most of the evidence suggests faster R-to-L transfer, this implies greater activation in the right hemisphere than the left. For this reason we suggest that right hemisphere dysfunction may give rise to differences in asymmetry of IHTT (faster R-to-L) in schizophrenia).
Miller (1996) argues that the right hemisphere has more myelinated axons specialised for rapid conduction and the processing of gestalts. Following Miller (1996), we suggest that the presence of more rapidly conducting cortico-cortical myelinated axons in the right hemisphere increases the likelihood of neural summation in that hemisphere, so increasing the speed of transfer from the R-to-L hemisphere relative to that from L-to-R. White matter enables corticocortical connectivity and information transfer and there is substantial evidence for white matter differences in schizophrenia. In fact, it has been suggested that myelination and white matter abnormalities may indicate a genetic marker for schizophrenia (Hakak et al., 2001, Hulshoff Pol et al., 2004a). White matter differences have been found in the right hemisphere of males with schizophrenia (Bullmore et al., 1995), especially those with negative symptoms (Wible et al., 2001).
We used 128-channel EEG to assess information transfer between the hemispheres in males with negative-symptom schizophrenia and hypothesise differences in IHTT asymmetry and right hemisphere activation. This study is basically a replication of that done by Endrass et al. (2002) with the specific aim of investigating the association between slowing of information transfer R-to-L and right hemisphere dysfunction. Participants performed a lateralized lexical-decision task while EEG was recorded continuously. Like Endrass et al. (2002) we recorded the N160 component from parietal regions, however, while they only assessed latency differences we also assessed amplitude differences between the groups. Previous reports have found the N160 to be pronounced in parietal regions (Brown and Jeeves, 1993, Brown et al., 1994, Endrass et al., 2002) and the N160 has previously been used to estimate IHTT in both letter-matching and linguistic tasks (Brown et al., 1994, Endrass et al., 2002).
Section snippets
Participants
Two groups (all males) were tested. Controls (N=12) had a mean age of 30.8 years (SD=6.9) and the schizophrenia group (N=12) a mean age of 31.8 years (SD=8.5). The Auckland District Health Board Ethics Committee approved this study and written informed consent was obtained. Controls were recruited from the University of Auckland and had no history of mental illness, neurological disorder, or drug and alcohol abuse. No control participant had a first-degree relative with schizophrenia.
Behavioural results: accuracy
There was no difference in accuracy between the two groups (P=.276) and no interactions involving group. Mean accuracy for controls was 75.4% (SD=8.9) and for the schizophrenia group 78.8% (SD=5.5). There was no main effect of visual field (P=.130), word (P=.299), however, there was a main effect of response hand (t(23)=2.772, P=.011) with participants making more correct responses when responding with the left hand (80%) than the right hand (77%). There was no interaction between field and
Discussion
Bilateral gain and IHTT were assessed in males with schizophrenia and controls matched for age and handedness. A lexical-decision task was used and words and non-words were presented to the LVF, RVF, or bilaterally, while 128-channel EEG was recorded. This was a complex task and while the schizophrenia group were not less accurate than controls, they were slower. Absence of bilateral gain for accuracy has been previously reported in schizophrenia using a RT task (Mohr et al., 2000). In
Acknowledgements
This study was supported by a research grant from the Schizophrenia Fellowship of New Zealand.
References (47)
- et al.
Differences in white matter connectivity in men and women with and without schizophrenia
Biol Psychiatry
(2000) - et al.
Corpus callosum and simple visuomotor integration
Neuropsychologia
(1995) - et al.
A preliminary comparison of flat affect schizophrenics and brain-damaged patients on measures of affective processing
J Commun Disord
(1989) - et al.
Bilateral visual field processing and evoked potential interhemispheric transmission time
Neuropsychologia
(1993) - et al.
Directional asymmetries in interhemispheric transmission time: evidence from visual evoked potentials
Neuropsychologia
(1994) Schizophrenia as a transcallosal misconnection syndrome
Schizophr Res
(1998)- et al.
Hemispheric dysfunction in schizophrenia: assessment by visual perception tasks
Psychiatr Res
(1979) - et al.
Emotional recognition via facial expression and affective prosody in schizophrenia: a methodological review
Clin Psychol Rev
(2002) - et al.
Reduced interhemispheric transmission in schizophrenia patients: evidence from event-related potentials
Neurosci Lett
(2002) - et al.
Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia
Biol Psychiatry
(2003)
Gray and white matter volume abnormalities in mono-zygotic and same-gender dizygotic twins discordant for schizophrenia
Biol Psychiatry
Focal white matter density changes in schizophrenia: reduced interhemispheric connectivity
Neuroimage
Differential activation of temporal cortex during sentence completion in schizophrenic patients with and without formal thought disorder
Schizophr Res
Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis
Neuropsychologia
Interhemispheric cooperation during word processing: evidence for callosal transfer dysfunction in schizophrenic patients
Schizophr Res
Functional asymmetry in schizophrenic patients during auditory speech processing
Schizophr Res
Schizophrenia—an emotional hypersensitivty of the right cerebral hemisphere
Int J Psychophysiol
The assessment and analysis of handedness: The Edinburgh inventory
Neuropsychologia
Schizophrenic patients and their first-degree relatives show an excess of mixed-handedness
Schizophr Res
A lack of cerebral lateralization in schizophrenia is within the normal variation in brain maturation but indicates late, slow maturation
Schizophr Res
The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance
Brain Res Rev
Recognition of facial expression and emotional prosody in schizophrenia
Biol Psychiatry
Increased duration of illness is associated with reduced volume in right medial temporal/anterior cingulate grey matter in patients with chronic schizophrenia
Schizophr Res
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