Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study
Introduction
The left superior temporal gyrus (STG) is believed to be a major anatomical substrate for speech, language and communication. The primary auditory cortex, corresponding to Brodmann areas 41 and 42, lies in Heschl's gyrus and is located in the middle and anterior part of the STG. The auditory association areas corresponding to Brodmann area 22, including planum temporale, lie posteriorly behind and surrounding Heschl's gyrus. Neuropathological injuries to this area due to strokes, tumors, epilepsy or stimulation produce disturbances of language function and hallucinations similar to some of the symptoms of schizophrenia. Although schizophrenia clearly is a disease of a widespread neural network or neurochemical system, (Buchsbaum, 1990, Tandon et al., 1998), significant evidence has accumulated over the past decade indicating a role of the STG in the pathophysiology of some symptoms of schizophrenia. It also seems certain that an abnormal STG alone cannot explain the schizophrenia syndrome, as several other structural abnormalities have been associated with the illness (Shenton et al., 1997).
A number of neuroimaging studies conducted in the past decade have found that the left STG is smaller in patients with schizophrenia than in normal controls. Additionally, some studies have noted a negative correlation between the left STG volume and the severity of hallucinations and/or thought disorder. Barta et al. (1990) first reported a volume reduction of the left anterior and middle STG in patients with schizophrenia and found a negative correlation between left anterior STG volume and auditory hallucinations. Shenton et al. (1992) reported reduced volume of the left posterior STG gray matter that negatively correlated with the severity of thought disorder. Since then, several other studies have replicated these findings; Table 1 summarizes the studies and findings. The volume loss in STG appears to be disease specific and not related to antipsychotic treatment (Barta et al., 1997, Hirayasu et al., 1998, Keshavan et al., 1998, Pearlson et al., 1997). Although volume loss of the STG in schizophrenia is fairly well replicated in findings in schizophrenia research, some studies have found no significant volume difference between patients and controls. One of the explanations for this discrepancy is differences in methodology, i.e. the type of image sequence, neuroanatomic definition of STG, method used to trace the STG (gray matter versus gray and white matter). It is also unclear how the heterogeneity of the schizophrenia syndrome, normal variations in the distribution of auditory cortex and histological subdivision of STG contribute to this inconsistency.
The STG has wide connections to temporo-limbic areas (including hippocampus, amygdala and entorhinal cortex), neocortical association areas in prefrontal and parietal cortices, and thalamus. In a detailed review of the anatomy of the auditory cortex, Pandya (1995) noted that these connections follow positional and architectonic (tissue type) organization. He reports that the rostral, caudal and middle thirds of the STG are connected to the orbital medial prefrontal cortex (PFC), caudal PFC, and lateral PFC respectively. The thalamic connections also follow architectonic principles, and primary auditory cortex preferentially projects to the ventral subdivision of the medial geniculate nucleus whereas other fibers project widely.
The implications of this differentiated tissue organization and the reciprocal connections are unknown, and the role of this region in the function of speech, memory, and interpretation and association of language is not fully understood. However, the wide and complex connections seem to integrate the above-mentioned brain regions. The primary auditory cortex may play a role in the discrimination, interpretation, or self-monitoring of auditory input, both internal and external (McGuire et al., 1996, Pandya, 1995). The auditory association areas, on the other hand, may be involved in integrating the auditory or language input with stored memory, and other somatosensory input.
In this study, we attempted to divide the STG into three parts in conjunction with the above histological and neural network difference of its subdivisions. We hypothesized the following: (i) the left STG will be smaller in patients than in normal controls; (ii) the volume of the middle and anterior parts of the STG would correlate negatively with hallucinations; (iii) the volume of posterior STG would negatively correlate with thought disorder.
Section snippets
Subjects
20 male patients suffering from schizophrenia (DSM III R) and twenty age matched (by ±2 years) male normal controls were studied. The patients and controls were chosen from a pool of research subjects from our database on the basis of completeness of data, imaging sequence and the ability to match on age and gender. None of the subjects (patients and controls) had any past or present neurological illness, head trauma, chronic medical illness or significant history of substance abuse. The
Results
The patients and controls were age matched and all male. The mean age of the patient group was 33.5±12.7 years (±SD), and control group was 33.9±12.6; there was no significant difference between groups. The patients with schizophrenia and control subjects did not significantly differ in handedness ratio: controls 16 right (80%), four left (20%); patients 17 (85%) right, three (15%) left. Patients and controls also did not differ on the number of slices per region of interest for any MRI measure
Discussion
Our data indicate that left anterior STG is smaller in the patient group than normal controls. Among patients, left anterior STG volume correlates negatively with the severity of hallucinations. The volume of the left posterior STG, though not smaller than normal controls, correlates negatively with the severity of thought disorder. We also found that the left anterior STG is smaller than the right among the patients but not in controls. Our findings are in agreement with the majority of
Conclusion
In conclusion, our data emphasize the involvement of the left STG in hallucinations and thought disorder of schizophrenia. This study supports the notion that the left anterior STG, consisting of primary auditory cortex, could be involved in production of hallucinations and the posterior STG, composed in large part of the auditory association cortex, may play a role in the pathophysiology of thought disorder. Although this might explain a piece of the ‘schizophrenia puzzle’, a comprehensive
Acknowledgements
Supported in part by National Alliance for Research on Schizophrenia and Depression (NARSAD) Grant (J.R.D).
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