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Supporting Evidence: New Research
Supporting Jaynes' Bicameral Mind Theory

Jaynes's Neurological Model: Neuroimaging of Auditory Hallucinations

Supporting Evidence > Jaynes's Neurological Model

In his theory, Julian Jaynes describes the role hallucinations played in an earlier mentality called the bicameral mind, prior to the development of subjective consciousness. Jaynes's neurological model for the bicameral mind predicts that auditory hallucinations would be generated by the language areas in the right temporal lobe and be "heard" or processed by the left. This prediction has been now been verified as accurate by numerous studies. Jaynes was not only correct about the neurology of auditory hallucinations, but decades ahead of his time. Below is a small sample of research supporting this aspect of Jaynes's theory (highlighted text calls attention to areas of the right hemisphere that Jaynes predicted would play a role in hallucinations).

Auditory Hallucinations Cerebral Activity Associated with Auditory Verbal Hallucinations: A Functional Magnetic Resonance Imaging Case Study
Bentaleb, L.A., M. Beauregard, P. Liddle, E. Stip. Journal of Psychiatry & Neuroscience, 2002, 27 (2), 110.
Among the many theories that have been advanced to explain the mechanism by which auditory verbal hallucinations (AVH) arise, 2 that have received a degree of empirical support are: the hypothesis that AVHs arise from misinterpreted inner speech and the proposal that they arise from aberrant activation of the primary auditory cortex. To test these hypotheses, we were fortunate to be able to study the interesting and rare case of a woman with schizophrenia who experienced continuous AVH which disappeared when she listened to loud external speech. Functional magnetic resonance imaging (fMRI) was used to measure the patient's brain activity in the temporal and inferior frontal regions during the AVHs and while the she was listening to external speech. The brain activity of a matched control subject was also recorded under the same experimental conditions. AVHs were associated with increased metabolic activity in the left primary auditory cortex and the right middle temporal gyrus. Our results suggest a possible interaction between these areas during AVHs and also that the hypotheses of defective internal monitoring and aberrant activation are not mutually exclusive. Potential limitations to the generalization of our results are discussed.

Cerebral Lateralization is Delayed in Children who Later Develop Schizophrenia
Crow, T.J., D.J. Done, A. Sacker. Schizophrenia Research, 1996, Vol. 22 (3): 181–185.
The origins of schizophrenia are obscure. One suggestion is that it represents a component of the genetic variation associated with the establishment of dominance in one or other cerebral hemisphere, a mechanism that has been crucial in the evolution of language. Indices of cerebral hemispheric dominance (hand, foot and eye preference, speed of checking squares) recorded on the 16 980 children in the UK National Child Development Study cohort were examined in relation to psychiatric admission by the age of 28 years. Diagnoses were established by the application of Present State Examination criteria to case notes. Pre-schizophrenic children (n = 34-36) were more likely (p < 0.0003 ) to be rated by their mothers as ambidextrous at the age of 7 years, and at 11 years were less (p < 0.01) strongly right-handed than their peers in the cohort population on a test of relative hand skill: children who later developed affective psychosis (n=25) or neurosis (n=60) did not differ significantly from controls. Delay in establishing dominance in one hemisphere could be the critical factor that predisposes to schizophrenia.

Activation of Bilateral Auditory Cortex during Verbal Hallucinations in a Child with Schizophrenia
Hoffman, R.E., B. Pittman, R.T. Constable, Z. Bhagwagar and M. Hampson. The British Journal of Psychiatry, 2011, 198 (4): 277–283.
Background: The pathophysiology of auditory verbal hallucinations remains poorly understood. Aims: To characterise the time course of regional brain activity leading to auditory verbal hallucinations. Method: During functional magnetic resonance imaging, 11 patients with schizophrenia or schizoaffective disorder signalled auditory verbal hallucination events by pressing a button. To control for effects of motor behaviour, regional activity associated with hallucination events was scaled against corresponding activity arising from random button-presses produced by 10 patients who did not experience hallucinations. Results: Immediately prior to the hallucinations, motor-adjusted activity in the left inferior frontal gyrus was significantly greater than corresponding activity in the right inferior frontal gyrus. In contrast, motor-adjusted activity in a right posterior temporal region overshadowed corresponding activity in the left homologous temporal region. Robustly elevated motor-adjusted activity in the left temporal region associated with auditory verbal hallucinations was also detected, but only subsequent to hallucination events. At the earliest time shift studied, the correlation between left inferior frontal gyrus and right temporal activity was significantly higher for the hallucination group compared with non-hallucinating patients. Conclusions: Findings suggest that heightened functional coupling between the left inferior frontal gyrus and right temporal regions leads to coactivation in these speech processing regions that is hallucinogenic. Delayed left temporal activation may reflect impaired corollary discharge contributing to source misattribution of resulting verbal images.

Activation of Bilateral Auditory Cortex during Verbal Hallucinations in a Child with Schizophrenia
Jardri, R., D. Pins, C. Delmaire, J-L. Goeb1, and P. Thomas. Molecular Psychiatry, 2007, 12: 319.
We used functional MRI to evidence neural substrates of verbal auditory hallucinations in a child suffering from very early onset schizophrenia. The data-driven analysis performed shows bilateral activation of the superior temporal gyri predominantly on the left hemisphere.

Functional MRI of Verbal Self-Monitoring in Schizophrenia
Kumari, V., D. Fannon, D.H. ffytche, V. Raveendran, E. Antonova, et al. Schizophrenia Bulletin, Nov. 7 2008.
Previous small-sample studies have shown altered frontotemporal activity in schizophrenia patients with auditory hallucinations and impaired monitoring of self-generated speech. We examined a large cohort of patients with schizophrenia (n = 63) and a representative group of healthy controls (n = 20) to disentangle performance, illness, and symptom-related effects in functional magnetic resonance imaging–detected brain abnormalities during monitoring of self- and externally generated speech in schizophrenia. Our results revealed activation of the thalamus (medial geniculate nucleus, MGN) and frontotemporal regions with accurate monitoring across all participants. Less activation of the thalamus (MGN, pulvinar) and superior-middle temporal and inferior frontal gyri occurred in poorly performing patients (1 standard deviation below controls' mean; n = 36), relative to the combined group of controls and well-performing patients. In patients, (1) greater deactivation of the ventral striatum and hypothalamus to own voice, combined with nonsignificant activation of the same regions to others' voice, associated positively with negative symptoms (blunted affect, emotional withdrawal, poor rapport, passive social avoidance) regardless of performance and (2) exaggerated activation of the right superior-middle temporal gyrus during undistorted, relative to distorted, feedback associated with both positive symptoms (hallucinations, persecution) and poor performance. A further thalamic abnormality characterized schizophrenia patients regardless of performance and symptoms. We conclude that hypoactivation of a neural network comprised of the thalamus and frontotemporal regions underlies impaired speech monitoring in schizophrenia. Positive symptoms and poor monitoring share a common activation abnormality in the right superior temporal gyrus during processing of degraded speech. Altered striatal and hypothalamic modulation to own and others’ voice characterizes emotionally withdrawn and socially avoidant patients.

Spatial and Temporal Mapping Auditory Hallucinations Spatial and Temporal Mapping of Neural Activity Associated with Auditory Hallucinations
Lennox B.R., S. Bert, G. Park, P.B. Jones, P.G. Morris. Lancet, 1999, Vol. 353: 644.
This study examined a 26-year-old, right-handed male that had been suffering from paranoid schizophrenia for 8 years. The patient pressed a button at the onset of a hallucination, and magnetic resonance imaging (MRI) was used to scan his brain, showing the areas of activity during his hallucinations. Results showed that activation first appeared in the right middle temporal gyrus and then extended to a wider area of the right superior temporal and left superior temporal gyri (where the hallucination is "heard"), right middle and inferior frontal gyri, right anterior cingulate, and right cuncus.

The Functional Anatomy of Auditory Hallucinations in Schizophrenia
Lennox B.R., S.B. Park, I. Medley, P.G. Morris, P.B. Jones. Psychiatry Research, November 2000, 100 (1): 13-20.
"We used continuous whole brain functional magnetic resonance imaging (fMRI) with a 3-T magnet to map the cerebral activation associated with auditory hallucinations in four subjects with schizophrenia. The subjects experienced episodes of hallucination whilst in the scanner so that periods of hallucination could be compared with periods of rest in the same individuals. Group analysis demonstrated shared areas of activation in right and left superior temporal gyri, left inferior parietal cortex and left middle frontal gyrus. When the data were examined on an individual basis, the temporal cortex and prefrontal cortex areas were activated during episodes of hallucination in all four subjects. These findings support the theory that auditory hallucination reflects abnormal activation of normal auditory pathways."

The Brain's Voices: Comparing Nonclinical Auditory Hallucinations and Imagery
Linden, David E.J., Katy Thornton, Carissa N. Kuswanto, Stephen J. Johnston, Vincent van de Ven and Michael C. Jackson. Cerebral Cortex, 2010, 21(2): 330-337.
Although auditory verbal hallucinations are often thought to denote mental illness, the majority of voice hearers do not satisfy the criteria for a psychiatric disorder. Here, we report the first functional imaging study of such nonclinical hallucinations in 7 healthy voice hearers comparing them with auditory imagery. The human voice area in the superior temporal sulcus was activated during both hallucinations and imagery. Other brain areas supporting both hallucinations and imagery included fronto temporal language areas in the left hemisphere and their contralateral homologues and the supplementary motor area (SMA). Hallucinations are critically distinguished from imagery by lack of voluntary control. We expected this difference to be reflected in the relative timing of prefrontal and sensory areas. Activity of the SMA indeed preceded that of auditory areas during imagery, whereas during hallucinations, the 2 processes occurred instantaneously. Voluntary control was thus represented in the relative timing of prefrontal and sensory activation, whereas the sense of reality of the sensory experience may be a product of the voice area activation. Our results reveal mechanisms of the generation of sensory experience in the absence of external stimulation and suggest new approaches to the investigation of the neurobiology of psychopathology.

Auditory Verbal Imagery Functional Anatomy of Auditory Verbal Imagery in Schizophrenic Patients With Auditory Hallucinations
Shergill , S.S., E. Bullmore, A. Simmons, R. Murray, and P. McGuire. American Journal of Psychiatry, October 2000, 157: 1691-1693.
This study investigated the functional neuroanatomy of inner speech and auditory verbal imagery in schizophrenic patients predisposed to auditory hallucinations. METHOD: Eight patients with schizophrenia with a history of prominent auditory hallucinations and six comparison subjects underwent functional magnetic resonance imaging while generating inner speech or imagining external speech. RESULTS: Patients showed no differences while generating inner speech but experienced a relatively attenuated response in the posterior cerebellar cortex, hippocampi, and lenticular nuclei bilaterally and the right thalamus, middle and superior temporal cortex, and left nucleus accumbens during auditory verbal imagery. CONCLUSIONS: Patients with schizophrenia who were prone to auditory hallucinations show attenuated activation when processing inner speech in areas implicated in verbal self-monitoring.

Auditory Hallucinations Engagement of Brain Areas Implicated in Processing Inner Speech in People with Auditory Hallucinations.
Shergill S.S., M.J. Brammer, R. Fukuda, S.C. Williams, R.M. Murray, P.K. McGuire. British Journal of Psychiatry, June 2003, 182: 525-31
The neurocognitive basis of auditory hallucinations is unclear, but there is increasing evidence implicating abnormalities in processing inner speech. Previous studies have shown that people with schizophrenia who were prone to auditory hallucinations demonstrated attenuated activation of brain areas during the monitoring of inner speech. AIMS: To investigate whether the same pattern of functional abnormalities would be evident as the rate of inner speech production was varied. METHOD: Eight people with schizophrenia who had a history of prominent auditory hallucinations and eight control participants were studied using functional magnetic resonance imaging while the rate of inner speech generation was varied experimentally. RESULTS: When the rate of inner speech generation was increased, the participants with schizophrenia showed a relatively attenuated response in the right temporal, parietal, parahippocampal and cerebellar cortex. CONCLUSIONS: In people with schizophrenia who are prone to auditory hallucinations, increasing the demands on the processing of inner speech is associated with attenuated engagement of the brain areas implicated in verbal self-monitoring.

Temporal Course of Auditory Hallucinations
Shergill S.S., M.J. Brammer, E. Amaro, S.C. Williams, R.M. Murray, P.K. McGuire. British Journal of Psychiatry, December 2004, 185: 516-7.
We used functional magnetic resonance imaging to examine how brain activity associated with auditory verbal hallucinations in schizophrenia changed during hallucinatory events. Activation in the left inferior frontal and right middle temporal gyri was evident 6-9 s before the person signalled the onset of the hallucination, whereas activation in the bilateral temporal gyri and the left insula coincided with the perception of the hallucination. This supports the hypothesis that during hallucinations activation in cortical regions mediating the generation of inner speech may precede the engagement of areas implicated in the perception of auditory verbal material.

Can fMRI-guidance Improve the Efficacy of rTMS Treatment for Auditory Verbal Hallucinations?
Sommer, I.E.C., C.W. Slotema, A.D. de Weijer, J. Blom, K. Daalman, S. Neggers, M. Somers, H. Hoek, A. Aleman, R. Kahn. Schizophrenia Research, 2007, 93 (1): 406-8.
The majority of schizophrenia patients showed prominent activity in the right-sided homologues of the classical language areas during AVH [auditory verbal hallucinations] (i.e. in the right inferior frontal gyrus, right superior temporal gyrus and supramarginal gyrus), while normal language is generally produced in the left hemisphere in right-handed subjects.

Auditory Verbal Hallucinations Predominantely Activate the Right Inferior Frontal Area
Sommer, I.E.C., K.M.J. Diederen, J-D. Blom, A. Willems, L. Kushan, K. Slotema, M.P.M. Boks, K. Daalman, H.W. Hoek, S.F.W. Neggers, and R.S. Kahn. Brain, October 13 2008.
The pathophysiology of auditory verbal hallucinations (AVH) is largely unknown. Several functional imaging studies have measured cerebral activation during these hallucinations, but sample sizes were relatively small (one to eight subjects) and findings inconsistent. In this study cerebral activation was measured using fMRI in 24 psychotic patients while they experienced AVHin the scanner and, in another session, while they silently generated words. All patients were right handed and diagnosed with schizophrenia, schizo-affective disorder or psychotic disorder not otherwise specified. Group analysis for AVH revealed activation in the right homologue of Broca’s area, bilateral insula, bilateral supramarginal gyri and right superior temporal gyrus. Broca's area and left superior temporal gyrus were not activated. Group analysis for word generation in these patients yielded activation in Broca’s and Wernicke's areas and to a lesser degree their right-sided homologues, bilateral insula and anterior cingulate gyri. Lateralization of activity during AVH was not correlated with language lateralization, but rather with the degree to which the content of the hallucinations had a negative emotional valence. The main difference between cerebral activity during AVH and activity during normal inner speech appears to be the lateralization. The predominant engagement of the right inferior frontal area during AVH may be related to the typical low semantic complexity and negative emotional content.

Language Production in the Non-Dominant Hemisphere as a Potential Source of Auditory Verbal Hallucinations
Sommer, Iris E. and Kelly M. Diederen. Brain, 2009, 132 (10): e124.
Excerpts: In our data, activity during auditory verbal hallucinations was not confined to the right anterior insula, but extended into the posterior insula and Broca's homologue (Sommer et al., 2008). We hypothesized that activity of this large cortical region reflects the (unconscious) generation of language. Although the right inferior frontal and insular region is not a classical language area, there is evidence that this area has limited capacity for language production (Thiel et al., 2006; Voets et al., 2006). We hypothesize that the right inferior frontal-insular area is insufficiently inhibited in patients with auditory verbal hallucinations, leading to unintended 'ectopic' language production. A similar mechanism of a right hemispheric area generating 'ectopic speech' has been described in aphasia patients (Winhuisen et al. 2005). ... The content and repetitive nature of the automatic utterances in aphasia patients, as well as the lack of voluntary control over these utterances, bear resemblance to auditory verbal hallucinations in schizophrenia patients (Gould, 1950). An obvious difference is that automatic utterances are spoken, while auditory verbal hallucinations are heard. However, before being heard, auditory verbal hallucinations are probably generated in speech production areas that may coincide with the source of automatic speech in aphasia. ... The regions (Broca's homologue and the right insula) coincide with the areas that showed greatest activation during auditory verbal hallucinations in our analysis of 24 patients (Sommer et al., 2008). It could therefore be hypothesized that auditory verbal hallucinations result from 'release' language activity in the right inferior frontal area that is inhibited in the healthy brain.

Auditory Hallucinations After Right Temporal Gyri Resection Auditory Hallucinations After Right Temporal Gyri Resection
Stewart, Bronagh and D.M. Brennan. Journal of Neuropsychiatry Clinical Neuroscience, May 2005, 17:243-245.
The authors present a case study on the development of auditory hallucinations secondary to right temporal lobe damage. Surgical resection in the study patient was of the right superficial middle and inferior temporal gyri. Carbamazepine at a dosage of 800 mg daily was the most effective medication used. A multidisciplinary approach involving the neurosurgeon, psychiatrist, family, and rehabilitation specialist is necessary in managing the psychiatric sequelae of brain injury. The case presented in this study adds to the literature on development of auditory hallucinations secondary to right temporal lobe damage.

Language Lateralization in Unmedicated Patients during an Acute Episode of Schizophrenia: A Functional MRI Study
Weiss, E.M., A. Hofer, S. Golaszewski, C. Siedentopf, S. Felber, W.W. Fleischhacker. Psychiatry Research, 2006, 146:185-190.
In a previous fMRI study of high-functioning outpatients with remitted schizophrenia, we found that healthy subjects and schizophrenia patients showed similar patterns of activation during a verbal fluency task. However, the activation in controls was primarily in Broca's area on the left, while it was more bilateral for schizophrenia patients, implicating a reduced language lateralization in schizophrenia patients. The same fMRI procedure was used in this subsequent study to investigate unmedicated patients during an acute episode of schizophrenia. Schizophrenia patients showed reduced language lateralization in the frontal cortex, because of a more bilateral activation of Broca's area compared with a primarily left hemisphere activation in healthy controls. Furthermore decreased lateralization was correlated to the severity of hallucinations. Although patients with schizophrenia showed a significantly reduced performance on the verbal fluency task when compared with healthy subjects, we were not able to find evidence of decreased language-related activity in the left hemisphere. These results suggest that decreased language lateralization is also evident in unmedicated patients experiencing an acute episode of schizophrenia.

Auditory Hallucinations in Schizophrenia Auditory Hallucinations and the Temporal Cortical Response to Speech in Schizophrenia: A Functional Magnetic Resonance Imaging Study
Woodruff, P.W.R., I.C. Wright, E.T. Bullmore, M. Brammer, R.J. Howard, S.C.R. Williams, J. Shapleske, S. Rossell, A.S. David, P.K. McGuire, R.M. Murray. American Journal of Psychiatry, 1997, 154: 1676-1682.
The authors explored whether abnormal functional lateralization of temporal cortical language areas in schizophrenia was associated with a predisposition to auditory hallucinations and whether the auditory hallucinatory state would reduce the temporal cortical response to external speech. METHOD: Functional magnetic resonance imaging was used to measure the blood-oxygenation-level-dependent signal induced by auditory perception of speech in three groups of male subjects: eight schizophrenic patients with a history of auditory hallucinations (trait-positive), none of whom was currently hallucinating; seven schizophrenic patients without such a history (trait-negative); and eight healthy volunteers. Seven schizophrenic patients were also examined while they were actually experiencing severe auditory verbal hallucinations and again after their hallucinations had diminished. RESULTS: Voxel-by-voxel comparison of the median power of subjects' responses to periodic external speech revealed that this measure was reduced in the left superior temporal gyrus but increased in the right middle temporal gyrus in the combined schizophrenic groups relative to the healthy comparison group. Comparison of the trait-positive and trait-negative patients revealed no clear difference in the power of temporal cortical activation. Comparison of patients when experiencing severe hallucinations and when hallucinations were mild revealed reduced responsivity of the temporal cortex, especially the right middle temporal gyrus, to external speech during the former state. CONCLUSIONS: These results suggest that schizophrenia is associated with a reduced left and increased right temporal cortical response to auditory perception of speech, with little distinction between patients who differ in their vulnerability to hallucinations. The auditory hallucinatory state is associated with reduced activity in temporal cortical regions that overlap with those that normally process external speech, possibly because of competition for common neurophysiological resources.

Auditory Hallucinations in Acute Stroke
Yampl, Y., M. Lorberboym, R. Gilad, M. Boaz, M. Sadeh. Behavioural Neurology, 2005, 16, 4: 211–216.
Auditory hallucinations are uncommon phenomena which can be directly caused by acute stroke, mostly described after lesions of the brain stem, very rarely reported after cortical strokes. The purpose of this study is to determine the frequency of this phenomenon. In a cross sectional study, 641 stroke patients were followed in the period between 1996-2000. Each patient underwent comprehensive investigation and follow-up. Four patients were found to have post cortical stroke auditory hallucinations. All of them occurred after an ischemic lesion of the right temporal lobe. After no more than four months, all patients were symptom-free and without therapy. The fact the auditory hallucinations may be of cortical origin must be taken into consideration in the treatment of stroke patients. The phenomenon may be completely reversible after a couple of months.