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Figure 1 Brain regions active in a schizophrenic patient experiencing auditory-visual hallucinations of disembodied, rolling heads speaking to him. The functional PET results are superimposed on the subject's own structural brain MRI scan. The bright areas pinpoint regions of heightened cortical activity associated with hallucinatory events [reproduced with permission from D. A. Silbersweig et al. (1995), A functional neuroanatomy of hallucinations in schizophrenia. Nature 378, 176-179].

paralimbic regions that may be involved in the generation or modulation of hallucinations (Fig. 2). Limbic structures, the least differentiated, or least distinctly structured, older regions of the cortex, are involved in the linking of drives with experience and the processing of emotion. Paralimbic regions are intermediate in structure between, and interconnected with, limbic and heteromodal association areas and serve to integrate emotion and drive with highly processed sensory information. Because limbic and paralimbic structures are closely interconnected and functionally integrated, they are often referred to collectively as the limbic system.

In our study, activation in limbic regions involved hippocampi (extending to the adjacent amygdalae) and ventral striatum. The hippocampal formation, a convoluted structure within the medial temporal lobe, is involved in memory and the processing of contextual

Ventral striatum: translates emotional significance of stimuli into goal-directed behavior

Anterior cingulate gyrus:

mediates attention and emotional behavior

Ventral striatum: translates emotional significance of stimuli into goal-directed behavior

Anterior cingulate gyrus:

mediates attention and emotional behavior

Scale: shows degree of significance of activity during hallucinations high highest

Figure 2 Common areas of brain activity in a group of schizophrenic patients experiencing auditory/verbal hallucinations. The functional PET results are superimposed on an anatomical MRI template. The bright areas pinpoint regions of heightened thalamic, limbic, and paralimbic activity associated with hallucinatory events [reproduced with permission from D. A. Silbersweig et al. (1995), A functional neuroanatomy of hallucinations in schizophrenia. Nature 378, 176-179].

aspects of emotional evaluation. The amygdaloid complex, a collection of nuclei adjacent to and interconnected with the hippocampus, plays a central role in evaluating the emotional significance of internally and externally generated stimuli. Both of these structures send output to the ventral striatum, the limbic portion of the subcortical basal ganglia, where emotional significance is translated into goal-directed behavior. Activation in paralimbic regions involved parahippocampal gyri, anterior cingulate, and orbito-frontal cortex. The parahippocampal gyrus, which lies on the medial surface of the temporal lobe, integrates sensory output from heteromodal and more complex unimodal association areas with limbically processed information. The anterior cingulate, the frontmost portion of a band running from medial frontal to parahippocampal regions, is involved in attention and social/emotional behaviors. The orbital frontal cortex is located in the medial ventral frontal lobes. Like the amygdala, it participates in the evaluation of emotional significance and sends output to the ventral striatum. In contrast to the amygdala, the orbital frontal region is able to modulate emotional respon-sivity and readjust behavioral responses to stimuli when their reinforcement value is changed or when a more complex assessment of the current context suggests the need for modification.

Just as abnormal activity in cortical sensory regions is correlated with the form and content of hallucinations, it is likely that aberrant activity in limbic/ paralimbic regions gives rise to the marked emotional significance of hallucinations in the setting of schizophrenia. Further evidence of a role for limbic system dysfunction in the generation of schizophrenic symptoms is provided by postmortem, neuropsychological, and neuroimaging studies that reveal structural and functional abnormalities of limbic regions in individuals with schizophrenia, including hyperactivity of temporal regions (left greater than right) associated with psychosis. Activity of the limbic system is closely interconnected with that of dopamine, a neurotrans-mitter implicated in the generation of hallucinations and delusions in the settings of schizophrenia, medication toxicity, and drug abuse. Dopaminergic activity is regulated, in part, by input from limbic system structures and in turn appears to modulate the responsiveness of ventral striatal neurons to limbic inputs. Recent work suggests that glutamate, an excitatory neurotransmitter, may also play a role in both limbic dysregulation and schizophrenia. Hallucinations that occur in the context of severe emotional stress may also involve abnormal limbic activity.

Temporolimbic structures also play a role in the generation of hallucinations associated with epilepsy. In addition to photopsias, the onset of partial seizures can be accompanied by simple hallucinations in any modality, reflecting ictal discharges in primary sensory areas, or by complex hallucinations, reflecting discharges in limbic and sensory association areas. These often involve temporal regions including hippocampus and amygdala, which have the lowest seizure thresholds of all brain structures, as well as sensory association areas. Like the complex hallucinations seen in schizophrenia, these are often emotionally charged. Unlike those seen in schizophrenia, they are more often visual than auditory and are not usually believed by the person experiencing them to represent reality. Relatedly, electrical stimulation of temporal lobe regions, including the amygdala, can give rise to hallucinatory experiences. In addition to hallucina tions experienced during seizures, there is evidence that individuals who have suffered from epilepsy for more than 10 years may develop hallucinations between seizure episodes. These are more likely to resemble fully those seen in schizophrenia as they are often emotionally charged, are as likely to be auditory as visual, are accompanied by delusions, and are believed to represent reality. As in schizophrenia, they appear to be associated with temporal lobe abnormalities (left more often than right).

3. Frontal/Executive Activity Associated with Hallucinations

The lack of awareness that hallucinatory experience does not correspond to reality is a striking feature of schizophrenia. In addition to temporal lobe abnormalities, numerous studies have revealed frontal dysfunction and abnormal frontotemporal connectivity associated with schizophrenia. The frontal lobes, in concert with interconnected regions, mediate the higher, more complex aspects of cognition, such as judgment, insight, and self-monitoring. These are termed executive functions. Although relevant studies have produced mixed results, there is evidence that frontal dysfunction may contribute to the inability of individuals with schizophrenia to identify the internal origin of their hallucinatory experience and its relation to their illness. Temporal lobe epilepsy may also be accompanied by executive as well as other forms of cognitive dysfunction and by abnormalities of frontal activity.

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