Jane R Garrison

The neural mechanisms of hallucinations: A quantitative meta-analysis of neuroimaging studies.

Activation likelihood estimation meta-analysis of functional neuroimaging data was used to investigate the neural mechanisms underlying auditory-verbal and visual hallucinations (AVHs and VHs). Consistent activation across studies during AVHs, but not VHs, in Wernickes and Brocas areas is consistent with involvement of speech and language processes in the experience of hearing voices when none are present. Similarly, greater activity in auditory cortex during AVHs and in visual cortex during VHs supports models proposing over-stimulation of sensory cortices in the generation of these perceptual anomalies. Activation across studies in the medial temporal lobe highlights a role for memory intrusions in the provision of content for AVHs, whereas insula activation may relate to the involvement of awareness and self-representation. Finally, activation in the paracingulate region of medial prefrontal cortex during AVHs is consistent with models implicating reality monitoring impairment in the misattribution of self-generated information as externally perceived. In the light of the results, the need for unified theoretical frameworks that account for the full range of hallucinatory experiences is discussed.

Don’t wait to incubate: Immediate versus delayed incubation in divergent thinking

Previous evidence for the effectiveness of immediate incubation in divergent creative tasks has been weak, because earlier studies exhibited a range of methodological problems. This issue is theoretically important, as a demonstration of the effects of immediate incubation would strengthen the case for the involvement of unconscious work in incubation effects. For the present experiment, we used a creative divergent-thinking task (alternative uses) in which separate experimental groups had incubation periods that were either delayed or immediate and that consisted of either spatial or verbal tasks. Control groups were tested without incubation periods, and we carried out checks for intermittent conscious work on the target task during the incubation periods. The results showed significant incubation effects that were stronger for immediate than for delayed incubation. Performance was not different between the verbal and spatial incubation conditions, and we found no evidence for intermittent conscious working during the incubation periods. These results support a role for unconscious work in creative divergent thinking, particularly in the case of immediate incubation.

Paracingulate sulcus morphology is associated with hallucinations in the human brain

Hallucinations are common in psychiatric disorders, and are also experienced by many individuals who are not mentally ill. Here, in 153 participants, we investigate brain structural markers that predict the occurrence of hallucinations by comparing patients with schizophrenia who have experienced hallucinations against patients who have not, matched on a number of demographic and clinical variables. Using both newly validated visual classification techniques and automated, data-driven methods, hallucinations were associated with specific brain morphology differences in the paracingulate sulcus, a fold in the medial prefrontal cortex, with a 1 cm reduction in sulcal length increasing the likelihood of hallucinations by 19.9%, regardless of the sensory modality in which they were experienced. The findings suggest a specific morphological basis for a pervasive feature of typical and atypical human experience.

Brain Mechanisms of Reality Monitoring

Reality monitoring processes are necessary for discriminating between internally generated information and information that originated in the outside world. They help us to identify our thoughts, feelings, and imaginations, and to distinguish them from events we may have experienced or have been told about by someone else. Reality monitoring errors range from confusions between real and imagined experiences, that are byproducts of normal cognition, to symptoms of mental illness such as hallucinations. Recent advances support an emerging neurocognitive characterization of reality monitoring that provides insights into its underlying operating principles and neural mechanisms, the differing ways in which impairment may occur in health and disease, and the potential for rehabilitation strategies to be devised that might help those who experience clinically significant reality monitoring disruption.

Testing continuum models of psychosis: No reduction in source monitoring ability in healthy individuals prone to auditory hallucinations

People with schizophrenia who hallucinate show impairments in reality monitoring (the ability to distinguish internally generated information from information obtained from external sources) compared to non-hallucinating patients and healthy individuals. While this may be explained at least in part by an increased externalizing bias, it remains unclear whether this impairment is specific to reality monitoring, or whether it also reflects a general deficit in the monitoring of self-generated information (internal source monitoring). Much interest has focused recently on continuum models of psychosis which argue that hallucination-proneness is distributed in clinical and non-clinical groups, but few studies have directly investigated reality monitoring and internal source monitoring abilities in healthy individuals with a proneness to hallucinations. Two experiments are presented here: the first (N = 47, with participants selected for hallucination-proneness from a larger sample of 677 adults) found no evidence of an impairment or externalizing bias on a reality monitoring task in hallucination-prone individuals; the second (N = 124) found no evidence of atypical performance on an internal source monitoring task in hallucination-prone individuals. The significance of these findings is reviewed in light of the clinical evidence and the implications for models of hallucination generation discussed.

Reality monitoring impairment in schizophrenia reflects specific prefrontal cortex dysfunction

Reality monitoring impairment is often reported in schizophrenia but the neural basis of this deficit is poorly understood. Difficulties with reality monitoring could be attributable to the same pattern of neural dysfunction as other cognitive deficits that characterize schizophrenia, or might instead represent a separable and dissociable impairment. This question was addressed through direct comparison of behavioral performance and neural activity associated with reality monitoring and working memory in patients with schizophrenia and matched healthy controls. Participants performed a word-pair reality monitoring task and a Sternberg working memory task while undergoing fMRI scanning. Distinct behavioral deficits were observed in the patients during performance of each task, which were associated with separable task- and region-specific dysfunction in the medial anterior prefrontal cortex for reality monitoring and dorsolateral prefrontal cortex for working memory. The results suggest that reality monitoring impairment is a distinct neurocognitive deficit in schizophrenia. The findings are consistent with the presence of a range of dissociable cognitive deficits in schizophrenia which may be associated with variable functional and structural dysconnectivity in underlying processing networks.

Monitoring what is real: The effects of modality and action on accuracy and type of reality monitoring error.

Reality monitoring refers to processes involved in distinguishing internally generated information from information presented in the external world, an activity thought to be based, in part, on assessment of activated features such as the amount and type of cognitive operations and perceptual content. Impairment in reality monitoring has been implicated in symptoms of mental illness and associated more widely with the occurrence of anomalous perceptions as well as false memories and beliefs. In the present experiment, the cognitive mechanisms of reality monitoring were probed in healthy individuals using a task that investigated the effects of stimulus modality (auditory vs visual) and the type of action undertaken during encoding (thought vs speech) on subsequent source memory. There was reduced source accuracy for auditory stimuli compared with visual, and when encoding was accompanied by thought as opposed to speech, and a greater rate of externalization than internalization errors that was stable across factors. Interpreted within the source monitoring framework (Johnson, Hashtroudi, & Lindsay, 1993), the results are consistent with the greater prevalence of clinically observed auditory than visual reality discrimination failures. The significance of these findings is discussed in light of theories of hallucinations, delusions and confabulation.

Dissociable Neural Networks Supporting Metacognition for Memory and Perception

Metacognition in its broadest sense refers both to knowledge about our mental abilities and to the regulatory processes by which we might use that knowledge to control cognition; for example, changing how we perform a task if we feel our current strategy is not optimal ([Fernandez-Duque et al., 2000

Paracingulate sulcus morphology and hallucinations in clinical and non-clinical groups.

Hallucinations are a characteristic symptom of psychotic mental health conditions that are also experienced by many individuals without a clinical diagnosis. Research has linked the experience of hallucinations in schizophrenia to differences in the length of the paracingulate sulcus (PCS), a structure in the medial prefrontal cortex of the brain which has previously been associated with the ability to differentiate perceived and imagined information. We investigated whether this notion of a specific morphological basis for hallucinations in the paracingulate cortex extends to individuals without a clinical diagnosis by testing the hypothesis that non-clinical individuals with hallucinations have shorter PCS than non-clinical individuals without hallucinations. Structural MRI scans were examined from three demographically matched groups of individuals: 50 patients with psychotic diagnoses who experienced auditory verbal hallucinations, 50 non-clinical individuals with auditory verbal hallucinations, and 50 healthy control subjects with no life-time history of hallucinations. Measurements of paracingulate sulcal length were compared between the groups and the results verified using automated data-driven gyrification analyses. Patients with hallucinations had shorter PCS than both healthy controls and non-clinical individuals with hallucinations, with no difference between non-clinical individuals with hallucinations and healthy controls. These findings suggest that the association of shorter PCS length with hallucinations is specific to patients with a psychotic disorder. This presents challenges for continuum models of psychosis and suggests possible differences in the mechanisms underlying hallucinations in clinical and non-clinical groups.

Meta-analytic evidence for the plurality of mechanisms in transdiagnostic structural MRI studies of hallucination status

BACKGROUND Hallucinations are transmodal and transdiagnostic phenomena, occurring across sensory modalities and presenting in psychiatric, neurodegenerative, neurological, and non-clinical populations. Despite their cross-category occurrence, little empirical work has directly compared between-group neural correlates of hallucinations. METHODS We performed whole-brain voxelwise meta-analyses of hallucination status across diagnoses using AES-SDM, and conducted a comprehensive systematic review in PubMed and Web of Science until May 2018 on other structural correlates of hallucinations, including cortical thickness and gyrification. FINDINGS 3214 abstracts were identified. Patients with psychiatric disorders and hallucinations (eight studies) exhibited reduced gray matter (GM) in the left insula, right inferior frontal gyrus, left anterior cingulate/paracingulate gyrus, left middle temporal gyrus, and increased in the bilateral fusiform gyrus, while patients with neurodegenerative disorders with hallucinations (eight studies) showed GM decreases in the left lingual gyrus, right supramarginal gyrus/parietal operculum, left parahippocampal gyrus, left fusiform gyrus, right thalamus, and right lateral occipital gyrus. Group differences between meta-analyses were formally confirmed and a jackknife sensitivity analysis established the reproducibility of results across nearly all study combinations. For other measures (28 studies), the most consistent findings associated with hallucination status were reduced cortical thickness in temporal gyri in schizophrenia and altered hippocampal volume in Parkinson’s disease and dementia. INTERPRETATION Distinct patterns of neuroanatomical alteration characterize hallucination status in patients with psychiatric and neurodegenerative diseases, suggesting a plurality of anatomical signatures. This approach has implications for treatment, theoretical frameworks, and generates refutable predictions for hallucinations in other diseases and their occurrence within the general population. FUNDING None. Research in context Evidence before this study There is increasing recognition that hallucinations occur beyond the archetype of schizophrenia, presenting in other psychiatric disorders, neurological and neurodegenerative conditions, and among the general population. Not only are hallucinations a transdiagnostic phenomenon, but also the experience of hallucinating is phenomenologically diverse, varying in modality, content, frequency, and affect. It has been suggested that no one type of hallucination is pathognomic to any one disorder, but rather that hallucinations may exist on a continuum. However, limited research has been done to directly compare the underlying neuroanatomy of hallucinations between different disorders. With this aim, we conducted a meta-analysis and systematic review of structural MRI studies comparing individuals who experience hallucinations with those who do not, to investigate the brain morphology related to the transdiagnostic presentation of hallucinations. We searched PubMed and Web of Science with no start date limit, up to May 2018 using the keyword combination (hallucinat*) AND (MRI OR magnetic resonance imaging OR morphology OR voxel?based OR morphometr* OR neural correlate OR structur*). We included only studies with a within-group no-hallucination control to tease out structural changes specific to hallucinations from effects of the broader pathology. Neuroimaging meta-analyses were conducted on studies performing whole-brain voxelwise gray matter differences, while studies assessing other structural correlates were qualitatively synthesized. Added value of this study This is the first meta-analysis to illustrate the brain structural correlates of hallucination occurrence derived from T1-weighted MRI, and to do so in a comparative manner across clinical groups. We identified two distinct gray matter substrates for hallucination presence in psychiatric compared to neurodegenerative diseases, which we hypothesise constitute at least two distinct mechanisms. In addition, we qualitatively assessed other structural neuroimaging studies over a variety of morphometric indices. We therefore provide a complete characterization of current knowledge of the brain morphology associated with hallucinations across clinical status and modality. Implications of all the available evidence Our findings show at least two structural substrates that link to the hallucinatory experience. This informs theoretical work on hallucinations which have to date been limited in generating unifying direction-specific predictions of brain structure and function. Understanding the plurality of anatomical signatures of hallucinations may also inform treatment strategies. We predict that other disorders in which patients experience hallucinations can be categorised by our approach based on the broader phenotype; for example, hallucinations in personality disorder may be of the psychiatric type, and similarly for early onset hallucinations in the general population, whilst later onset will be neurodegenerative. Moreover, by differentiating the mechanisms of hallucinations we recommend the contextualising of research by the appropriate phenotype.