Auditory Hallucinations as Translational Psychiatry: Evidence from Magnetic Resonance Imaging

Abstract

In this invited review article, I present a translational perspective and overview of our research on auditory hallucinations in schizophrenia at the University of Bergen, Norway, with a focus on the neuronal mechanisms underlying the phenomenology of experiencing “hearing voices”. An auditory verbal hallucination (i.e. hearing a voice) is defined as a sensory experience in the absence of a corresponding external sensory source that could explain the phenomenological experience. I suggest a general frame or scheme for the study of auditory verbal hallucinations, called Levels of Explanation. Using a Levels of Explanation approach, mental phenomena can be described and explained at different levels (cultural, clinical, cognitive, brain-imaging, cellular and molecular). Another way of saying this is that, to advance knowledge in a research field, it is not only necessary to replicate findings, but also to show how evidence obtained with one method, and at one level of explanation, converges with evidence obtained with another method at another level. To achieve breakthroughs in our understanding of auditory verbal hallucinations, we have to advance vertically through the various levels, rather than the more common approach of staying at our favourite level and advancing horizontally (e.g., more advanced techniques and data acquisition analyses). The horizontal expansion will, however, not advance a deeper understanding of how an auditory verbal hallucination spontaneously starts and stops. Finally, I present data from the clinical, cognitive, brain-imaging, and cellular levels, where data from one level validate and support data at another level, called converging of evidence. Using a translational approach, the current status of auditory verbal hallucinations is that they implicate speech perception areas in the left temporal lobe, impairing perception of and attention to external sounds. Preliminary results also show that amygdala is implicated in the emotional «colouring» of the voices and that excitatory neurotransmitters might be involved. What we do not know is why hallucinatory episodes occur spontaneously, why they fluctuate over time, and what makes them spontaneously stop. Moreover, is voice hearing a category or dimension in its own right, independent of diagnosis, and why is the auditory modality predominantly implicated in psychotic disorders, while the visual modality dominates in, for example, neurological diseases?

A unified model of shared brain structural alterations in patients with different mental disorders who experience own‐thought auditory verbal hallucinations—A pilot study

“…Based on the common structural pattern observed, we postulate that there may be common pathological features specific to OTAVH symptoms that are independent of the patients' particular mental disorder diagnosis. These findings are consistent with Hugdahl's model wherein AVHs are suggested to be a result of impairments affecting WM connections linking the temporal-lobe auditory-perceptual and frontal-lobe attention-executive networks (Hugdahl, 2015(Hugdahl, , 2017Hugdahl & Sommer, 2018;Zmigrod et al, 2016), which are pivotal components of bottom-up and topdown networks, respectively. In this study, we observed reduced Chang et al, 2017;Kuhn & Gallinat, 2012).…”

Current Practice and New Developments in the Use of In Vivo Magnetic Resonance Spectroscopy for the Assessment of Key Metabolites Implicated in the Pathophysiology of Schizophrenia

“…fMRI studies into AVHs suggest that they are an anomaly of speech perception rather than speech production, although speech production areas are also involved to some extent (Sommer et al, 2008). Converging evidence from separate meta-analyses showed spontaneous activity in speech perception areas in the left superior temporal gyrus (STG) and superior temporal sulcus (STS) and that these patterns of activity closely resemble patterns of activity measured in healthy individuals when listening to speech from an external source (Hugdahl, 2017;Jardri, Pouchet, Pins, & Thomas, 2011;Kompus, Westerhausen, & Hugdahl, 2011;Kühn & Gallinat, 2012;van den Noort, Specht, Rimol, Ersland, & Hugdahl, 2008). However, during AVHs, spontaneous activity has also been observed in the right prefrontal cortex, believed to be related to the semantic simplicity and negative emotional valence typically associated with AVHs in schizophrenia patients (Hugdahl, 2017;Jardri et al, 2011;Sommer et al, 2008).…”

Change in the Neural Response to Auditory Deviance Following Cognitive Therapy for Hallucinations in Patients With Schizophrenia

“…Functional neuroimaging has shown that the neural encoding of natural sounds (e.g., speech, voice) entails the formation of multiple representations of sound spectrograms with different degrees of spectral and temporal resolution (152)(153)(154). Combining the superior temporal and spatial resolution of EEG and fMRI techniques, respectively, to image neural activity during resting-state (absence of external auditory stimulation) and in response to behaviorally relevant, real-world sound stimuli would be an optimal strategy for achieving a more complete picture of brain mechanisms involved in AVH responsiveness to CBTv in SZ patients (155)(156)(157)(158)(159)(160).…”