Are Auditory Hallucinations Related to the Brain's Resting State Activity? A 'Neurophenomenal Resting State Hypothesis'

Abstract

While several hypotheses about the neural mechanisms underlying auditory verbal hallucinations (AVH) have been suggested, the exact role of the recently highlighted intrinsic resting state activity of the brain remains unclear. Based on recent findings, we therefore developed what we call the 'resting state hypotheses' of AVH. Our hypothesis suggest that AVH may be traced back to abnormally elevated resting state activity in auditory cortex itself, abnormal modulation of the auditory cortex by anterior cortical midline regions as part of the default-mode network, and neural confusion between auditory cortical resting state changes and stimulus-induced activity. We discuss evidence in favour of our 'resting state hypothesis' and show its correspondence with phenomenal, i.e., subjective-experiential features as explored in phenomenological accounts. Therefore I speak of a 'neurophenomenal resting state hypothesis' of auditory hallucinations in schizophrenia.

Keywords: Auditory cortex; Hallucinations, Schizophrenia; Intrinsic activity.

Fig. 1

This figure schematically illustrates our resting state hypothesis of the auditory verbal hallucination (AVH). (A) Healthy subjects. We hypothesize that the external stimuli can induce neural activity in the and related association cortex. At the same time, the resting state activity in the auditory cortex (AC) and other brain regions can interact with each other which the resulting neural difference from such rest-rest interaction being smaller than the one between resting state and stimulus-induced activity, e.g., rest-stimulus interaction. This larger neural difference during rest-stimulus interaction is supposed to generate the perception of the external stimuli. The broken line represents the smaller neural difference in the resting state itself, e.g., rest-rest interaction, when compared to the one between resting state and stimulus-induced activity from the external stimuli, e.g., rest-stimulus interaction. (B) Patients with AVH. We hypothesize that high resting state in default-mode network (DMN) induces high resting state in AC. This leads to high and increased larger neural differences during rest-rest interaction in the AC and subsequent auditory pathways. At the same time though such increased rest-rest interaction with larger neural differences diminishes the impact of external stimuli on neural activity in the AC thus leading to decreased rest-stimulus interaction. Rest-rest interaction is thus confused with rest-stimulus interaction which in turn leads to the generation of AVH. The broken line represents the larger neural difference in the resting state itself, e.g., increased rest-rest interaction, when compared to the one between resting state and stimulus-induced activity from the external stimuli, e.g., rest-stimulus interaction. Dark gray indicates the effect of external stimuli, e.g., rest-stimulus interaction, while light gray describes the effects within the resting state itself, e.g., rest-rest interaction.

Fig. 2

This figure schematically illustrates the intrinsic activity, i.e., resting state activity and its fluctuations, in relation to extrinsic, i.e., stimulus-induced activity, in auditory cortex (AC) in healthy and patients with schizophrenia. (A) Healthy subjects. We hypothesize that intrinsic spontaneous fluctuation are not as large and are hence treated and coded as resting state fluctuations rather than as stimulus-induced activity. This enables the external stimuli to induce sufficient changes in neural activity, i.e., stimulus-induced activity, as distinct from the level of the resting state activity. (B) On the contrary, in patients with the auditory verbal hallucination (AVH), the intrinsic spontaneous fluctuation is either too large or/and does not return back to the original resting state activity level. The difference between original resting state level, i.e., before occurrence of the intrinsic fluctuation, and the resting state level after the fluctuation may then be as large as the change normally induced by external stimuli; the difference in activity level before and after the resting state fluctuation may then be coded by the brain as if it was induced by an external stimulus which in turn enables and predisposes to perceive it as AVH.