The role of the primary auditory cortex in the neural mechanism of auditory verbal hallucinations

Abstract

Auditory verbal hallucinations (AVHs) are a subjective experience of “hearing voices” in the absence of corresponding physical stimulation in the environment. The most remarkable feature of AVHs is their perceptual quality, that is, the experience is subjectively often as vivid as hearing an actual voice, as opposed to mental imagery or auditory memories. This has lead to propositions that dysregulation of the primary auditory cortex (PAC) is a crucial component of the neural mechanism of AVHs. One possible mechanism by which the PAC could give rise to the experience of hallucinations is aberrant patterns of neuronal activity whereby the PAC is overly sensitive to activation arising from internal processing, while being less responsive to external stimulation. In this paper, we review recent research relevant to the role of the PAC in the generation of AVHs. We present new data from a functional magnetic resonance imaging (fMRI) study, examining the responsivity of the left and right PAC to parametrical modulation of the intensity of auditory verbal stimulation, and corresponding attentional top-down control in non-clinical participants with AVHs, and non-clinical participants with no AVHs. Non-clinical hallucinators showed reduced activation to speech sounds but intact attentional modulation in the right PAC. Additionally, we present data from a group of schizophrenia patients with AVHs, who do not show attentional modulation of left or right PAC. The context-appropriate modulation of the PAC may be a protective factor in non-clinical hallucinations.

Auditory verbal hallucinations and continuum models of psychosis: A systematic review of the healthy voice-hearer literature

“…These include more errors in top down semantic expectation when compared to HCs (Daalman, Verkooijen, Derks, Aleman, & Sommer, 2012*). Moreover, auditory acuity appears somewhat lower in HVHs than HCs (Kompus et al, 2013). Similarly, some cognitive functions, mainly in the verbal domain, have been demonstrated to be significantly lower in HVHs compared to HCs (Daalman, van Zandvoort, et al, 2011*).…”

“…A total of 9 studies used neuroimaging to investigate HVHs, with methodologies ranging from electroencephalography (EEG), functional magnetic resonance imaging (fMRI), structural MRI, diffusion tensor imaging (DTI) as well as positron emission tomography (PET) (Table 4; De Weijer et al, 2013, Diederen et al, 2013, Diederen et al, 2010, Diederen et al, 2012, Howes et al, 2013, Howes et al, 2013, Kompus et al, 2013, Linden et al, 2011, van Lutterveld et al, 2010, van Lutterveld et al, 2014). Howes, Shotbolt et al (2013*) used PET imaging with [18F]-DOPA to investigate dopamine (DA) synthesis capacity in HVHs and HCs.…”

Prevalence of auditory verbal hallucinations in a general population: A group comparison study

“…General population studies (Johns et al, 2004;Kendler, Gallagher, Abelson & Kessler, 1996;Ohayon, 2000;Tien, 1991;van Os et al, 2000) as well as studies comparing patients with schizophrenia with non-patients (Johns et al, 2014) all suggest that AVH in non-clinical and clinical groups may share some of the same psychological factors associated with AVH, such as anxiety and depression (Lawrence, Jones & Cooper, 2010), as well as a history of trauma (Daalman, Diederen, Derks, van Lutterveld, Kahn & Sommer, 2012;Lataster, van Os, Drukker et al, 2006;Romme & Escher, 1989). Also, reduced brain activation in non-clinical groups with AVH has been found in speech areas (Kompus, Falkenberg, Bless et al, 2013), resembling findings from clinical groups (Hugdahl, Løberg & Nyg ard, 2009). In addition to this, phenomenological similarities appear to be related to the perceptual and/or acoustic aspects of AVH (Daalman et al, 2011;Honig, Romme, Ensink, Escher, Pennings & deVries, 1998;Leudar, Thomas, McNally & Glinski, 1997), whereas differences are related to aspects such as the negative content and severity of AVH, their deleterious impact on functioning, and the significantly higher age of onset of AVH in the clinical group compared with the non-clinical group (Larøi, 2012).…”

Auditory Cortex Characteristics in Schizophrenia: Associations With Auditory Hallucinations

“…In a longitudinal study following 150 psychosis patients for 20 years, 40%-45% of the schizophrenia patients had frequent or persistent hallucinations during this period, 3 and having AH at index hospitalization was associated with a reduced likelihood of recovery over the next 20 years. 4 Despite extensive efforts to elucidate the neural mechanisms underlying AH in schizophrenia patients, [5][6][7] so far the neurobiological underpinnings remain obscure.…”

“…5,8 Evidence suggests that schizophrenia patients show deficits in basic auditory processing that may be consistent with auditory cortex pathology. 9 The auditory cortex includes the primary auditory cortex (in the Heschl's gyrus [HG]), 10 and surrounding auditory association cortex in the planum temporale (PT) and the superior temporal gyrus (STG).…”