The cognitive neuropsychology of auditory hallucinations: a parallel auditory pathways framework

Abstract

Auditory hallucinations are generally defined as false perceptions. Recent developments in auditory neuroscience have rapidly increased our understanding of normal auditory perception revealing (partially) separate pathways for the identification ("what") and localization ("where") of auditory objects. The current review offers a reexamination of the nature of auditory hallucinations in schizophrenia using this object-based framework. First, the structural and functional organization of auditory what and where pathways is briefly described. Then, using recent functional neuroimaging data from healthy subjects and patients with schizophrenia, key phenomenological features of hallucinations are linked to abnormal processing both within and between these pathways. Finally, current cognitive explanations of hallucinations, based on intrusive cognitions and impaired source memory, are briefly outlined and set within this framework to provide an integrated cognitive neuropsychological model of auditory hallucinations.

Fig. 1.

Schematic Illustration of Parallel Pathways in the Human Auditory Cortex. A. Approximate projections and selected functions of separable “what” and “where” auditory pathways (dashed lines), within which both top-down and bottom-up activation may occur—signified by dual headed arrows. The dorsal auditory where pathway, involved in processing spatial attributes of sounds, originates in posterior, but not anterior, areas of the superior temporal cortex and projects to inferior parietal and superior frontal cortical areas. Activation in planum temporale and inferior parietal cortex contributes to external sound localization. A dorsal stream auditory-motor integration function has also been proposed, implicating area Spt (within planum temporale) and frontal articulatory/action networks. Hearing action-related speech activates relevant motor representations in premotor cortex. In contrast, processing of sound identity in the ventral auditory what pathway is more distributed, within anterior (voice recognition) and posterior (environmental sound recognition) temporal cortex, and projects to inferior frontal cortex.,, B. Phenomenological features of auditory hallucinations linked to auditory pathway functions. Abnormal activity in the auditory what pathway may lead to the perception of complex objects (voices, environmental sounds) in the absence of external stimulation (ie, auditory hallucinations). Additionally, less detailed processing of vocal information in the ventral pathway, probably involving basic auditory sensory deficits, results in more male-sounding voices and may lead to the predominance of male “voices” (see text for details). Abnormal activation within the posterior region of the auditory where pathway, including planum temporal and inferior parietal lobe, may produce hallucinations perceived in external space (ie, “outside the head”), while “voices” commenting on patients’ actions/telling patients what to do may engage neural structures in the anterior dorsal stream coding the heard actions.