Sensory Attenuation Deficit and Auditory Hallucinations in Schizophrenia: A Causal Mechanism or a Risk Factor? Evidence From Meta-Analyses on the N1 Event-Related Potential Component

Marika Mariano; Ileana Rossetti; Angelo Maravita; Eraldo Paulesu; Laura Zapparoli

doi:10.1016/j.biopsych.2023.12.026

Sensory Attenuation Deficit and Auditory Hallucinations in Schizophrenia: A Causal Mechanism or a Risk Factor? Evidence From Meta-Analyses on the N1 Event-Related Potential Component

Biol Psychiatry. 2024 Jan 20:S0006-3223(24)00035-0. doi: 10.1016/j.biopsych.2023.12.026. Online ahead of print.

Authors

Marika Mariano¹, Ileana Rossetti², Angelo Maravita², Eraldo Paulesu³, Laura Zapparoli⁴

Affiliations

¹ Psychology Department and NeuroMi, Milan Centre for Neuroscience, University of Milano-Bicocca, Milan, Italy. Electronic address: m.mariano5@campus.unimib.it.
² Psychology Department and NeuroMi, Milan Centre for Neuroscience, University of Milano-Bicocca, Milan, Italy.
³ Psychology Department and NeuroMi, Milan Centre for Neuroscience, University of Milano-Bicocca, Milan, Italy; IRCCS Orthopedic Institute Galeazzi, Milan, Italy.
⁴ Psychology Department and NeuroMi, Milan Centre for Neuroscience, University of Milano-Bicocca, Milan, Italy; IRCCS Orthopedic Institute Galeazzi, Milan, Italy. Electronic address: laura.zapparoli@unimib.it.

PMID: 38246250
DOI: 10.1016/j.biopsych.2023.12.026

Abstract

Background: Sensory attenuation (SA), the dampened perception of self-generated sensory information, is typically associated with reduced event-related potential signals, such as for the N1 component of auditory event-related potentials. SA, together with efficient monitoring of intentions and actions, should facilitate the distinction between self-generated and externally generated sensory events, thereby optimizing interaction with the world. According to many, SA is deficient in schizophrenia. The question arises whether altered SA reflects a sufficient mechanism to explain positive symptoms such as auditory hallucinations. A systematic association of reduced auditory SA in hallucinating patients would support this hypothesis.

Methods: We conducted a series of meta-analyses on 15 studies on auditory SA in which the N1 component of event-related potential-electroencephalogram signals was measured during talking (self-generated sensory signals condition) or when listening to prerecorded vocalizations (externally generated sensory signals condition).

Results: We found that individuals with schizophrenia did show some auditory SA because their N1 signal was significantly attenuated in talking conditions compared with listening conditions. However, the magnitude of such attenuation was reduced in individuals with schizophrenia compared to healthy control participants. This phenomenon generalizes independently from the stage of the disease, the severity of positive symptoms, and whether patients have auditory hallucinations or not.

Conclusions: These findings suggest that reduced SA cannot be a sufficient mechanism for explaining positive symptoms such as auditory hallucinations in schizophrenia. Because reduced SA was also present in participants at risk of schizophrenia, reduced SA may represent a risk factor for the disorder. We discuss the implications of these results for clinical-cognitive models of schizophrenia.

Keywords: Auditory hallucinations; Meta-analysis; N1; Schizophrenia; Sensory attenuation; Sensory suppression.