Impaired motor-to-sensory transformation mediates auditory hallucinations

Area of Science:

• Neuroscience
• Psychiatry
• Cognitive Science

Background:

• A sense of agency relies on monitoring motor commands and their sensory consequences.
• The efference copy (EC) or corollary discharge (CD) hypothesis suggests motor signals predict sensory feedback to suppress self-generated sensations.
• Dysfunction in this predictive mechanism is implicated in hallucinations, but the precise nature of impairment remains unclear.

Purpose of the Study:

• To investigate selective impairments in corollary discharge (CD) and efference copy (EC) signals during motor-to-sensory transformation in patients with auditory verbal hallucinations (AVHs).
• To differentiate the roles of general versus specific motor preparation in auditory response modulation in schizophrenia.
• To develop a computational model to quantify motor-to-sensory transformation deficits in AVHs.

Main Methods:

• Electroencephalography (EEG) experiment using a delayed articulation paradigm in schizophrenic patients with (AVHs) and without (non-AVHs) auditory verbal hallucinations.
• Assessed auditory response suppression during general motor preparation (speaking without knowing content) and enhancement during specific motor preparation (preparing a specific syllable).
• Developed a computational model simulating "broken" CD and "noisy" EC with virtual lesions and sensitized auditory cortices to fit empirical data.

Main Results:

• General motor preparation failed to suppress auditory responses in both AVH and non-AVH groups, indicating absent inhibitory CD function.
• Specific motor preparation enhanced auditory responses to prepared syllables in non-AVHs but enhanced responses to unprepared syllables in AVHs, unlike healthy individuals.
• The computational model successfully replicated empirical data, quantifying distinct impairments in motor-to-sensory transformation, specifically "broken" CD and "noisy" EC, in AVHs.

Conclusions:

• Auditory verbal hallucinations in schizophrenia result from a combination of impaired corollary discharge (CD) inhibition and imprecise efference copy (EC) enhancement.
• These "broken" CD and "noisy" EC signals lead to erroneous monitoring and imprecise generation of internal auditory representations.
• Specific deficits in the functional granularity of motor-to-sensory transformation mediate positive symptoms of agency abnormality in mental disorders like schizophrenia.