New research reveals that the brain's failure to self-monitor motor signals plays a key role in schizophrenia-related hallucinations, offering fresh insights into the mechanisms behind these perceptual distortions.
Study: Impaired motor-to-sensory transformation mediates auditory hallucinations. Image Credit: PeopleImages.com / Yuri A / Shutterstock.com
In a recent study published in the journal PLOS Biology, researchers investigate how impaired self-monitoring linked to dysfunctions in motor signal copies contributes to auditory hallucinations in schizophrenia.
Perception vs. reality
Our perceptions about the surrounding environment originate from external sensory stimuli like sights, sounds, imagination, and recalling memories. Monitoring the different sources of these perceptions is vital, with hallucinations arising when these fail, and the brain is unable to separate the source from the perception.
This self-monitoring of different sources of perception is achieved through internal forward models, in which copies of motor signals such as corollary discharge (CD) or efference copy (EC) are involved in inhibiting or enhancing sensory processing. These copies of motor signals either enhance or suppress sensory processing, which allows internally generated sensations to be distinguished from external sensory stimuli.
In mental health diseases like schizophrenia, patients often experience auditory hallucinations. Recent evidence suggests that distinct dysfunctions in CD and EC, rather than a single inhibitory failure, might be disrupted and, as a result, cause auditory hallucinations in these patients.
About the study
In the present study, researchers examine specific impairments in the inhibitory function of CD and the enhancement function of EC that contribute to auditory hallucinations experienced by individuals with schizophrenia.
A total of 40 schizophrenia patients were divided into two groups based on whether the patient did or did not experience auditory verbal hallucinations. General preparation and specific preparation tasks were utilized to determine how speech preparation affects perception. These tasks were designed to explore how CD and EC influence auditory responses during different stages of speech preparation.
In both tasks, study participants were shown visual cues and were required to speak while hearing auditory probes in the form of tones or syllables.
The general preparation task involved a visual cue with no linguistic information; therefore, the participants were not aware of what they would say. Auditory probes, which were introduced in half of the trials, consisted of one of four auditory syllables ‘ba,’ ‘ka,’ ‘ga,’ or ‘pa’ or a pure tone of one kHz.
In the specific presentation task, the visual cue consisted of a specific syllable that the participants prepared to speak with auditory probes that either matched or were different from the syllable in the visual cue.
Baseline trials included speaking without preparation and passive listening to the probes without speaking. The reaction times for speaking were recorded for each participant and analyzed to determine how different task conditions impacted the response times.
Brain activity was also recorded using an electroencephalogram (EEG), with all data filtered to remove artifacts such as eye movements. Brain responses to the auditory probes were then analyzed to explore the influence of motor signals on sensory processing.
Clinical and demographic data were also analyzed using various statistical tools.
Study findings
Dysregulation of motor signal copies involving the inhibition of CD and enhancement of EC caused errors in self-monitoring, leading to auditory hallucinations in schizophrenia patients. The study's computational modeling revealed that the combination of a "broken" CD and a "noisy" EC in patients with auditory hallucinations could explain their inability to accurately distinguish between internal and external auditory signals.
Failure of the CD system to inhibit auditory responses during general speech preparation led to auditory verbal hallucinations, as patients found it difficult to differentiate between external sounds and internally generated sounds. The model showed that impaired CD led to a failure in suppressing neural responses during general speech preparation, contributing to difficulties in differentiating internally generated sounds from external sounds. The impaired CD function supports findings from previous studies of reduced sensory suppression in schizophrenia, thus indicating that the lack of inhibitory signals was associated with other negative symptoms, such as reduced motivation to act.
The absence of auditory response suppression in general speech preparation tasks suggests that CD function was not effective in both groups of patients. However, the specific speech preparation tasks indicated that patients without auditory verbal hallucinations exhibit enhanced neural responses to prepared speech sounds, whereas those with auditory hallucinations had heightened responses to unprepared sounds, thus indicating enhanced EC function.
Conclusions
The study findings suggest that a combination of impaired CD and "noisy" EC in patients with schizophrenia resulted in the inability to distinguish between internal and external auditory signals, thereby causing auditory hallucinations. The researchers' computational model supports this conclusion by simulating the neural dynamics involved, showing how distinct dysfunctions in CD and EC lead to different patterns of auditory processing in hallucinating versus non-hallucinating patients. Thus, the brain’s mechanisms for self-monitoring and interpreting sensory feedback may be disrupted in schizophrenic patients experiencing auditory hallucinations.
Journal reference:
- Yang, F., Zhu, H., Cao, X., et al. (2024). Impaired motor-to-sensory transformation mediates auditory hallucinations. PLOS Biology 22(10). doi:10.1371/journal.pbio.3002836