Neurobiological Signatures of Auditory False Perception and Phantom Perception as a Consequence of Sensory Prediction Errors

Abstract

In this study, we hypothesized that top-down sensory prediction error due to peripheral hearing loss might influence sensorimotor integration using the efference copy (EC) signals as functional connections between auditory and motor brain areas. Using neurophysiological methods, we demonstrated that the auditory responses to self-generated sound were not suppressed in a group of patients with tinnitus accompanied by significant hearing impairment and in a schizophrenia group. However, the response was attenuated in a group with tinnitus accompanied by mild hearing impairment, similar to a healthy control group. The bias of attentional networks to self-generated sound was also observed in the subjects with tinnitus with significant hearing impairment compared to those with mild hearing impairment and healthy subjects, but it did not reach the notable disintegration found in those in the schizophrenia group. Even though the present study had significant constraints in that we did not include hearing loss subjects without tinnitus, these results might suggest that auditory deafferentation (hearing loss) may influence sensorimotor integration process using EC signals. However, the impaired sensorimotor integration in subjects with tinnitus with significant hearing impairment may have resulted from aberrant auditory signals due to sensory loss, not fundamental deficits in the reafference system, as the auditory attention network to self-generated sound is relatively well preserved in these subjects.

Neurobiology of Behavior—Influences of Neuropsychiatric Disorders on Neurobiology and Behavior

“…In the study conducted by Ahn and colleagues [ 3 ], the function of top-down sensory prediction error and efference copy (EC) signals to investigate the effects of peripheral hearing loss on auditory false perception and phantom perception is examined. Patients in the study have either schizophrenia or tinnitus accompanied by varied degrees of hearing loss.…”

The role of prediction and attention in phantom voice perception

“…These findings give rise to a few pertinent questions. What all within the framework of predictive processing using EEG and talk-listen paradigm (Ahn et al, 2022). Lack of N100 suppression was observed in both, tinnitus patients with severe (but not mild) hearing loss and patients with psychosis but not in tinnitus without hearing loss, suggesting a common dysfunction in predictive processing following severe sensory deprivation in tinnitus and psychotic hallucinations.…”

Altered listening changes the way we predict the auditory environment

“…Participants produced vowels and then listened to their own voice recordings (i.e., 'Talk/Listen' paradigm) while EEG was recorded. The results indicated that N100 suppression, which is typically indicative of successful sensory processing, was reduced in schizophrenia patients and in the group of tinnitus with hearing difficulties (which also showed increased levels of hearing loss when compared to the tinnitus group without hearing difficulties) (Ahn et al, 2022). The authors thus argued that hearing loss and self-perceived hearing impairment may influence N100 suppression to selfgenerated sounds (Ahn et al, 2022).…”

“…In humans, position predictions were investigated in tinnitus and results indicated increased variability in the amount of suppression a person with tinnitus displays (Ahn et al, 2022;Campbell, Bean, & LaBrec, 2018). In animals, on the other hand, where evoked potentials in the MGB were analyzed, results indicated successful gating of formal-, temporal-, and position predictions (Zare et al, 2023).…”

“…Research that includes persons with tinnitus with and without hearing loss and comparisons to hearing-matched persons without tinnitus remains scarce. One EEG study that investigated prediction errors for auditory false perceptions and phantom perceptions in persons with tinnitus assigned participants to groups with mild or severe hearing loss and compared them to a group of persons with schizophrenia(Ahn et al, 2022). The results showed that auditory ERP responses for self-generated sounds were not suppressed in persons with tinnitus + severe hearing loss (n = 15) and persons with schizophrenia (n = 10), whereas the typical suppression was observed in persons without tinnitus (n = 23) and in persons with tinnitus + mild hearing loss (n = 8)(Ahn et al, 2022…”