Restoring hearing with an auditory midbrain implant in humans – current evidence from cortical event-related potentials

Auditory brainstem implants (ABI) are used to restore speech perception in patients with sensorineural hearing loss. Unfortunately, the ABI has achieved only limited success in patients suffering from neurofibromatosis type 2 (NF2). Recently, a new hearing prosthesis has been developed that stimulates the midbrain at the tonotopically organized inferior colliculus (IC) with a penetrating 20-contact electrode array (AMI – auditory midbrain implant; Cochlea Ltd., Lenarz et al., 2008). We applied the mismatch negativity (MMN) event-related potential (ERP) to measure preattentive subthreshold stimulus detection and the P3b ERP to evaluate attentive processing to stimuli of different pitch and rise time in a NF2 patient implanted at the level of the IC.

Freefield stimuli (700Hz sine tone, 75ms duration, 5ms rise-/fall time) were presented using a multi-feature MMN paradigm as proposed by Näätänen et al. (2004, 2007; Pakarinen et al., 2007). Deviants were 1300, 1900, 3100Hz in a frequency perception condition and 15, 40, 65ms in a rise time condition. ERPs were recorded from all sites of the 10–20 System. Time constant was 10s, low pass at 100Hz. Electrodes were referenced to the nose tip. ERPs were averaged for 1024ms epochs. Before averaging artefact rejection was performed off-line and excluded trials contaminated with ocular or other artefacts using individualized amplitude criteria. Separate averages were obtained for the standard sound and the different deviant tones in a passive and active listening condition.

Hitrates differed between the frequency (38.1/86.4/90.0%) and the rise time condition (5.0/5.1/6.6%), thus indicating superior pitch discrimination in our pilot subject. Reliable P3b ERPs were recorded for correctly detected 1900 and 3100Hz pitch deviants in the active condition. Whilst passively presented, the MMN was observed for 1900 and 3100Hz pitch as well as 65ms rise time deviants.

Stimulation of the auditory pathway at the level of the inferior colliculus results in a differential electrophysiological cortical response that is comparable to normal hearing subjects for pitch processing. ERPs were successfully applied as an objective marker to indicate attentional pitch perception and to trace subthreshold preattentive auditory percepts. Clinically, the patient obtained enhancements in lip reading and environmental awareness as well as improvements in speech perception comparable with that of NF2 ABI patients.