Auditory Midbrain Implant Research Articles

Auditory Midbrain Implant: Present Clinical Results and Future Directions

Introduction: Tumor-induced damage in the cochlear nucleus may be responsible for the limited success of the auditory brainstem implant (ABI) in neurofibromatosis type 2 (NF2) patients. Therefore, an alternative implantation site that bypasses the damaged pathways in the brainstem may provide better hearing performance in NF2 patients. The central nucleus of the inferior colliculus (ICC) provides access to almost all ascending auditory information and has a well-defined tonotopic organization, which is important for an auditory prosthesis. The auditory midbrain implant (AMI) is a single-shank multielectrode array designed according to the dimensions of the human ICC with the goal of stimulating the different frequency layers of its central nucleus.

Effects of phase duration and pulse rate on loudness and pitch percepts in the first auditory midbrain implant patients: Comparison to cochlear implant and auditory brainstem implant results

The auditory midbrain implant (AMI), which is designed for stimulation of the inferior colliculus (IC), is now in clinical trials. The AMI consists of a single shank array (20 contacts) and uses a stimulation strategy originally designed for cochlear implants since it is already approved for human use and we do not yet know how to optimally activate the auditory midbrain. The goal of this study was to investigate the effects of different pulse rates and phase durations on loudness and pitch percepts because these parameters are required to implement the AMI stimulation strategy. Although each patient was implanted into a different region (i.e. lateral lemniscus, central nucleus of IC, dorsal cortex of IC), they generally exhibited similar threshold versus phase duration, threshold versus pulse rate, and pitch versus pulse rate curves. In particular, stimulation with 100 μs/phase, 250 pulse per second (pps) pulse trains achieved an optimal balance among safety, energy, and current threshold requirements while avoiding rate pitch effects. However, we observed large differences across patients in loudness adaptation to continuous pulse stimulation over long time scales. One patient (implanted in dorsal cortex of IC) even experienced complete loudness decay and elevation of thresholds with daily stimulation. Comparing these results with those of cochlear implant and auditory brainstem implant patients, it appears that stimulation of higher order neurons exhibits less and even no loudness summation for higher rate stimuli and greater current leakage for longer phase durations than that of cochlear neurons. The fact that all midbrain regions we stimulated, which includes three distinctly different nuclei, exhibited similar loudness summation effects (i.e. none for pulse rates above 250 pps) suggests a possible shift in some coding properties that is affected more by which stage along the auditory pathway rather than the types of neurons are being stimulated. However, loudness adaptation occurs at multiple stages from the cochlea up to the midbrain.

The auditory midbrain implant: Effects of electrode location

The auditory midbrain implant (AMI) is a new hearing prosthesis designed for stimulation of the inferior colliculus in patients who do not receive sufficient benefit from cochlear or brainstem prostheses. We have begun clinical trials in which three patients have been implanted with the AMI. Although the intended target was the central nucleus of the inferior colliculus (ICC), the electrode array was implanted into different locations across patients (i.e., ICC, dorsal cortex of inferior colliculus, lateral lemniscus). In this paper, we will summarize the effects of electrical stimulation of these different midbrain regions on various psychophysical properties and speech perception performance. The patient implanted within the intended target, the ICC, exhibited the greatest improvements in hearing performance. However, this patient has not yet achieved open-set speech perception to the performance level typically observed for cochlear implant patients, which we believe is partially due to the location of the array within the ICC. We will present findings from previous AMI studies in guinea pigs demonstrating the existence of spatially distinct functional output regions within the ICC and suggesting that further improvements in performance may be achieved by stimulating within a rostral-ventral region. Remaining questions include if a similar organization exists in the human ICC and if stimulation of its rostral-ventral region with currently available strategies (i.e., those designed for cochlear implants) can restore sufficient speech perception.

Electrical Stimulation of the Midbrain for Hearing Restoration: Insight into the Functional Organization of the Human Central Auditory System

The cochlear implant can restore speech perception in patients with sensorineural hearing loss. However, it is ineffective for those without an implantable cochlea or a functional auditory nerve. These patients can be implanted with the auditory brainstem implant (ABI), which stimulates the surface of the cochlear nucleus. Unfortunately, the ABI has achieved limited success in its main patient group [i.e., those with neurofibromatosis type 2 (NF2)] and requires a difficult surgical procedure. These limitations have motivated us to develop a new hearing prosthesis that stimulates the midbrain with a penetrating electrode array. We recently implanted three patients with the auditory midbrain implant (AMI), and it has proven to be safe with minimal movement over time. The AMI provides loudness, pitch, temporal, and directional cues, features that have shown to be important for speech perception and more complex sound processing. Thus far, all three patients obtain enhancements in lip reading capabilities and environmental awareness and some improvements in speech perception comparable with that of NF2 ABI patients. Considering that our midbrain target is more surgically exposable than the cochlear nucleus, this argues for the use of the AMI as an alternative to the ABI. Fortunately, we were able to stimulate different midbrain regions in our patients and investigate the functional organization of the human central auditory system. These findings provide some insight into how we may need to stimulate the midbrain to improve hearing performance with the AMI.

Auditory Midbrain Implant

Chronic implantation and electric stimulation with a human prototype auditory midbrain implant (AMI) array within the inferior colliculus achieves minimal neuronal damage and does not cause any severe complications. An AMI array has been developed for patients with neural deafness and, based on animal studies, has shown to possess potential as an auditory prosthesis in humans. To investigate the safety of the AMI for clinical use, we characterized the histomorphologic effects of chronic implantation and stimulation within its target structure, the inferior colliculus. Eight cats were chronically implanted for 3 months, and histologic sections were analyzed to assess long-term tissue effects. Four of the 8 cats were additionally stimulated for 60 days (4 h/d) starting 4 weeks after implantation to assess if clinically relevant stimuli further affected the tissue response. In general, both neurons and neuropil surrounding the implant track were apparently unaffected, whereas a fibrillary sheath (approximately 50 microm thick) developed around the array. There was a significant decrease in neuron density 50 to 100 microm away from the track with a significantly elevated number of glial cells out to approximately 250 to 350 microm. Chronic stimulation seemed to improve the tissue response and neuronal survival around the implant, although further studies are needed to confirm this finding. The histomorphologic effects and extent of neuronal damage observed for our AMI array are similar to those of other neural implants currently and safely used in humans. The minimal tissue damage surrounding the implanted array is encouraging with regard to the safety of the array for human use.

Spatially Distinct Functional Output Regions within the Central Nucleus of the Inferior Colliculus: Implications for an Auditory Midbrain Implant

The inferior colliculus central nucleus (ICC) has potential as a new site for an auditory prosthesis [i.e., auditory midbrain implant (AMI)] for deaf patients who cannot benefit from cochlear implants (CIs). We have previously shown that ICC stimulation achieves lower thresholds, greater dynamic ranges, and more localized, frequency-specific primary auditory cortex (A1) activation than CI stimulation. However, we also observed that stimulation location along the caudorostral (isofrequency) dimension of the ICC affects thresholds and frequency specificity in A1, suggesting possible differences in functional (output) organization within the ICC. In this study, we electrically stimulated different regions along the isofrequency laminas of the ICC and recorded the corresponding A1 activity in ketamine-anesthetized guinea pigs using multisite probes to systematically assess ICC stimulation location effects. Our results indicate that stimulation of more rostral and somewhat ventral regions within an ICC lamina achieves lower thresholds, smaller discriminable level steps, and larger evoked potentials in A1. We also observed longer first spike latencies, which correlated with reduced spiking precision, when stimulating in more caudal and dorsal ICC regions. These findings suggest that at least two spatially distinct functional output regions exist along an ICC lamina: a caudal-dorsal region and a rostral-ventral region. The AMI will be implanted along the tonotopic axis of the ICC to achieve frequency-specific activation. However, stimulation location along the ICC laminas affects response properties that have shown to be important for speech perception performance, and needs to be considered when implanting future AMI patients.

Auditory Midbrain Implant

The lateral suboccipital approach is a well-established route for safe removal of vestibular schwannomas in neurofibromatosis Type 2 (NF2) patients. The goal of this study was to assess if this approach can be extended to a lateral supracerebellar infratentorial approach to enable insertion of an auditory midbrain implant (AMI) penetrating array along the tonotopic gradient of the inferior colliculus central nucleus (ICC). The AMI is a new auditory prosthesis designed for penetrating stimulation of the ICC in patients with neural deafness. The initial candidates are NF2 patients who, because of the growth and/or surgical removal of bilateral acoustic neuromas, develop neural deafness and are unable to benefit from cochlear implants. The ideal surgical approach in NF2 patients must first enable safe removal of vestibular schwannomas and then provide sufficient exposure of the midbrain for AMI implantation. This study was performed on formalin-fixed and fresh cadaver specimens. Computed tomography scan and magnetic resonance imaging were used to study the heads of the specimens and for surgical navigation. The lateral suboccipital craniotomy enabled sufficient exposure of the cerebellopontine angle and internal auditory canal for tumor removal. It could then be extended to a lateral supracerebellar infratentorial approach that provided good exposure of the dorsolateral aspect of the tentorial hiatus and mesencephalon for implantation of the AMI along the tonotopic gradient of the ICC. This approach did not endanger the trochlear nerve or any major midline venous structures in the quadrigeminal cistern. This modified lateral suboccipital approach ensures safe removal of large vestibular schwannomas and provides sufficient exposure of the inferior colliculus for ideal AMI implantation.

Electrophysiological validation of a human prototype auditory midbrain implant in a guinea pig model.

The auditory midbrain implant (AMI) is a new treatment for hearing restoration in patients with neural deafness or surgically inaccessible cochleae who cannot benefit from cochlear implants (CI). This includes neurofibromatosis type II (NF2) patients who, due to development and/or removal of vestibular schwannomas, usually experience complete damage of their auditory nerves. Although the auditory brainstem implant (ABI) provides sound awareness and aids lip-reading capabilities for these NF2 patients, it generally only achieves hearing performance levels comparable with a single-channel CI. In collaboration with Cochlear Ltd. (Lane Cove, Australia), we developed a human prototype AMI, which is designed for electrical stimulation along the well-defined tonotopic gradient of the inferior colliculus central nucleus (ICC). Considering that better speech perception and hearing performance has been correlated with a greater number of discriminable frequency channels of information available, the ability of the AMI to effectively activate discrete frequency regions within the ICC may enable better hearing performance than achieved by the ABI. Therefore, the goal of this study was to investigate if our AMI array could achieve low-threshold, frequency-specific activation within the ICC, and whether the levels for ICC activation via AMI stimulation were within safe limits for human application. We electrically stimulated different frequency regions within the ICC via the AMI array and recorded the corresponding neural activity in the primary auditory cortex (A1) using a multisite silicon probe in ketamine-anesthetized guinea pigs. Based on our results, AMI stimulation achieves lower thresholds and more localized, frequency-specific activation than CI stimulation. Furthermore, AMI stimulation achieves cortical activation with current levels that are within safe limits for central nervous system stimulation. This study confirms that our AMI design is sufficient for ensuring safe and effective activation of the ICC, and warrants further studies to translate the AMI into clinical application.

The Auditory Midbrain Implant

The auditory midbrain implant (AMI) is a new central auditory prosthesis designed for penetrating stimulation of the human inferior colliculus. The major group of candidates for the AMI consists of neurofibromatosis type 2 (NF2) patients who develop neural deafness because of growth and/or surgical removal of bilateral acoustic neuromas. Because of the absence of a viable auditory nerve, these patients cannot benefit from cochlear implants. An alternative solution has been the auditory brainstem implant (ABI), which stimulates the cochlear nucleus. However, speech perception performance in NF2 ABI patients has been limited. The fact that the ABI is able to produce high levels of speech perception in nontumor patients (with inaccessible cochleae or posttraumatic damage to the cochlear nerve) suggests that limitations in ABI performance in NF2 patients may be associated with cochlear nucleus damage caused by the tumors or the tumor removal process. Thus, stimulation of the auditory midbrain proximal to the damaged cochlear nucleus may be a better alternative for hearing restoration in NF2 patients. We propose the central nucleus of the inferior colliculus (ICC) as the potential site. A penetrating electrode array aligned along the well-defined tonotopic gradient of the ICC should selectively activate different frequency regions, which is an important elementfor supporting good speech understanding. The goal of this article is to present the ICC as an alternative site for an auditory implant for NF2 patients and to describe the design of the first human prototype AMI. Practical considerations for implementation of the AMI will also be discussed.

Auditory Cortical Responses to Electrical Stimulation of the Inferior Colliculus: Implications for an Auditory Midbrain Implant

The success and limitations of cochlear implants (CIs) along with recent advances in deep brain stimulation and neural engineering have motivated the development of a central auditory prosthesis. In this study, we investigated the effects of electrical stimulation of the inferior colliculus central nucleus (ICC) on primary auditory cortex (A1) activity to determine the potential benefits of an auditory midbrain implant (AMI). We recorded multiunit activity in A1 of ketamine-anesthetized guinea pigs in response to single-pulse (200 micros/phase) monopolar stimulation of the ICC using multisite silicon-substrate probes. We then compared measures of threshold, dynamic range, and tonotopic spread of activation for ICC stimulation with that of published data for CI stimulation. Our results showed that compared with cochlear stimulation, ICC stimulation achieved: 1) thresholds about 8 dB lower; 2) dynamic ranges > or = 4 dB greater; and 3) more localized, frequency-specific activation, even though frequency specificity was partially lost at higher stimulus levels for low-frequency ICC regions. Our results also showed that stimulation of rostral ICC regions elicited lower thresholds but with greater activation spread along the tonotopic gradient of A1 than did stimulation of more caudal regions. These results suggest that an AMI may improve frequency and level coding with lower energy requirements compared with CIs. However, a trade-off between lower perceptual thresholds and better frequency discrimination may exist that depends on location of stimulation along the caudorostral dimension of the ICC. Overall, this study provides the foundation for future AMI research and development.

Auditory Rehabilitation with Cochlear Implants, Auditory Brainstem Implants and Auditory Midbrain Implants—A New Field for the Skull Base Surgeon

Auditory rehabilitation can be achieved with an auditory brainstem implant in patients with bilaterally missing or damaged auditory nerve. Since 1995, 28 patients suffering from neurofibromatosis type 2 or ossified cochlea have been selected out of a group of more than 300 patients fulfilling the following criteria: duration of deafness less than 10 years, otherwise healthy, high motivation, tumor removal possible. Objective audiometry and the electrical promontory test performed preoperatively must show neural deafness.

Electrophysiological Assessment and Validation of the Auditory Midbrain Implant (AMI)

Electrophysiological Assessment and Validation of the Auditory Midbrain Implant (AMI)