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 μs/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 ≥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.

Download Full-text

Stimulation-mapping of the upper human auditory pathway

Journal of Neurosurgery ◽

10.3171/jns.1973.38.3.0320 ◽

1973 ◽

Vol 38 (3) ◽

pp. 320-325 ◽

Cited By ~ 9

Author(s):

Ronald R. Tasker ◽

L. W. Organ

Keyword(s):

Electrical Stimulation ◽

Auditory Cortex ◽

Brain Stem ◽

Inferior Colliculus ◽

Primary Auditory Cortex ◽

Auditory Pathway ◽

Association Cortex ◽

Content Type ◽

Medial Geniculate ◽

Stimulation Of

✓ Auditory hallucinations were produced by electrical stimulation of the human upper brain stem during stereotaxic operations. The responses were confined to stimulation of the inferior colliculus, brachium of the inferior colliculus, medial geniculate body, and auditory radiations. Anatomical confirmation of an auditory site was obtained in one patient. The hallucination produced was a low-pitched nonspecific auditory “paresthesia” independent of the structure stimulated, the conditions of stimulation, or sonotopic factors. The effect was identical to that reported from stimulating the primary auditory cortex, and virtually all responses were contralateral. These observations have led to the following generalizations concerning electrical stimulation of the somesthetic, auditory, vestibular, and visual pathways within the human brain stem: the hallucination induced in each is the response to comparable conditions of stimulation, is nonspecific, independent of stimulation site, confined to the primary pathway concerned, chiefly contralateral, and identical to that induced by stimulating the corresponding primary auditory cortex. No sensory responses are found in the brain stem corresponding to those from the sensory association cortex.

Download Full-text

Coactivation of different neurons within an isofrequency lamina of the inferior colliculus elicits enhanced auditory cortical activation

Journal of Neurophysiology ◽

10.1152/jn.00111.2012 ◽

2012 ◽

Vol 108 (4) ◽

pp. 1199-1210 ◽

Cited By ~ 10

Author(s):

Roger Calixto ◽

Minoo Lenarz ◽

Anke Neuheiser ◽

Verena Scheper ◽

Thomas Lenarz ◽

...

Keyword(s):

Inferior Colliculus ◽

Temporal Integration ◽

Three Dimensional ◽

Primary Auditory Cortex ◽

Cortical Activation ◽

Central Nucleus ◽

Speech Understanding ◽

Auditory Midbrain ◽

Temporal Cues ◽

Multiple Regions

The phenomenal success of the cochlear implant (CI) is attributed to its ability to provide sufficient temporal and spectral cues for speech understanding. Unfortunately, the CI is ineffective for those without a functional auditory nerve or an implantable cochlea required for CI implementation. As an alternative, our group developed and implanted in deaf patients a new auditory midbrain implant (AMI) to stimulate the central nucleus of the inferior colliculus (ICC). Although the AMI can provide frequency cues, it appears to insufficiently transmit temporal cues for speech understanding. The three-dimensional ICC consists of two-dimensional isofrequency laminae. The single-shank AMI only stimulates one site in any given ICC lamina and does not exhibit enhanced activity (i.e., louder percepts or lower thresholds) for repeated pulses on the same site with intervals <2–5 ms, as occurs for CI pulse or acoustic click stimulation. This enhanced activation, related to short-term temporal integration, is important for tracking the rapid temporal fluctuations of a speech signal. Therefore, we investigated the effects of coactivation of different regions within an ICC lamina on primary auditory cortex activity in ketamine-anesthetized guinea pigs. Interestingly, our findings reveal an enhancement mechanism for integrating converging inputs from an ICC lamina on a fast scale (<6-ms window) that is compromised when stimulating just a single ICC location. Coactivation of two ICC regions also reduces the strong and long-term (>100 ms) suppressive effects induced by repeated stimulation of just a single location. Improving AMI performance may require at least two shanks implanted along the tonotopic gradient of the ICC that enables coactivation of multiple regions along an ICC lamina with the appropriate interstimulus delays.

Download Full-text

Passive stimulation and behavioral training differentially transform temporal processing in the inferior colliculus and primary auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.00392.2016 ◽

2017 ◽

Vol 117 (1) ◽

pp. 47-64 ◽

Cited By ~ 12

Author(s):

Maike Vollmer ◽

Ralph E. Beitel ◽

Christoph E. Schreiner ◽

Patricia A. Leake

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

Temporal Processing ◽

Electric Stimulation ◽

Primary Auditory Cortex ◽

Central Nucleus ◽

Electrophysiological Recording ◽

Response Patterns ◽

Behavioral Training ◽

Auditory Midbrain

In profoundly deaf cats, behavioral training with intracochlear electric stimulation (ICES) can improve temporal processing in the primary auditory cortex (AI). To investigate whether similar effects are manifest in the auditory midbrain, ICES was initiated in neonatally deafened cats either during development after short durations of deafness (8 wk of age) or in adulthood after long durations of deafness (≥3.5 yr). All of these animals received behaviorally meaningless, “passive” ICES. Some animals also received behavioral training with ICES. Two long-deaf cats received no ICES prior to acute electrophysiological recording. After several months of passive ICES and behavioral training, animals were anesthetized, and neuronal responses to pulse trains of increasing rates were recorded in the central (ICC) and external (ICX) nuclei of the inferior colliculus. Neuronal temporal response patterns (repetition rate coding, minimum latencies, response precision) were compared with results from recordings made in the AI of the same animals (Beitel RE, Vollmer M, Raggio MW, Schreiner CE. J Neurophysiol 106: 944–959, 2011; Vollmer M, Beitel RE. J Neurophysiol 106: 2423–2436, 2011). Passive ICES in long-deaf cats remediated severely degraded temporal processing in the ICC and had no effects in the ICX. In contrast to observations in the AI, behaviorally relevant ICES had no effects on temporal processing in the ICC or ICX, with the single exception of shorter latencies in the ICC in short-deaf cats. The results suggest that independent of deafness duration passive stimulation and behavioral training differentially transform temporal processing in auditory midbrain and cortex, and primary auditory cortex emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf cat. NEW & NOTEWORTHY Behaviorally relevant vs. passive electric stimulation of the auditory nerve differentially affects neuronal temporal processing in the central nucleus of the inferior colliculus (ICC) and the primary auditory cortex (AI) in profoundly short-deaf and long-deaf cats. Temporal plasticity in the ICC depends on a critical amount of electric stimulation, independent of its behavioral relevance. In contrast, the AI emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf auditory system.

Download Full-text