Effect of Pulse Rate and Polarity on the Sensitivity of Auditory Brainstem and Cochlear Implant Users to Electrical Stimulation

To further understand the response of the human brainstem to electrical stimulation, a series of experiments compared the effect of pulse rate and polarity on detection thresholds between auditory brainstem implant (ABI) and cochlear implant (CI) patients. Experiment 1 showed that for 400-ms pulse trains, ABI users’ thresholds dropped by about 2 dB as pulse rate was increased from 71 to 500 pps, but only by an average of 0.6 dB as rate was increased further to 3500 pps. This latter decrease was much smaller than the 7.7-dB observed for CI users. A similar result was obtained for pulse trains with a 40-ms duration. Furthermore, experiment 2 showed that the threshold difference between 500- and 3500-pps pulse trains remained much smaller for ABI than for CI users, even for durations as short as 2 ms, indicating the effect of a fast-acting mechanism. Experiment 3 showed that ABI users’ thresholds were lower for alternating-polarity than for fixed-polarity pulse trains, and that this difference was greater at 3500 pps than at 500 pps, consistent with the effect of pulse rate on ABI users’ thresholds being influenced by charge interactions between successive biphasic pulses. Experiment 4 compared thresholds and loudness between trains of asymmetric pulses of opposite polarity, in monopolar mode, and showed that in both cases less current was needed when the anodic, rather than the cathodic, current was concentrated into a short time interval. This finding is similar to that previously observed for CI users and is consistent with ABI users being more sensitive to anodic than cathodic current. We argue that our results constrain potential explanations for the differences in the perception of electrical stimulation by CI and ABI users, and have potential implications for future ABI stimulation strategies.     

Delayed Auditory Brainstem Responses in Prelingually Deaf and Late-Implanted Cochlear Implant Users

Neurophysiological studies in animals and humans suggest that severe hearing loss during early development impairs the maturation of the auditory brainstem. To date, studies in humans have mainly focused on the neural activation of the auditory brainstem in children treated with a cochlear implant (CI), but little is known about the pattern of activation in adult CI users with early onset of deafness (prelingual, before the age of 2 years). In this study, we compare auditory brainstem activation in prelingually deaf and late-implanted adult CI users to that in postlingually deaf CI users. Electrically evoked auditory brainstem responses (eABRs) were recorded by monopolar stimulation, separately using a middle and an apical electrode of the CI. Comparison of the eABR latencies revealed that wave V was significantly delayed in the prelingually deaf CI users on both electrode locations. Accordingly, when the apical electrode was stimulated, the III–V interwave interval was significantly longer in the prelingually deaf group. These findings suggest a slower neural conduction in the auditory brainstem, probably caused by impairment of maturation during the long duration of severe hearing loss in infancy. Shorter wave V latencies, reflecting a more mature brainstem, appeared to be a predictor for better speech perception.     

Sensitivity to Interaural Time Differences with Combined Cochlear Implant and Acoustic Stimulation

The interaural time difference (ITD) is an important cue to localize sound sources. Sensitivity to ITD was measured in eight users of a cochlear implant (CI) in the one ear and a hearing aid (HA) in the other severely impaired ear. The stimulus consisted of an electric pulse train of 100 pps and an acoustic filtered click train. Just-noticeable differences (JNDs) in ITD were measured using a lateralization paradigm. Four subjects exhibited median JNDs in ITD of 156, 341, 254, and 91 μs; the other subjects could not lateralize the stimuli consistently. Only the subjects who could lateralize had average acoustic hearing thresholds at 1,000 and 2,000 Hz better than 100-dB SPL. The electric signal had to be delayed by 1.5 ms to achieve synchronous stimulation at the auditory nerves.

Using Evoked Potentials to Match Interaural Electrode Pairs with Bilateral Cochlear Implants

Bilateral cochlear implantation seeks to restore the advantages of binaural hearing to the profoundly deaf by providing binaural cues normally important for accurate sound localization and speech reception in noise. Psychophysical observations suggest that a key issue for the implementation of a successful binaural prosthesis is the ability to match the cochlear positions of stimulation channels in each ear. We used a cat model of bilateral cochlear implants with eight-electrode arrays implanted in each cochlea to develop and test a noninvasive method based on evoked potentials for matching interaural electrodes. The arrays allowed the cochlear location of stimulation to be independently varied in each ear. The binaural interaction component (BIC) of the electrically evoked auditory brainstem response (EABR) was used as an assay of binaural processing. BIC amplitude peaked for interaural electrode pairs at the same relative cochlear position and dropped with increasing cochlear separation in either direction. To test the hypothesis that BIC amplitude peaks when electrodes from the two sides activate maximally overlapping neural populations, we measured multiunit neural activity along the tonotopic gradient of the inferior colliculus (IC) with 16-channel recording probes and determined the spatial pattern of IC activation for each stimulating electrode. We found that the interaural electrode pairings that produced the best aligned IC activation patterns were also those that yielded maximum BIC amplitude. These results suggest that EABR measurements may provide a method for assigning frequency–channel mappings in bilateral implant recipients, such as pediatric patients, for which psychophysical measures of pitch ranking or binaural fusion are unavailable.     

Modulation Enhancement in the Electrical Signal Improves Perception of Interaural Time Differences with Bimodal Stimulation

Interaural timing cues are important for sound source localization and for binaural unmasking of speech that is spatially separated from interfering sounds. Users of a cochlear implant (CI) with residual hearing in the non-implanted ear (bimodal listeners) can only make very limited use of interaural timing cues with their clinical devices. Previous studies showed that bimodal listeners can be sensitive to interaural time differences (ITDs) for simple single- and three-channel stimuli. The modulation enhancement strategy (MEnS) was developed to improve the ITD perception of bimodal listeners. It enhances temporal modulations on all stimulated electrodes, synchronously with modulations in the acoustic signal presented to the non-implanted ear, based on measurement of the amplitude peaks occurring at the rate of the fundamental frequency in voiced phonemes. In the first experiment, ITD detection thresholds were measured using the method of constant stimuli for five bimodal listeners for an artificial vowel, processed with either the advanced combination encoder (ACE) strategy or with MEnS. With MEnS, detection thresholds were significantly lower, and for four subjects well within the physically relevant range. In the second experiment, the extent of lateralization was measured in three subjects with both strategies, and ITD sensitivity was determined using an adaptive procedure. All subjects could lateralize sounds based on ITD and sensitivity was significantly better with MEnS than with ACE. The current results indicate that ITD cues can be provided to bimodal listeners with modified sound processing.     

Electrical Excitation of the Acoustically Sensitive Auditory Nerve: Single-Fiber Responses to Electric Pulse Trains

Nearly all studies on auditory-nerve responses to electric stimuli have been conducted using chemically deafened animals so as to more realistically model the implanted human ear that has typically been profoundly deaf. However, clinical criteria for implantation have recently been relaxed. Ears with “residual” acoustic sensitivity are now being implanted, calling for the systematic evaluation of auditory-nerve responses to electric stimuli as well as combined electric and acoustic stimuli in acoustically sensitive ears. This article presents a systematic investigation of single-fiber responses to electric stimuli in acoustically sensitive ears. Responses to 250 pulse/s electric pulse trains were collected from 18 cats. Properties such as threshold, dynamic range, and jitter were found to differ from those of deaf ears. Other types of fiber activity observed in acoustically sensitive ears (i.e., spontaneous activity and electrophonic responses) were found to alter the temporal coding of electric stimuli. The electrophonic response, which was shown to greatly change the information encoded by spike intervals, also exhibited fast adaptation relative to that observed in the “direct” response to electric stimuli. More complex responses, such as “buildup” (increased responsiveness to successive pulses) and “bursting” (alternating periods of responsiveness and unresponsiveness) were observed. Our findings suggest that bursting is a response unique to sustained electric stimulation in ears with functional hair cells.     

Interaural Time-Delay Sensitivity in Bilateral Cochlear Implant Users: Effects of Pulse Rate, Modulation Rate, and Place of Stimulation

Electrical interaural time delay (ITD) discrimination was measured using 300-ms bursts applied to binaural pitch matched electrodes at basal, mid, and apical locations in each ear. Six bilateral implant users, who had previously shown good ITD sensitivity at a pulse rate of 100 pulses per second (pps), were assessed. Thresholds were measured as a function of pulse rate between 100 and 1,000 Hz, as well as modulation rate over that same range for high-rate pulse trains at 6,000 pps. Results were similar for all three places of stimulation and showed decreasing ITD sensitivity as either pulse rate or modulation rate increased, although the extent of that effect varied across subjects. The results support a model comprising a common ITD mechanism for high- and low-frequency places of stimulation, which, for electrical stimulation, is rate-limited in the same way across electrodes because peripheral temporal responses are largely place invariant. Overall, ITD sensitivity was somewhat better with unmodulated pulse trains than with high-rate pulse trains modulated at matched rates, although comparisons at individual rates showed that difference to be significant only at 300 Hz. Electrodes presenting with the lowest thresholds at 600 Hz were further assessed using bursts with a ramped onset of 10 ms. The slower rise time resulted in decreased performance in four of the listeners, but not in the two best performers, indicating that those two could use ongoing cues at 600 Hz. Performance at each place was also measured using single-pulse stimuli. Comparison of those data with the unmodulated 300-ms burst thresholds showed that on average, the addition of ongoing cues beyond the onset enhanced overall ITD sensitivity at 100 and 300 Hz, but not at 600 Hz. At 1,000 Hz, the added ongoing cues actually decreased performance. That result is attributed to the introduction of ambiguous cues within the physiologically relevant range and increased dichotic firing.     

Auditory Nerve Fiber Responses to Combined Acoustic and Electric Stimulation

Persons with a prosthesis implanted in a cochlea with residual acoustic sensitivity can, in some cases, achieve better speech perception with “hybrid” stimulation than with either acoustic or electric stimulation presented alone. Such improvements may involve “across auditory-nerve fiber” processes within central nuclei of the auditory system and within-fiber interactions at the level of the auditory nerve. Our study explored acoustic–electric interactions within feline auditory nerve fibers (ANFs) so as to address two goals. First, we sought to better understand recent results that showed non-monotonic recovery of the electrically evoked compound action potential (ECAP) following acoustic masking (Nourski et al. 2007, Hear. Res. 232:87–103). We hypothesized that post-masking changes in ANF temporal properties and responsiveness (spike rate) accounted for the ECAP results. We also sought to describe, more broadly, the changes in ANF responses that result from prior acoustic stimulation. Five response properties—spike rate, latency, jitter, spike amplitude, and spontaneous activity—were examined. Post-masking reductions in spike rate, within-fiber jitter and across-fiber variance in latency were found, with the changes in temporal response properties limited to ANFs with high spontaneous rates. Thus, our results suggest how non-monotonic ECAP recovery occurs for ears with spontaneous activity, but cannot account for that pattern of recovery when there is no spontaneous activity, including the results from the presumably deafened ears used in the Nourski et al. (2007) study. Finally, during simultaneous (electric+acoustic) stimulation, the degree of electrically driven spike activity had a strong influence on spike rate, but did not affect spike jitter, which apparently was determined by the acoustic noise stimulus or spontaneous activity.     

Effects of Pulse Phase Duration and Location of Stimulation Within the Inferior Colliculus on Auditory Cortical Evoked Potentials in a Guinea Pig Model

The auditory midbrain implant (AMI), which consists of a single shank array designed for stimulation within the central nucleus of the inferior colliculus (ICC), has been developed for deaf patients who cannot benefit from a cochlear implant. Currently, performance levels in clinical trials for the AMI are far from those achieved by the cochlear implant and vary dramatically across patients, in part due to stimulation location effects. As an initial step towards improving the AMI, we investigated how stimulation of different regions along the isofrequency domain of the ICC as well as varying pulse phase durations and levels affected auditory cortical activity in anesthetized guinea pigs. This study was motivated by the need to determine in which region to implant the single shank array within a three-dimensional ICC structure and what stimulus parameters to use in patients. Our findings indicate that complex and unfavorable cortical activation properties are elicited by stimulation of caudal–dorsal ICC regions with the AMI array. Our results also confirm the existence of different functional regions along the isofrequency domain of the ICC (i.e., a caudal–dorsal and a rostral–ventral region), which has been traditionally unclassified. Based on our study as well as previous animal and human AMI findings, we may need to deliver more complex stimuli than currently used in the AMI patients to effectively activate the caudal ICC or ensure that the single shank AMI is only implanted into a rostral–ventral ICC region in future patients.     

Limitations on Monaural and Binaural Temporal Processing in Bilateral Cochlear Implant Listeners

Monaural rate discrimination and binaural interaural time difference (ITD) discrimination were studied as functions of pulse rate in a group of bilaterally implanted cochlear implant users. Stimuli for the rate discrimination task were pulse trains presented to one electrode, which could be in the apical, middle, or basal part of the array, and in either the left or the right ear. In each two-interval trial, the standard stimulus had a rate of 100, 200, 300, or 500 pulses per second and the signal stimulus had a rate 35 % higher. ITD discrimination between pitch-matched electrode pairs was measured for the same standard rates as in the rate discrimination task and with an ITD of +/− 500 μs. Sensitivity (d′) on both tasks decreased with increasing rate, as has been reported previously. This study tested the hypothesis that deterioration in performance at high rates occurs for the two tasks due to a common neural basis, specific to the stimulation of each electrode. Results show that ITD scores for different pairs of electrodes correlated with the lower rate discrimination scores for those two electrodes. Statistical analysis, which partialed out overall differences between listeners, electrodes, and rates, supports the hypothesis that monaural and binaural temporal processing limitations are at least partly due to a common mechanism.     

Cross Correlation by Neurons of the Medial Superior Olive: a Reexamination

Initial analysis of interaural temporal disparities (ITDs), a cue for sound localization, occurs in the superior olivary complex. The medial superior olive (MSO) receives excitatory input from the left and right cochlear nuclei. Its neurons are believed to be coincidence detectors, discharging when input arrives simultaneously from the two sides. Many current psychophysical models assume a strict version of coincidence, in which neurons of the MSO cross correlate their left and right inputs. However, there have been few tests of this assumption. Here we examine data derived from two earlier studies of the MSO and compare the responses to the output of a computational model. We find that the MSO is not an ideal cross correlator. Ideal cross correlation implies a strict relationship between the precision of phase-locking of the inputs and the range of ITDs to which a neuron responds. This relationship does not appear to be met. Instead, the modeling implies that a neuron responds over a wider range of ITDs than expected from the inferred precision of phase-locking of the inputs. The responses are more consistent with a scheme in which the neuron can also be activated by the input from one side alone. Such activation degrades the tuning of neurons in the MSO to ITDs.     

Effects of Temporal Fine Structure on the Lateralization of Speech and on Speech Understanding in Noise

This study evaluated the role of temporal fine structure in the lateralization and understanding of speech in six normal-hearing listeners. Interaural time differences (ITDs) were introduced to invoke lateralization. Speech reception thresholds (SRTs) were evaluated in backgrounds of two-talker babble and speech-shaped noise. Two-syllable words with ITDs of 0 and 700 μs were used as targets. A vocoder technique, which systematically randomized fine structure, was used to evaluate the effects of fine structure on these tasks. Randomization of temporal fine structure was found to significantly reduce the ability of normal-hearing listeners to lateralize words, although for many listeners, good lateralization performance was achieved with as much as 80% fine-structure randomization. Most listeners demonstrated some rudimentary ability to lateralize with 100% fine-structure randomization. When ITDs were 0 μs, randomization of fine structure had a much greater effect on SRT in two-talker babble than in speech-shaped noise. Binaural advantages were also observed. In steady noise, the difference in SRT between words with 0- vs 700-μs ITDs was, on average, 6 dB with no fine-structure randomization and 2 dB with 100% fine-structure randomization. In two-talker babble this difference was 1.9 dB and, for most listeners, showed little effect of the degree of fine-structure randomization. These results suggest that (1) improved delivery of temporal fine structure would improve speech understanding in noise for implant recipients, (2) bilateral implant recipients might benefit from temporal envelope ITDs, and (3) improved delivery of temporal information could improve binaural benefits.     

Auditory Brainstem Models: Adapting Cochlear Nuclei Improve Spatial Encoding by the Medial Superior Olive in Reverberation

Listeners typically perceive a sound as originating from the direction of its source, even as direct sound is followed milliseconds later by reflected sound from multiple different directions. Early-arriving sound is emphasised in the ascending auditory pathway, including the medial superior olive (MSO) where binaural neurons encode the interaural-time-difference (ITD) cue for spatial location. Perceptually, weighting of ITD conveyed during rising sound energy is stronger at 600 Hz than at 200 Hz, consistent with the minimum stimulus rate for binaural adaptation, and with the longer reverberation times at 600 Hz, compared with 200 Hz, in many natural outdoor environments. Here, we computationally explore the combined efficacy of adaptation prior to the binaural encoding of ITD cues, and excitatory binaural coincidence detection within MSO neurons, in emphasising ITDs conveyed in early-arriving sound. With excitatory inputs from adapting, nonlinear model spherical bushy cells (SBCs) of the bilateral cochlear nuclei, a nonlinear model MSO neuron with low-threshold potassium channels reproduces the rate-dependent emphasis of rising vs. peak sound energy in ITD encoding; adaptation is equally effective in the model MSO. Maintaining adaptation in model SBCs, and adjusting membrane speed in model MSO neurons, ‘left’ and ‘right’ populations of computationally efficient, linear model SBCs and MSO neurons reproduce this stronger weighting of ITD conveyed during rising sound energy at 600 Hz compared to 200 Hz. This hemispheric population model demonstrates a link between strong weighting of spatial information during rising sound energy, and correct unambiguous lateralisation of a speech source in reverberation.     

Interaction of cochlear nucleus explants with semiconductor materials

OBJECTIVE/HYPOTHESIS: Implantable hearing devices such as cochlear implants and auditory brainstem implants deliver auditory information through electrical stimulation of auditory neurons. The combination of microelectronic electrodes with auditory nerve cells may lead to further improvement of the hearing quality with these devices. Whereas several kinds of neurons are known to grow on semiconductor substrates, interactions of cochlear nucleus (CN) neurons with such materials have yet to be described. MATERIALS AND METHODS: To investigate survival and growth behavior of CN neurons on different semiconductor materials. CN explants from postnatal day 10 Sprague-Dawley rats were cultured for 96 hours in Neurobasal medium on polished and unpolished silicon wafers (p-type Si [100] and p-type Si3N4[100]) as well as plastic surface. These surfaces had been coated with poly-L-lysine and laminin. Neuronal outgrowth was examined using image analysis software after immunohistologic staining for neurofilament. Neurite length and directional changes were quantified. Additionally, neurite morphology and adhesion to the semiconductor material was evaluated by scanning electron microscopy. RESULTS: Although proper adhesion of CN explants was seen, no neurite growth could be detected on unpolished silicon wafers (Si and Si3N4). Compared with the other test conditions, polished, laminin-coated Si3N4 wafers showed best biocompatibility regarding neurite length and number per explant. CN explants developed a mean of eight neurons with an average length of 236 mum in 96 hours of culture on these wafers. CONCLUSION: The results of this study demonstrate the general possibility of CN neuron growth in culture on semiconductors in vitro. The differences in neuron length and number per explant indicate that the growth of CN neurons is influenced by the semiconductor substrate as well as extracellular matrix proteins, with laminin-coated p-type Si3N4[100] being a preferable material for future hybrid experiments on auditory-neuron semiconductor chips.     

Desynchronisation of auditory steady-state responses related to changes in interaural phase differences: an objective measure of binaural hearing

Objective: Binaural processing can be measured objectively as a desynchronisation of phase-locked neural activity to changes in interaural phase differences (IPDs). This was reported in a magnetoencephalography study for 40?Hz amplitude modulated tones. The goal of this study was to measure this desynchronisation using electroencephalography and explore the outcomes for different modulation frequencies. Design: Auditory steady-state responses (ASSRs) were recorded to pure tones, amplitude modulated at 20, 40 or 80?Hz. IPDs switched between 0 and 180° at fixed time intervals. Study sample: Sixteen young listeners with bilateral normal hearing thresholds (≤25?dB HL at 125–8000?Hz) participated in this study. Results: Significant ASSR phase desynchronisations to IPD changes were detected in 14 out of 16 participants for 40?Hz and in 8, respectively 9, out of 13 participants for 20 and 80?Hz modulators. Desynchronisation and restoration of ASSR phase took place significantly faster for 80?Hz than for 40 and 20?Hz. Conclusions: ASSR desynchronisation to IPD changes was successfully recorded using electroencephalography. It was feasible for 20, 40 and 80?Hz modulators and could be an objective tool to assess processing of changes in binaural information.     

Effects of Electrical Stimulation of Olivocochlear Fibers in Cochlear Potentials in the Chinchilla

The mammalian cochlea has two types of sensory cells; inner hair cells, which receive auditory-nerve afferent innervation, and outer hair cells, innervated by efferent axons of the medial olivocochlear (MOC) system. The role of the MOC system in hearing is still controversial. Recently, by recording cochlear potentials in behaving chinchillas, we suggested that one of the possible functions of the efferent system is to reduce cochlear sensitivity during attention to other sensory modalities (Delano et al. in J Neurosci 27:4146–4153, 2007). However, in spite of these compelling results, the physiological effects of electrical MOC activation on cochlear potentials have not been described in detail in chinchillas. The main objective of the present work was to describe these efferent effects in the chinchilla, comparing them with those in other species and in behavioral experiments. We activated the MOC efferent axons in chinchillas with sectioned middle-ear muscles by applying current pulses at the fourth-ventricle floor. Auditory-nerve compound action potentials (CAP) and cochlear microphonics (CM) were acquired in response to clicks and tones of several frequencies, using a round-window electrode. Electrical efferent stimulation produced CAP amplitude suppressions reaching up to 11 dB. They were higher for low to moderate sound levels. Additionally, CM amplitude increments were found, the largest (≤ 2.5 dB) for low intensity tones. CAP suppression was present at all stimulus frequencies, but was greatest for 2 kHz. CM increments were highest for low-frequency tones, and almost absent at high frequencies. We conclude that the effect obtained in chinchilla is similar to but smaller than that observed in cats, and that the effects seen in awake chinchillas, albeit different in magnitude, are consistent with the activation of efferent fibers.     

Topographic Spread of Inferior Colliculus Activation in Response to Acoustic and Intracochlear Electric Stimulation

The design of contemporary multichannel cochlear implants is predicated on the presumption that they activate multiple independent sectors of the auditory nerve array. The independence of these channels, however, is limited by the spread of activation from each intracochlear electrode across the auditory nerve array. In this study, we evaluated factors that influence intracochlear spread of activation using two types of intracochlear electrodes: (1) a clinical-type device consisting of a linear series of ring contacts positioned along a silicon elastomer carrier, and (2) a pair of visually placed (VP) ball electrodes that could be positioned independently relative to particular intracochlear structures, e.g., the spiral ganglion. Activation spread was estimated by recording multineuronal evoked activity along the cochleotopic axis of the central nucleus of the inferior colliculus (ICC). This activity was recorded using silicon-based single-shank, 16-site recording probes, which were fixed within the ICC at a depth defined by responses to acoustic tones. After deafening, electric stimuli consisting of single biphasic electric pulses were presented with each electrode type in various stimulation configurations (monopolar, bipolar, tripolar) and/or various electrode orientations (radial, off-radial, longitudinal). The results indicate that monopolar (MP) stimulation with either electrode type produced widepread excitation across the ICC. Bipolar (BP) stimulation with banded pairs of electrodes oriented longitudinally produced activation that was somewhat less broad than MP stimulation, and tripolar (TP) stimulation produced activation that was more restricted than MP or BP stimulation. Bipolar stimulation with radially oriented pairs of VP ball electrodes produced the most restricted activation. The activity patterns evoked by radial VP balls were comparable to those produced by pure tones in normal-hearing animals. Variations in distance between radially oriented VP balls had little effect on activation spread, although increases in interelectrode spacing tended to reduce thresholds. Bipolar stimulation with longitudinally oriented VP electrodes produced broad activation that tended to broaden as the separation between electrodes increased.