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.     

Cochlear implant electrode configuration effects on activation threshold and tonotopic selectivity

The multichannel design of contemporary cochlear implants (CIs) is predicated on the assumption that each channel activates a relatively restricted and independent sector of the deaf auditory nerve array, just as a sound within a restricted frequency band activates a restricted region of the normal cochlea The independence of CI channels, however, is limited; and the factors that determine their independence, the relative overlap of the activity patterns that they evoke, are poorly understood. In this study, we evaluate the spread of activity evoked by cochlear implant channels by monitoring activity at 16 sites along the tonotopic axis of the guinea pig inferior colliculus (IC). "Spatial tuning curves" (STCs) measured in this way serve as an estimate of activation spread within the cochlea and the ascending auditory pathways. We contrast natural stimulation using acoustic tones with two kinds of electrical stimulation either (1) a loose fitting banded array consisting of a cylindrical silicone elastomer carrier with a linear series of ring contacts; or (2) a space-filling array consisting of a tapered silicone elastomer carrier that is designed to fit snugly into the guinea pig scala tympani with a linear series of ball contacts positioned along it Spatial tuning curves evoked by individual acoustic tones, and by activation of each contact of each array as a monopole, bipole or tripole were recorded. Several channel configurations and a wide range of electrode separations were tested for each array, and their thresholds and selectivity were estimated. The results indicate that the tapered space-filling arrays evoked more restricted activity patterns at lower thresholds than did the banded arrays. Monopolar stimulation (one intracochlear contact activated with an extracochlear return) using either array evoked broad activation patterns that involved the entire recording array at current levels <6dBSL, but at relatively low thresholds. Bi- and tri-polar configurations of both array types evoked more restricted activity patterns, but their thresholds were higher than those of monopolar configurations. Bipolar and tripolar configurations with closely spaced contacts evoked activity patterns that were comparable to those evoked by pure tones. As the spacing of bipolar electrodes was increased (separations >1mm), the activity patterns became broader and evoked patterns with two distinct threshold minima, one associated with each contact.     

电刺激耳蜗记录下丘的空间调谐曲线

目的探索耳蜗电刺激的听觉中枢电活动机理，为多道人工耳蜗电刺激的部位代码提供生理依据。方法利用记录单单位和多单位电位反应的方法，分别描记１７只猫听觉下丘核团对耳蜗内单极电刺激，耳蜗内双极电刺激和纯音刺激反应的空间调谐曲线。结果耳蜗内双极电刺激能兴奋下丘中的特定区域，类似于对纯音刺激的反应；而耳蜗内单极电刺激使下丘细胞广泛地被兴奋，不能提供部位代码。结论使用双极电极时，刺激电流的局限范围是提高部位代码的关键；耳蜗内单极电刺激部位代码的电生理结果与心理物理学的结论以及人工耳蜗植入患者的临床效果相矛盾，对此的解释有待进一步研究。     

电刺激耳蜗记录下丘的空间调谐曲线

探索耳蜗电刺激的听觉中枢电活动机理，为多道人工耳蜗电刺激的部位代码提供依据。方法 利用记录单单位和多单位电位反应的方法，分别描记１７只猫听觉下丘核团对耳蜗内单极电刺激，耳蜗内双极电刺激和纯音刺激反应的空间调谐曲线。结果 耳蜗内双极电刺激能兴奋下丘中的特定区域，类似于纯音刺激的反应；而耳蜗内单极电刺激使下丘细胞广泛地被兴奋，不能提供部位代码。     

Binaural electric-acoustic interactions recorded from the inferior colliculus of Guinea pigs: the effect of masking observed in the central nucleus of the inferior colliculus

Objectives

To investigate the electric-acoustic interactions within the inferior colliculus of guinea pigs and to observe how central masking appears in invasive neural recordings of the inferior colliculus (IC).

Methods

A platinum-iridium wire was inserted to scala tympani through cochleostomy with a depth no greater than 1 mm for intracochlear stimulation of electric pulse train. A 5 mm 100 µm, single-shank, thin-film, penetrating recording probe was inserted perpendicularly to the surface of the IC in the coronal plane at an angle of 30-40° off the parasagittal plane with a depth of 2.0-2.5 mm. The peripheral and central masking effects were compared using electric pulse trains to the left ear and acoustic noise to the left ear (ipsilateral) and to the right ear (contralateral). Binaural acoustic stimuli were presented with different time delays and compared with combined electric and acoustic stimuli. The averaged evoked potentials and total spike numbers were measured using thin-film electrodes inserted into the central nucleus of the IC.

Results

Ipsilateral noise had more obvious effects on the electric response than did contralateral noise. Contralateral noise decreased slightly the response amplitude to the electric pulse train stimuli. Immediately after the onset of acoustic noise, the response pattern changed transiently with shorter response intervals. The effects of contralateral noise were evident at the beginning of the continuous noise. The total spike number decreased when the binaural stimuli reached the IC most simultaneously.

Conclusion

These results suggest that central masking is quite different from peripheral masking and occurs within the binaural auditory system, and this study showed that the effect of masking could be observed in the IC recording. These effects are more evident and consistent with the psychophysical data from spike number analyses than with the previously reported gross potential data.     

Chronic intracochlear electrical stimulation in the neonatally deafened cat. II. Temporal properties of neurons in the inferior colliculus.

The major focus of this study was to define the effects of chronic intracochlear electrical stimulation (ICES) on single unit responses in the inferior colliculus from three experimental groups: 1) normal adults 2) neonatally-deafened/unstimulated adults; and 3) neonatally-deafened/chronically stimulated adults. The major findings include: 1) IC neurons in normal adults showed a diversity of perstimulus responses to ICES which were qualitatively similar to those evoked by acoustic stimuli. They responded with: an onset burst, a sustained discharge, a decrease in their spontaneous activity, or a strong post-stimulus response. The excitatory responses showed either a monotonic or a nonmonotonic increase in activity with increasing stimulus intensity. Response latencies ranged from 5 to over 40 ms. 2) Responses to ICES in normal and deafened/unstimulated animals were virtually indistinguishable from one another. 3) In contrast, responses to ICES in neonatally deafened stimulated animals were different from normal and from deafened, unstimulated animals. Their perstimulus response latencies were significantly shorter, their late response latencies were significantly longer, and the frequency of occurrence of inhibitory and late responses were significantly higher. From these results we conclude that the responses to intracochlear electrical stimulation are directly comparable to those observed following normal acoustic stimulation; that development of cochleotopic organization of the inferior colliculus is not affected by the almost complete lack of normal acoustic input experienced by neonatally deafened animals; and that the basic response properties of IC units are likewise unaffected by neonatal deafening. Moreover, the results suggest that, although the limited regime of electrical stimulation employed in these studies produced no major qualitative distortions in the perstimulus response patterns of IC neurons, it did result in some quantitative changes in those responses.     

Electrode configuration influences action potential initiation site and ensemble stochastic response properties

The configuration of intracochlear electrodes used to electrically stimulate the auditory nerve influences the ensemble fiber response. For example, monopolar stimulation produces lower thresholds and greater spread of excitation than does bipolar stimulation. We used two approaches to investigate how the ensemble of auditory-nerve fibers responds to stimulation delivered by different electrode configurations. As the electrically evoked compound action potential (ECAP) reflects the ensemble response of the nerve, we used its morphology and changes with stimulus level to assess issues related to site-of-excitation and fiber recruitment. In our first approach, feline ECAPs were obtained using a nucleus-style banded electrode array. ECAP latency functions indicated that bipolar stimulation can initiate action potentials at more peripheral sites than does monopolar stimulation. We observed double-peaked ECAPs with bipolar and tripolar stimulation, suggesting excitation of both peripheral and central neural processes. Finally, we observed in some cases a tendency for monopolar stimulation to produce wider ECAP potentials, consistent with the notion that monopolar stimulation excites a broader spatial extent of the fiber population. In our second approach, we applied a simple model to published surveys of single-fiber responses to provide insight into the stochastic properties of the ensemble response. Our results suggest that broader recruitment of fiber activity produced by monopolar stimulation results in a population response with more probabilistic response characteristics and ensemble spike jitter. These observations and our ECAP results are consistent with reports of perceptual advantages attributed to monopolar or other less-focused modes of stimulation.     

Cortical Responses to Cochlear Implant Stimulation: Channel Interactions

This study examined the interactions between electrical stimuli presented through two channels of a cochlear implant. Experiments were conducted in anesthetized guinea pigs. Multiunit spike activity recorded from the auditory cortex reflected the cumulative effects of electric field interactions in the cochlea as well as any neural interactions along the ascending auditory pathway. The cochlea was stimulated electrically through a 6-electrode intracochlear array. The stimulus on each channel was a single 80-µs/phase biphasic pulse. Channel interactions were quantified as changes in the thresholds for elevation of cortical spike rates. Experimental parameters were interchannel temporal offset (0 to ±2000 µs), interelectrode cochlear spacing (1.5 or 2.25 mm), electrode configuration (monopolar, bipolar, or tripolar), and relative polarity between channels (same or inverted). In most conditions, presentation of a subthreshold pulse on one channel reduced the threshold for a pulse on a second channel. Threshold shifts were greatest for simultaneous pulses, but appreciable threshold reductions could persist for temporal offsets up to 640 µs. Channel interactions varied strongly with electrode configuration: threshold shifts increased in magnitude in the order tripolar, bipolar, monopolar. Channel interactions were greater for closer electrode spacing. The results have implications for design of speech processors for cochlear implants. Current address (Julie Arenberg Bierer): Epstein Laboratory, Box 0526, University of California, San Francisco, CA 94143-0526, USA.     

Rate and Temporal Coding of Regular and Irregular Pulse Trains in Auditory Midbrain of Normal-Hearing and Cochlear-Implanted Rabbits

Although pitch is closely related to temporal periodicity, stimuli with a degree of temporal irregularity can evoke a pitch sensation in human listeners. However, the neural mechanisms underlying pitch perception for irregular sounds are poorly understood. Here, we recorded responses of single units in the inferior colliculus (IC) of normal hearing (NH) rabbits to acoustic pulse trains with different amounts of random jitter in the inter-pulse intervals and compared with responses to electric pulse trains delivered through a cochlear implant (CI) in a different group of rabbits. In both NH and CI animals, many IC neurons demonstrated tuning of firing rate to the average pulse rate (APR) that was robust against temporal jitter, although jitter tended to increase the firing rates for APRs ≥ 1280 Hz. Strength and limiting frequency of spike synchronization to stimulus pulses were also comparable between periodic and irregular pulse trains, although there was a slight increase in synchronization at high APRs with CI stimulation. There were clear differences between CI and NH animals in both the range of APRs over which firing rate tuning was observed and the prevalence of synchronized responses. These results suggest that the pitches of regular and irregular pulse trains are coded differently by IC neurons depending on the APR, the degree of irregularity, and the mode of stimulation. In particular, the temporal pitch produced by periodic pulse trains lacking spectral cues may be based on a rate code rather than a temporal code at higher APRs.     

Electrically Evoked Auditory Steady State Responses in Cochlear Implant Users

Auditory steady state responses are neural potentials in response to repeated auditory stimuli. This study shows that electrically evoked auditory steady state responses (EASSRs) to low-rate pulse trains can be reliably recorded by electrodes placed on the scalp of a cochlear implant (CI) user and separated from the artifacts generated by the electrical stimulation. Response properties are described, and the predictive value of EASSRs for behaviorally hearing thresholds is analyzed. For six users of a Cochlear Nucleus CI, EASSRs to symmetric biphasic pulse trains with rates between 35 and 47 Hz were recorded with seven scalp electrodes. The influence of various stimulus parameters was assessed: pulse rate, stimulus intensity, monopolar or bipolar stimulation mode, and presentation of either one pulse train on one electrode or interleaved pulse trains with different pulse rates on multiple electrodes. To compensate for the electrical artifacts caused by the stimulus pulses and radio frequency transmission, different methods of artifact reduction were employed. The validity of the recorded responses was confirmed by recording on–off responses, determination of response latency across the measured pulse rates, and comparison of amplitude growth of stimulus artifact and response amplitude. For stimulation in the 40 Hz range, response latencies of 35.6 ms (SD = 5.3 ms) were obtained. Responses to multiple simultaneous stimuli on different electrodes can be evoked, and the electrophysiological thresholds determined from EASSR amplitude growth in the 40 Hz range correlate well with behaviorally determined threshold levels for pulse rates of 41 Hz.     

Responses of inferior colliculus neurons to harmonic and mistuned complex tones

Responses of inferior colliculus neurons to simplified stimuli that may engage mechanisms that contribute to auditory scene analysis were obtained. The stimuli were harmonic complex tones, which are heard by human listeners as single sounds, and the same tones with one component 'mistuned', which are heard as two separate sounds. The temporal discharge pattern elicited by a harmonic complex tone usually resembled the same neuron's response to a pure tone. In contrast, tones with a mistuned component elicited responses with distinctive, stereotypical temporal patterns that were not obviously related to the stimulus waveform. For a particular stimulus configuration, the discharge pattern was similar across neurons with different pure-tone frequency selectivity. A computational model that compared response envelopes across multiple narrow bands successfully reproduced the stereotypical response patterns elicited by different stimulus configurations. The results suggest that mistuning created a temporally synchronous distributed representation of the mistuned component that could be identified by higher auditory centers in the presence of the ongoing response produced by the remaining components; this kind of representation might facilitate the identification of individual sound sources in complex acoustic environments.     

Changes in Auditory Nerve Responses Across the Duration of Sinusoidally Amplitude-Modulated Electric Pulse-Train Stimuli

Response rates of auditory nerve fibers (ANFs) to electric pulse trains change over time, reflecting substantial spike-rate adaptation that depends on stimulus parameters. We hypothesize that adaptation affects the representation of amplitude-modulated pulse trains used by cochlear prostheses to transmit speech information to the auditory system. We recorded cat ANF responses to sinusoidally amplitude-modulated (SAM) trains with 5,000 pulse/s carriers. Stimuli delivered by a monopolar intracochlear electrode had fixed modulation frequency (100 Hz) and depth (10%). ANF responses were assessed by spike-rate measures, while representation of modulation was evaluated by vector strength (VS) and the fundamental component of the fast Fourier transform (F₀ amplitude). These measures were assessed across the 400 ms duration of pulse-train stimuli, a duration relevant to speech stimuli. Different stimulus levels were explored and responses were categorized into four spike-rate groups to assess level effects across ANFs. The temporal pattern of rate adaptation to modulated trains was similar to that of unmodulated trains, but with less rate adaptation. VS to the modulator increased over time and tended to saturate at lower spike rates, while F₀ amplitude typically decreased over time for low driven rates and increased for higher driven rates. VS at moderate and high spike rates and degree of F₀ amplitude temporal changes at low and moderate spike rates were positively correlated with the degree of rate adaptation. Thus, high-rate carriers will modify the ANF representation of the modulator over time. As the VS and F₀ measures were sensitive to adaptation-related changes over different spike-rate ranges, there is value in assessing both measures.     

Models of Brainstem Responses to Bilateral Electrical Stimulation

A simple, biophysically specified cell model is used to predict responses of binaurally sensitive neurons to patterns of input spikes that represent stimulation by acoustic and electric waveforms. Specifically, the effects of changes in parameters of input spike trains on model responses to interaural time difference (ITD) were studied for low-frequency periodic stimuli, with or without amplitude modulation. Simulations were limited to purely excitatory, bilaterally driven cell models with basic ionic currents and multiple input fibers. Parameters explored include average firing rate, synchrony index, modulation frequency, and latency dispersion of the input trains as well as the excitatory conductance and time constant of individual synapses in the cell model. Results are compared to physiological recordings from the inferior colliculus (IC) and discussed in terms of ITD-discrimination abilities of listeners with cochlear implants. Several empirically observed aspects of ITD sensitivity were simulated without evoking complex neural processing. Specifically, our results show saturation effects in rate–ITD curves, the absence of sustained responses to high-rate unmodulated pulse trains, the renewal of sensitivity to ITD in high-rate trains when inputs are amplitude-modulated, and interactions between envelope and fine-structure delays for some modulation frequencies.     

Perceptual dissimilarities among acoustic stimuli and ipsilateral electric stimuli

Five users of cochlear implants who had residual acoustic hearing in the implanted ear postoperatively participated in a study comparing the percepts elicited by acoustic and electric stimuli. The stimuli comprised pulse trains delivered to single electrodes and pure tones presented ipsilaterally. In the experiments, 12 equally loud stimuli with differing frequencies, electrode positions, and pulse rates were generated. Subjects listened to all of the possible pairs of stimuli in each set, and provided a relative dissimilarity rating for the members of each stimulus pair. The data were analyzed using non-metric multi-dimensional scaling techniques. Stimulus spaces were plotted in two dimensions to represent the results for each subject with each stimulus set. The results suggested that one dimension was associated with a pitch-like percept, related to the acoustic tone frequency and the active electrode position. The second dimension separated the acoustic stimuli from the electric stimuli. Generally, the electric pulse rate seemed to have a relatively small perceptual effect in this experimental context. Overall, the results show that acoustic pure tones are perceived as very different from electric pulse trains delivered to single electrode positions with constant rate, even when both the acoustic and the electric stimuli are presented to the same ear.     

Temporal integration of electrical stimulation of auditory nuclei in normal-hearing and hearing-impaired cat

Temporal integration functions were measured, before and after a sound-induced hearing loss, in 5 cats using trains of electrical pulses applied to auditory nuclei in the brainstem. The 8 stimuli ranged from 1 pulse (0.25 ms duration) to 16 pulses (0.25 ms pulses spaced over 240 ms). The stimuli were applied to inferior colliculus or cochlear nucleus via permanently implanted electrodes. One electrode was tested extensively in each animal to obtain 10 sets of behaviorally-measured electrical detection thresholds counterbalanced across stimuli. The animal was then exposed to a 110 dB SPL, 2 kHz tone for 48 h and pre- and post-exposure audiograms were measured. The mean permanent threshold shift for acoustic stimuli was 48.5 dB. Another 10 thresholds for each of the 8 electrical stimuli were then measured. In the normal hearing animals, the mean slope of the temporal integration function for electrical stimulation was -7.6 dB per factor of 10 pulses. Alternatively, the mean time constant was 139 ms. In the hearing impaired animals, the slope was reduced to -1.5 dB per factor of 10 pulses, which corresponded to a mean time constant of 17 ms. In addition, the hearing impaired animals showed a decreased threshold for the electrical stimuli (stimulation hypersensitivity) as well as reduced variability across electrical stimulation thresholds. The results suggest that a major contribution to temporal integration occurs in inferior colliculus or higher. In addition, the results suggest that the reduction in temporal integration that follows hearing impairment is a peripherally-induced, central effect.     

Intraoperative facial nerve monitoring: a comparison of stimulating electrodes

Preservation of the facial nerve during acoustic neuroma resection may be enhanced by the use of intraoperative electrical stimulation. Although stimulation of the extratemporal facial nerve is an effective and established procedure, anatomic differences of the intradural facial nerve and its microenvironment demand more exacting stimulus protocols. The absence of epineurium may make the intradural nerve more susceptible to mechanical or electrical trauma while intermittent pooling of cerebrospinal fluid (CSF) at the cerebellopontine angle may shunt current away from nerve. Four stimulus configurations were examined under varying conditions simulating CSF pooling. The results indicated that: 1. insulation of stimulating electrodes prevents CSF current shunting and allows utilization of a constant current source, and 2. monopolar and bipolar configurations demonstrate significantly different electrical characteristics which may be employed selectively based upon specific clinical goals.     

Binaural interactions of electrically and acoustically evoked responses recorded from the inferior colliculus of guinea pigs

Binaural interactions within the inferior colliculus (IC) elicited by electric and acoustic stimuli were investigated in this study. Using a guinea pig model, binaural acoustic stimuli were presented with different time delays, as were combinations of binaural electric and acoustic stimuli. Averaged evoked potentials were measured using electrodes inserted into the central nucleus of the IC to obtain the binaural interaction component (BIC), computed by subtracting the sum of the two monaural responses from the binaural response. The BICs to acoustic-acoustic stimulation and electric-acoustic stimulation were found to be similar. The BIC amplitude increased with stimulus intensity, but the shapes of the delay functions were similar across the levels tested. The gross-potential data are thus consistent with the thesis that the central auditory system processes binaural electric and acoustic stimuli in a similar manner. These results suggest that the binaural auditory system can process combinations of electric and acoustic stimulation presented across ears and that evoked gross potentials may be used to measure such interaction.     

Binaural interactions of electrically and acoustically evoked responses recorded from the inferior colliculus of guinea pigs

Binaural interactions within the inferior colliculus (IC) elicited by electric and acoustic stimuli were investigated in this study. Using a guinea pig model, binaural acoustic stimuli were presented with different time delays, as were combinations of binaural electric and acoustic stimuli. Averaged evoked potentials were measured using electrodes inserted into the central nucleus of the IC to obtain the binaural interaction component (BIC), computed by subtracting the sum of the two monaural responses from the binaural response. The BICs to acoustic-acoustic stimulation and electric-acoustic stimulation were found to be similar. The BIC amplitude increased with stimulus intensity, but the shapes of the delay functions were similar across the levels tested. The gross-potential data are thus consistent with the thesis that the central auditory system processes binaural electric and acoustic stimuli in a similar manner. These results suggest that the binaural auditory system can process combinations of electric and acoustic stimulation presented across ears and that evoked gross potentials may be used to measure such interaction.     

An experimental study on the auditory brainstem response to electrical stimulation of the cochlea

This animal research was undertaken to study some important issues for cochlear implantation. This included investigations of 1) the difference in the auditory brainstem responses (ABRs) to extra- and intracochlear electrical stimulations. 2) stimulus parameters and ABRs to a bipolar intracochlear stimulation, and 3) electrode placements and ABRs. There were no distinct differences in waveforms and input-output curves of ABRs between extracochlear electrical stimulation and intracochlear bipolar stimulation of the cochlea. Changes in amplitude and latency of ABRs were investigated at changes of the pulse amplitude or the pulse width of stimulating electric rectangular waves. Increase in the pulse amplitude or the pulse width resulted in increase of the amplitude of ABRs and no increase in the ABR latency. This results showed the amplitude of ABR was dependent on the amount of electricity; coulomb. Electrically evoked ABRs were studied for stimulations at different sites of the cochlea. The ABR elicited with a bipolar electrode placed at the third turn of the cochlea had a longer latency of each peak of ABR waves than the one at the basal turn. This indicates that electrical stimulation with a bipolar electrode can give rise to a localized excitation in the cochlea and a latency change along the longitudinal axis of the cochlea, so that it suggests a multichannel cochlea implant system can transmit more information as a spacious pattern than a single channel system.