Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation.

To understand the auditory neural response to electrical stimuli similar to those used in a cochlear implant, it will be necessary to understand the neural refraction and summation response kinetics. Evidence exists indicating that the cell soma may alter the auditory neural response kinetics and could be the site of conduction failure for excitation initiated on the peripheral process. There is, however, reason to believe that the excitation site in some healthy, type I neurons and in pathological, type III neurons is the central process of the cell. To characterize the neural response to activation at a controlled central process site, cat auditory neurons were stimulated with an intrameatal electrode, and the summation and refraction response kinetics were measured. This approach was used to: (1) characterize the behavior of the neural response to central process excitation; (2) make comparisons between intrameatal excitation at a known central site and scala tympani excitation at an unknown site; and (3) provide membrane characterization free from the possible alteration of membrane kinetics produced by the cell soma. The membrane kinetics measured using intrameatal stimulation differ from those recorded with scala tympani stimulation indicating that the mechanisms for scala tympani and intrameatal stimulation differ.

Pseudospontaneous activity: stochastic independence of auditory nerve fibers with electrical stimulation.

We describe a novel signal processing strategy for cochlear implants designed to emphasize stochastic independence across the excited neural population. The strategy is based on the observation that high rate pulse trains may produce random spike patterns in auditory nerve fibers that are statistically similar to those produced by spontaneous activity in the normal cochlea. We call this activity 'pseudospontaneous'. A supercomputer-based computational model of a population of auditory nerve fibers suggests that different average rates of pseudospontaneous activity can be created by varying the stimulus current of a fixed-amplitude, high-rate pulse train, e.g. 5000 pps. Electrically-evoked compound action potentials recorded in a human cochlear implant subject are consistent with the hypothesis that such a stimulus can desynchronize the fiber population. This desynchronization may enhance neural representation of temporal detail and dynamic range with a cochlear implant and eliminate a major difference between acoustic and electric hearing.

Bilateral cochlear implants controlled by a single speech processor.

OBJECTIVE: This study aimed to assess, in one profoundly hearing impaired subject, potential benefits and limitations in placing bilaterally implanted scala tympani electrode arrays under control of a single speech processor. STUDY DESIGN: All available stimulation sites in both ears were compared in studies of pitch discrimination and pitch ranking, identifying three bilateral pairs capable of supporting interaural comparisons with no perceptible difference in pitch. Using those pairs, the subject's ability to lateralize sound was studied as a function of interaural time delay and interaural amplitude difference. Consonant identification scores were obtained for continuous interleaved sampling processors using various unilateral and bilateral combinations of electrodes. RESULTS: For loudness-matched stimuli composed of 50-msec bursts of 80-microsec/phase pulses at 480 pulses/sec, the subject was able to identify the ear receiving the earlier onset for interaural delays at least as brief as 150 microsec for all three matched pairs. For similar simultaneous stimuli, the subject could identify the ear receiving the louder signal for the smallest deviations from loudness-matched amplitudes available from the implanted electronics. The consonant studies found no evidence that bilateral stimulation per se degrades speech processor performance, even for arbitrary divisions of information between the two ears. Additional contralateral as well as ipsilateral channels were observed to improve speech processor performance. CONCLUSIONS: The ability of this subject to lateralize sounds on the basis of interaural delay or loudness difference, combined with the consonant identification results, supports further use of coordinated binaural stimulation to improve cochlear implant users' ability to understand speech, especially in the presence of competing speech noise.

Temporal representations with cochlear implants.

OBJECTIVE: To record and characterize intracochlear evoked potentials (EPs) for a variety of electrical stimuli in studies with cochlear implant patients. METHODS: Recordings were made with patients having direct percutaneous access to their implanted electrodes. Intracochlear voltages were recorded via unstimulated electrodes. The stimuli included trains of identical pulses, with pulse rates ranging from 100 to 4065/s, and a modulated pulse train produced by a single-channel speech processor, with the pulse rate of 824/s. RESULTS: Magnitudes of EPs for each pulse in trains of identical pulses were uniform for pulse rates below about 200/s. For rates between about 400 and 1000/s, an alternating pattern of EP magnitudes was observed, with relatively large EPs following the odd-numbered pulses. For rates between about 1000 and 3000/s, more complex patterns were observed. After the first millisecond of each train at even higher rates, uniform EPs again were observed across pulses, although the absolute magnitude of the EPs was much lower than that observed for low rates of stimulation. The approximate rates corresponding to boundaries between these different regions varied among subjects and among electrodes within subjects. EP magnitudes for the modulated pulse train reflected the gross periodicity of the modulation waveform but did not reflect temporal details within the periods. CONCLUSIONS: Population responses of the human auditory nerve, as indicated by EP magnitudes, reflect the amplitudes of electrical pulses for pulse rates below about 200/s and above about 3000/s. Use of intermediate rates may introduce distortions in the transmission of stimulus information with cochlear implants.

Microstimulation of auditory nerve for estimating cochlear place of single fibers in a deaf ear.

Multielectrode cochlear prostheses seek to approximate the cochlea's normal frequency-place mapping through spatial segregation of stimulus currents. Various electrode configurations have been employed to achieve such segregation. Direct measurements of stimulation regions among single auditory nerve (AN) fibers has been possible only when normal hearing is preserved, such that each fiber's cochlear place can be inferred from its tuning curve. This precludes measurements in deafened ears, or ears compromised by implantation of the electrodes. Data presented here demonstrate that the cochlear place of an AN fiber can be estimated without acoustic sensitivity, using electrical microstimulation through a recording pipette in the AN bundle. The procedure exploits cochleotopic projection to isofrequency laminae within the contralateral inferior colliculus (IC). Microstimulation excites a small group of fibers neighboring the recorded fiber, generating centrally propagated volleys along a narrow frequency-specific pathway. Evoked potential recordings at varying depths are made to identify the ICC lamina where the response to AN microstimulation is greatest. Preliminary data are also presented for an alternative method of identifying the lamina using a frequency domain measure of binaural interactions within the IC.

Cochlear implant studies at Research Triangle Institute and Duke University Medical Center.

Examples from several areas of cochlear implant research are presented, with emphasis on the continuous interleaved sampling (CIS) approach to speech processor design. Within-subject comparisons of such processors with the compressed analog (CA) approach of the clinical Ineraid device are reviewed, and ongoing similar comparisons with the clinical Nucleus spectral peak (SPEAK) strategy are outlined. Correlations between chronic performance levels with clinical CA processors and initial performance levels with CIS, data on further improvements in performance with chronic use of CIS, and instances of substantial benefit from custom fitting of CIS parameters are presented as examples of findings with immediate clinical implications. New studies are described, involving the measurement of intracochlear evoked potentials in response to cochlear implant stimulation, and the integration of such work with computer modeling studies.

Effects of electrode configuration on psychophysical strength-duration functions for single biphasic electrical stimuli in cats.

The interface between electrode and neural target tissue is thought to influence certain characteristics of neural and behavioral responses to electrical stimulation of the auditory system. At present, the biophysical properties of this interface are not well understood. Here the effects of biphasic phase duration and electrode configuration on psychophysical threshold in response to electrical stimulation in cats are described. Five cats were trained to respond to acoustic stimuli using food as a reward in an operant reinforcement paradigm. After training, the animals were unilaterally deafened and implanted with a multicontact intracochlear electrode array. Thresholds for single presentations of biphasic current pulses were measured as a function of phase duration and electrode arrangement. Statistical analyses of the data indicated that strength-duration function slopes between 200 and 1600 microseconds/phase were significantly different for the different electrode configurations and, overall, were unrelated to the absolute level of the strength-duration function (i.e., were independent of absolute threshold). For all subjects, the slope of this function for intermediate pulse durations was dependent on electrode configuration and most shallow for radial-bipolar configurations (-3.4 dB/doubling), was steepest for monopolar arrangements (-5.9 dB/doubling), and was intermediate for longitudinal-bipolar pairings. (-4.4 dB/doubling). Slopes for both shorter and longer phase duration stimuli were not significantly different. The underlying mechanisms for these effects may include, or be a combination of altered electrical field patterns, integrated activity across multiple fibers, and stochastic behavior of individual auditory neurons to electrical stimulation.

New processing strategies in cochlear implantation.

New strategies for representing acoustic information with multichannel cochlear implants have produced substantial improvements in speech recognition for implant users. This report reviews within-subject comparison of a new continuous interleaved sampling (CIS) strategy with a compressed analog (CA) strategy used in a standard clinical device. In general, the comparison show higher levels of open-set speech recognition with CIS for each of the 11 subjects studied. Data on the importance of the patients variable in determining outcomes with cochlear implants are presented. A brief description of another new strategy, the spectral maxima sound processor (SMSP) strategy is given as well as information on the availability of CIS in various implant systems.

Behavioral and electrophysiological responses to electrical stimulation in the cat. I. Absolute thresholds.

Estimates of electrical auditory brainstem response (EABR) thresholds are compared with behavioral thresholds for electrical stimulation in the same subject using identical stimuli and electrode configurations. Four cats were behaviorally trained to measure acoustic auditory thresholds using food as a reward in an operant reinforcement paradigm. One of the animals was then implanted, in an otherwise normal ear, with a scaled-UCSF multi-contact electrode array containing four intracochlear electrodes. Three animals were implanted with an electrode array containing eight intracochlear contacts and one extracochlear contact under the temporalis muscle following unilateral cochlear perfusion with 10% neomycin solution. Stimuli for the behavioral studies were single presentations of 200 us/phase biphasic current pulses. For the EABR studies, the same stimulus was presented at a rate of 32/s. In general, for the animal with the four-contact array and two of the three subjects with the eight-contact implant, changes in electrode configuration produced well-differentiated changes in threshold. For these three subjects, comparisons of behavioral and EABR thresholds for the majority of monopolar and bipolar electrode configurations tested showed excellent agreement (r2 = 0.88). Correlations between behavioral and EABR measures in these animals were comparable for bipolar and monopolar arrangements (r2 = 0.88 for bipolar and 0.87 for monopolar). For one subject with the eight-contact electrode, who showed similar monopolar and bipolar electrode behavioral thresholds for all tested electrode spacings or configurations, most EABR thresholds were substantially higher than, and poorly correlated with, behavioral thresholds (r2 = 0.15; r2 = 0.28 for monopolar arrangements, and r2 = 0.12 for bipolar arrangements).

Importance of patient and processor variables in determining outcomes with cochlear implants.

Within-subjects comparisons of processing strategies for cochlear implants are reviewed. Compressed analog strategies were compared to interleaved pulses strategies in tests with one group of 8 subjects, and to continuous interleaved sampling strategies in tests with another group of 11 subjects. The tests included open-set recognition of words and sentences. The results show that, while different strategies may produce quite different outcomes across subjects, individual performances with one processing strategy are significantly correlated with those of alternative strategies. These findings emphasize the importance of patient variables in determining outcomes across a variety of prosthesis designs.

New processing strategies for multichannel cochlear prostheses.

Various strategies for representing speech information with multichannel cochlear prostheses were compared in tests with implant patients. The strategies included the compressed analog (CA) approach of a standard clinical device, and alternative interleaved pulses (IP) and continuous interleaved sampling (CIS) strategies. CA and IP strategies had been compared in previous studies with a wide range of subjects. The present studies compared all three types in tests with one subject and CA and CIS strategies in tests with six additional subjects. Subjects for the present studies were selected for their excellent performance with the clinical CA processor, and the tests included closed-set identification of consonants and open-set recognition of words and sentences. For every test, every subject obtained his or her highest score, or repeated a score of 100% correct, using a CIS strategy. In the comparisons of all three approaches, IP processor scores were between those obtained with CA and CIS processors. The results are discussed in terms of their implications for processor design.

Design and evaluation of a continuous interleaved sampling (CIS) processing strategy for multichannel cochlear implants.

Two approaches for representing speech information with multichannel cochlear prostheses are being compared in tests with implant patients. Included in these studies are the compressed analog (CA) approach of a standard clinical device and research processors utilizing continuous interleaved sampling (CIS). Initial studies have been completed with nine subjects, seven of whom were selected on the basis of excellent performance with the Ineraid clinical processor, and the remaining two for their relatively poor performance with the same device. The tests include open-set recognition of words and sentences. Every subject has obtained a higher score--or repeated a score of 100% correct--on every test when using a CIS processor. These results are discussed in terms of their implications for processor design.

Better speech recognition with cochlear implants.

HIGH levels of speech recognition have been achieved with a new sound processing strategy for multielectrode cochlear implants. A cochlear implant system consists of one or more implanted electrodes for direct electrical activation of the auditory nerve, an external speech processor that transforms a microphone input into stimuli for each electrode, and a transcutaneous (rf-link) or percutaneous (direct) connection between the processor and the electrodes. We report here the comparison of the new strategy and a standard clinical processor. The standard compressed analogue (CA) processor presented analogue waveforms simultaneously to all electrodes, whereas the new continuous interleaved sampling (CIS) strategy presented brief pulses to each electrode in a nonoverlapping sequence. Seven experienced implant users, selected for their excellent performance with the CA processor, participated as subjects. The new strategy produced large improvements in the scores of speech reception tests for all subjects. These results have important implications for the treatment of deafness and for minimal representations of speech at the auditory periphery.

Coding strategies for multichannel cochlear prostheses.

Comparisons of analog and pulsatile coding strategies for multichannel cochlear prostheses are reviewed. The results are related to design considerations for pediatric implants, including efficacy, safety, ease of fitting, and access to future improvements.

Comparative studies of speech processing strategies for cochlear implants.

A wide variety of speech processing strategies for multichannel auditory prostheses were compared in studies of two patients implanted with the UCSF electrode array. Each strategy was evaluated using tests of vowel and consonant confusions, with and without lipreading. Included among the strategies were the compressed analog processor of the present UCSF/Storz prosthesis and a group of interleaved pulses processors in which the amplitudes of nonsimultaneous pulses code the spectral variations of speech. For these patients, each with indications of poor nerve survival, test scores were significantly higher with the interleaved pulses processors. We believe this superior performance was a result of 1. the substantial release from channel interactions provided by nonsimultaneous stimuli and 2. a fast enough rotation among the channels to support adequate temporal and spectral resolution of perceived speech sounds.

Spinal cord seizures elicited by high pressures of helium.

Rats with complete spinal transections were compressed in helium-oxygen to 120 bars. Tremors and increased EMG activity in limbs rostral as well as caudal to the lesions were observed beginning at 30 bars. Spinal seizures occurred at 95 bars, similar to cortical seizure thresholds of intact rats. Denervated limbs remained flaccid throughout the dives. No rostro-caudal progression of symptoms was evident in normal animals, but fluctuation of symptoms with increasing pressure was frequently observed. These findings are consistent with the hypothesis that the effects of pressure on aggregates of neurons exceed those on isolated components.