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.

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.

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.

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).

Single fiber mapping of spatial excitation patterns in the electrically stimulated auditory nerve.

Spatial maps of electrical excitation were constructed by comparing electrical threshold with acoustic CF for large populations of auditory nerve fibers in cats. Thresholds among fibers with the same CF varied by factors of 4 or more. Monopolar electrodes, both intracochlear and extracochlear, excited fibers throughout the cochlea without spatial selectivity. Stimulation with intracochlear bipolar electrodes produced a minimum in the threshold distribution adjacent to the electrodes. With longitudinally oriented pairs, the width, depth, and location of the minimum shifted with stimulus polarity; spread of excitation throughout the cochlea occurred with stimulus intensities 6.2 to 14 dB above the lowest threshold. With radially oriented pairs, minima were sharper and deeper; spread of excitation occurred at intensities 23.7 to 32.8 dB above the minimum threshold.

Temporal response patterns of single auditory nerve fibers elicited by periodic electrical stimuli.

Single auditory nerve fibers exhibit firing synchronized to one or both phases of periodic AC stimulus currents. Responses to biphasic pulses depend on order and excitation sites of the two phases. Sine and triangle stimuli between 100 Hz and 500 Hz elicit similar response patterns. Responses to square waves are sometimes more synchronized and generally shifted in phase with respect to sine wave responses. Preferred firing phase(s): (1) are largely independent of stimulus intensity; (2) vary among fibers; (3) may shift continuously or discontinuously over several seconds before steady state is achieved. Responses to an unprocessed synthetic vowel stimulus were dominated by pitch period, first formant, and 'spurious' components.

Electrophysiologic evaluation of the cochlear implant patient.

Electrically evoked auditory brain stem responses (EABRs) have been measured in experimental animals and human subjects. The EABR may hold promise as a clinical tool in the evaluation of the auditory system in candidates or users of cochlear prostheses.

Characterization of the electrically evoked auditory brainstem response (ABR) in cats and humans.

Electrically evoked auditory brainstem response (EABR) recordings were made from 38 humans implanted with one of three cochlear prostheses, and from 25 cats. Recognizable auditory potentials were identified in 27 of the profoundly deaf implanted subjects. In both cats and humans EABR waveform morphology and magnitude were independent of electrode configuration and paralleled those of the normal acoustic ABR, but with reduced absolute latencies. EABR recordings are highly susceptible to contamination by stimulus artifact and by elicited non-auditory potentials. Latency, morphology, and magnitude criteria are proposed for identification and analysis of EABR components.

Physiological properties of the electrically stimulated auditory nerve. I. Compound action potential recordings.

The electrically evoked compound action potential (CAP) of the auditory nerve exhibits two peaks, termed N0, at 350 microseconds latency, and N1, at 550 microseconds latency. At low stimulus intensities the CAP consists solely of the long latency N1 peak. As the stimulus strength is increased the higher threshold N0 appears. At high stimulus intensities N1 disappears and only the N0 component of the CAP remains. It is postulated that N1 represents action potentials propagated from the dendritic processes of the auditory neurons and that N0 represents action potentials initiated on the axons of these cells. The N1 peak exhibits anomalous refractory behavior which can be identified in the electrically evoked auditory brainstem response (EABR). That behavior may be useful diagnostically in assessing the extent of dendrite degeneration in cochlear implant candidates and users.

Physiological properties of the electrically stimulated auditory nerve. II. Single fiber recordings.

Single fiber recordings from the electrically stimulated auditory nerve yield post-stimulus time (PST) histograms demonstrating several response patterns. With pulsatile stimulation of the cochlea, the PST histogram for most fibers at threshold consists of a long-latency (500-800 microseconds), broad response peak with significant latency variability. At increased stimulus intensities, the response pattern changes to a short-latency (300-500 microseconds), high-synchrony peak. In preparations where stimulation is applied directly to the axons of the auditory nerve, the response pattern consists solely of a short-latency, high-synchrony peak. It is postulated that threshold excitation of normal auditory neurons occurs on the dendritic processes. At higher stimulus intensities, the site of excitation appears to shift to the axonal region of the cells. Two additional response patterns to electrical stimulation which are attributed to synaptic excitation of the auditory neurons via the hair cells are described.

Generation of unidirectionally propagated action potentials in a peripheral nerve by brief stimuli.

Single, unidirectionally propagated action potentials can be elicited in peripheral nerves by electrical stimuli of short duration. Propagation in one direction is blocked anodically by means of a quasi-trapezoidal stimulus wave form and a modified tripolar electrode configuration. Propagation in the other direction proceeds unhindered. This technique may be applicable to collision blocking of motor nerves for neural prostheses.