Guinea pig auditory nerve response triggered by a high density electrode array.

The electrically evoked potential in the auditory nerve is measured when the cochlear is stimulated with a high density electrode array whose microcontacts (20 x 160 microns) are placed close to the nerve cells. Threshold range from 8 to 35 microA with the stimulating electrodes near the spiral ganglion cells. A multi-pole technique for restricting the spread of current with electrical stimulation of the cochlea is tested using neural recording in deafened guinea pigs. The ground based quadrupolar electrode driving configuration has thresholds for neural activation only slightly greater than monopolar stimulation when the electrode contacts are placed less than 50 microns from the neurons. During simultaneous stimulation the monopole and the ground based quadrupolar modes tend to generate similar growth functions (magnitude and latency). The electrode interactions are generally factorial, which means that the algebraic sum of the responses (magnitude growth functions) produced by 2 distinct electrodes is less than when the same 2 electrodes are stimulated simultaneously.

Quadrupolar stimulation for Cochlear prostheses: modeling and experimental data.

Cochlear implants are electrically driven in monopolar, bipolar, or common ground mode. Ideally, a quadrupolar mode is created with three colinear electrodes, where the outer poles are half the inverse polarity value of the center electrode. The resulting field is highly focused. Models of point sources show that the quadrupolar paradigm offers a greater choice of parameters to shape the field. Simulation with a lumped-parameter model of the cochlea confirms the focusing action of the quadrupole in the layers of the inner ear. Field measurements in saline solution and in the scala tympani of guinea pigs show that focusing occurs with the quadrupolar mode. It is conceivable that quadrupolar stimulation will affect the pitch place coding, reduce channel interaction and limit facial or tactile stimulation induced by current spread.

Electrode configuration and spread of neural excitation: compartmental models of spiral ganglion cells.

A compartmental model of spiral ganglion cells in a potential field was used to predict spike discharges to electrical stimuli. The field was generated by monopolar, bipolar, or quadrupolar point source electrode geometries. The discharges of a population of afferent neurons were modeled to compare the relative spread of excitation. At the same stimulus intensity the spread of excitation was least for the quadrupolar and greatest for the radial bipolar, and this ordering held after equating for maximal spike discharge rates over the three geometries. Excitation spread from quadrupolar stimulation was highly dependent on stimulus intensity.

Effects of electrical current configuration on stimulus detection.

Psychophysical detection of electrical stimulation of the cochlea was studied as a function of electrical-current configuration. Subjects were postlingually deaf humans with Nucleus 20 + 2, Nucleus 22, and Ineraid cochlear implants and nonhuman primates unilaterally deafened and implanted with a multielectrode array similar to the Nucleus implant. In nonhuman primate and human Ineraid subjects, which had percutaneous connectors, we compared threshold functions for sinusoids and pulse trains for quadrupolar, bipolar, monopolar, and parallel multipolar stimulation. Thresholds decreased across this set of configurations. In some cases, the effects of current configuration were dependent on sinusoidal frequency and pulse duration. Pulse duration-dependent effects were also seen when comparing bipolar, monopolar, and common-ground configurations. Bipolar and monopolar stimulation were compared in Nucleus subjects using pulse trains at 50 microseconds per phase. For bipolar stimulation, thresholds decreased as a function of electrode separation, reaching a level near that for monopolar stimulation at separations of 3.5 to 6.5 mm in most cases. These results may be interpreted in terms of effects of current configuration on the magnitude and shape of electrical-potential fields produced in the cochlea, although more central factors also play a role in determining psychophysical detection thresholds.

Effects of electrical current configuration on potential fields in the electrically stimulated cochlea: field models and measurements.

Potential distributions measured within the scala tympani of the anesthetized guinea pig support the assertion that focusing is possible when currents are appropriately delivered to the electrodes in the scala tympani. Results obtained with a lumped-element model agree with measurements made in the inner ears of monkeys during monopolar and bipolar stimulation. The predictions are closer for potential distributions apical to the stimulating electrode than they are for basal distributions. In one monkey, in which electrodes were implanted in the middle ear as well as in the inner ear, we obtained measurements of the impedance from inside the scala tympani to points within the middle ear. These impedances are smaller that those initially used in the model, in which the round window membrane was assumed to have a relatively high impedance. A model of the common ground configuration was developed using finite electrode impedances. Finite impedances broaden the potential distributions in this model. Potential distributions from the lumped element model are compared with those obtained with an analytical model, to suggest ways in which focused and unfocused stimuli can affect the excitation of neurons in the implanted ear.

Shared-stimulus driving and connectivity in groups of neurons in the dorsal cochlear nucleus.

Extracellular spike discharges were recorded from ensembles of up to five neurons simultaneously in the DCN of guinea pig using solid-state, thin-film, multichannel electrodes having up to five recording sites spanning up to 600 microns. Responses from 73 unit pairs were collected of which 54 had both units responding to pseudorandom wideband noise stimulation. Shared-stimulus driving was present in 78% (42/54) of the unit pairs and could be attributed to an overlap in their spectral sensitivities. Effective connectivity was indicated for 87% (47/54) of the unit pairs. Wideband noise proved more useful than tonebursts for investigating shared-stimulus driving and connectivity because it evoked widespread, but not overly synchronous, responses in the ensembles.

A spectrotemporal analysis of DCN single unit responses to wideband noise in guinea pig.

Spectrotemporal receptive fields (STRFs) were estimated for chopper and pauser units recorded in guinea pig dorsal cochlear nucleus (DCN). Sixteen wideband, periodic noise stimuli, represented as time-frequency surfaces of energy density, were cross correlated in time with the unit's corresponding period histograms to determine if specific energy patterns tended to precede spike occurrence. The STRFs obtained were unique to the DCN, as compared to the ventral cochlear nucleus (VCN) [Clopton and Backoff, 1991, Hear. Res. 52, 329-344] in their degree of temporal and spectral complexity. Certain unit response types, classified from their peristimulus-time histograms (PSTHs) to tonebursts, were associated with distinctive patterns in the STRFs. All STRFs had at least one region of elevated energy density (peak region) closely preceding spike occurrence, which may reflect a short-pathway, primary excitatory input (or inputs) to the neuron. In addition, some units displayed low-energy regions (troughs) with greater temporal precedences on their STRFs, particularly when higher stimulus intensities were used. This analysis approach appears to have potential for investigating functional neural connectivity and predicting responses to novel complex stimuli, although specific implementations of the technique impose limitations on the interpretation of results.

Spectrotemporal receptive fields of neurons in cochlear nucleus of guinea pig.

Spectrotemporal receptive fields (STRFs) [Hermes et al., Hear. Res. 5, 147-178, 1981] for neurons in the cochlear nuclei (CN) of guinea pig were estimated. Sixteen periodic segments of bandlimited, synthesized noise evoked replicable, distinctive period histograms for spike discharges. All driven units in the major divisions of the CN having their characteristic frequency (CF) within the noise bandlimits had unique STRFs for a given intensity of noise stimulation. The STRF maximum corresponded to the unit's CF, and details of the STRF patterns differed over CN divisions and response classes derived from tonebursts. The sizes of features in STRFs from this mammal appeared significantly smaller in their temporal and spectral extents than those reported in the torus semicircularis of an amphibian and were roughly comparable to the few units reported from cat ventral CN [Eggermont et al., Quart. Rev. Biophys. 16, 341-414, 1983]. STRFs, as they are presently obtained, provide useful insight into some aspects of afferent processing and perhaps connectivity, but their interpretation is specific to the level of stimulation and limited by the need to choose a specific energy distribution to represent the stimulus.

Effect of electrical pulse shape on AVCN unit responses to cochlear stimulation.

Electrical stimulation of the cochlea with a multiple-electrode array is best accomplished using pulsatile instead of continuous stimulation. The optimum shapes of electrical pulses for this purpose are still uncertain due to a lack of knowledge about their stimulation efficiency and requirements of the encoding strategy. We presented an extensive set of charge-balanced, rectangular pulse shapes to the guinea pig cochlea. Durations per phase for these constant-current pulses ranged from 20 microseconds to 900 microseconds with initially positive and initially negative polarities. Spike counts from single units in the anteroventral cochlear nucleus differed significantly for different pulse shapes, as did their initial latencies. Implications for stimulation efficiency and encoding strategies are discussed.

Radial current flow and source density in the basal scala tympani.

Ionic movement between the scala media and scala tympani is modulated by acoustic stimulation. It underlies electrical currents in the fluids of these compartments and produces voltage gradients from which partial current-flow densities can be estimated. Radial voltage gradients were sampled in the first turn of the scala tympani of the guinea pig cochlea at known distances from the basilar membrane. Large potential gradients indicated significant current-flow densities near the organ of Corti with less flow near the lateral wall of the cochlea and over the spiral lamina. Current-source densities were highest within 100 micron of the organ of Corti. Current-source density analysis suggested that source-sink pairs can be detected from field observations in the scala tympani.

Unit responses in ventral cochlear nucleus reflect cochlear coding of rapid frequency sweeps.

This study examines the encoding of rapid frequency sweeps in single units of the ventral cochlear nucleus (VCN). Sweeps were designed to explore the role of cochlear mechanics in shaping the temporal responses across cells in the VCN. The time course of frequency change for rapidly rising frequency sweeps theoretically produced simultaneous displacement maxima by cancelling travel time along the cochlear partition. Rising sweeps with longer time courses only partially canceled travel time, while falling sweeps had time courses of frequency change equal to or greater than travel time. Falling sweeps thus augmented normal travel time. Latency of unit firing to sweeps across unit characteristic frequency (CF) reflected cochlear delay-line mechanics. The latency-CF functions agreed with predictions from travel-time estimates for rising-frequency sweeps, but responses to falling sweeps were less predictable.

Unit responses at cochlear nucleus to electrical stimulation through a cochlear prosthesis.

Afferent auditory fibers of the guinea pig cochlea were electrically stimulated with current introduced through electrodes in the scala tympani. Thresholds were determined for unit responses recorded in the ventral cochlear nuclei to a sinusoid of 98 Hz from response-rate growth functions versus stimulus intensity. Suprathreshold response rates for most units grew rapidly from threshold to saturation at 2-15 dB above threshold. Peristimulus time histograms were collected for responses to single sinusoids and combinations of two and five sinusoids ranging from 86 to 134 Hz. Spike occurrences were highly synchronous with individual cycles of the pure sinusoids, but responses to the more complex waveforms occurred primarily to the more intense peaks. The amplitude envelope was thus a major contributor to responses to multiple sinusoids. Destruction of cochlear structures with neomycin increased unit thresholds and produced some changes in waveform encoding.

Tissue impedance and current flow in the implanted ear. Implications for the cochlear prosthesis.

Tissue impedance was measured in the cochleas of monkeys and guinea pigs implanted with electrode arrays. The impedances were measured within the scala tympani and between the scala tympani and the internal auditory meatus of the modiolus. The measurements revealed several impedance properties. 1) The impedances inside and outside of the scala tympani are resistive for frequencies between 8 Hz and 12.5 kHz. 2). The impedances measured between the scala tympani and the internal auditory meatus were larger in magnitude than the impedances measured in the scala tympani. 3) Impedance was not affected significantly by changing stimulus current flow from 0.45 to 45 microA rms. 4) Impedance magnitude increased rapidly by different factors inside and outside the scala tympani after sacrifice of the subject animals. Measurements of the tissue impedance made in conjunction with measurements of threshold of response to electrical stimulation revealed that the threshold of response to electrical stimuli was lowest when the stimulating currents were highest outside the scala tympani. We conclude that the excitable elements of the auditory nerve are being stimulated within the modiolus rather than within the scala tympani.

Neural mechanisms relevant to the design of an auditory prosthesis. Location and electrical characteristics.

A cochlear prosthesis designed to electrically stimulate eighth nerve fibers in deaf subjects was studied in acute guinea pig preparations. The prosthesis, which consisted of two pairs of platinum-iridium electrodes, was inserted into the scala tympani through the round window. The electrical impedances of different current paths and their effectiveness in evoking neural responses in the central auditory system are compared. Assuming lumped neural elements, the results indicate that the sites of neural excitation lie outside the scala tympani. Frequency-response characteristics of neural excitation are in agreement with resistive spread of current through tissue to the site of stimulation. Neural membrane characteristics similar to those previously studied in nonmammalian nerves seem to account for the response initiation.

Effectiveness of middle ear electrical stimulation for activating central auditory pathways.

Electrical stimulation of afferent auditory elements through electrodes placed in the middle ear was investigated in acute guinea pig preparations. Thresholds for auditory activation were current dependent for low frequencies (less than 1 kHz) and charge-dependent at higher frequencies. Threshold currents were 3-5 times those for intracochlear stimulation. Mechanisms of activation were examined with removal of cochlear fluids and injection of neomycin, Xylocaine, saline, and artificial perilymph with different calcium concentrations. Neurons of the spiral ganglion are indicated as mediators of this stimulation.

Estimates of essential neural elements for stimulation through a cochlear prosthesis.

Electrical stimulation of afferent auditory pathways through electrodes placed within and outside of the cochlea were used to study stimulation and design parameters relevant to a cochlear prosthesis. In the acute guinea pig preparation, the tract response evoked in brachium of the inferior colliculus by electrical stimulation to an ear provided estimates of the effectiveness of various electrode placements. Stimulation between an electrode in the cochlea and a site along the eighth nerve was characterized by the lowest thresholds. Stimulation between intracochlear electrodes was somewhat less effective, and stimulation between external electrodes at the nerve, cochlear nucleus, or distant point was least effective. Thresholds, expressed as current, rose at approximately 6 dB per octave for stimulus frequencies from 1 kHz to 16 kHz. Thresholds below 10 microA rms were seen for optimal placements. These observations suggest that the neural elements being stimulated are the cell bodies of the spiral ganglion cells.

Design of the cochlear prosthesis: effects of the flow of current in the implanted ear.

When structures within the temporal bone are stimulated electrically it is desirable to maximize the dynamic range of the stimulus. The maximum dynamic range of electrical stimulus seems to be found when the threshold of stimulation is minimum. The minimum threshold of stimulus is likely to be reached when the electrical current that flow through regions containing excitable cells is maximized. By implanting electrodes throughout the temporal bone, it is possible to apply electrical currents to the ear and to measure the distributions of current flowing within the ear. The results of these measurements demonstrate that when current flow is directed outside the scala tympani, lower thresholds can be obtained. Frequency dependence of the paths of current flow cannot be used to explain the frequency dependence of the frequency-threshold functions measured in animals.

Biophysical measurements in the implanted cochlea.

Electrical stimulation via implanted electrode has been used to produce perceptions of sound in human subjects. This study describes preliminary work needed to understand the implanted ear and the distribution of current within it so that a stimulus system can be designed that is optimal for longevity, information transfer, and safety.