Ben H. Bonham

Current focusing and steering: Modeling, physiology, and psychophysics

Current steering and current focusing are stimulation techniques designed to increase the number of distinct perceptual channels available to cochlear implant (CI) users by adjusting currents applied simultaneously to multiple CI electrodes. Previous studies exploring current steering and current focusing stimulation strategies are reviewed, including results of research using computational models, animal neurophysiology, and human psychophysics. Preliminary results of additional neurophysiological and human psychophysical studies are presented that demonstrate the success of current steering strategies in stimulating auditory nerve regions lying between physical CI electrodes, as well as current focusing strategies that excite regions narrower than those stimulated using monopolar configurations. These results are interpreted in the context of perception and speech reception by CI users. Disparities between results of physiological and psychophysical studies are discussed. The differences in stimulation used for physiological and psychophysical studies are hypothesized to contribute to these disparities. Finally, application of current steering and focusing strategies to other types of auditory prostheses is also discussed.

Considerations for Design of Future Cochlear Implant Electrode Arrays: Electrode Array Stiffness, Size, and Depth of Insertion

The level of hearing rehabilitation enjoyed by cochlear implant (CI) recipients has increased dramatically since the introduction of these devices. This improvement is the result of continual development of these systems and the inclusion of subjects with less severe auditory pathology. Developments include advanced signal processing, higher stimulation rates, greater numbers of channels, and more efficient electrode arrays that are less likely to produce insertion damage. New directions in the application of CIs, particularly in combined acoustic and electrical stimulation, and increasing performance expectations will place greater demands on future electrode arrays. Specifically, the next generation of arrays must be reliably inserted without damage, must maintain residual acoustic function, and may need to be inserted more deeply. In this study, we measured the mechanical properties of eight clinical and prototype human CI electrode arrays and evaluated insertion trauma and insertion depth in 79 implanted cadaver temporal bones. We found that the size and shape of the array directly affect the incidence of observed trauma. Further, arrays with greater stiffness in the plane perpendicular to the plane of the cochlear spiral are less likely to cause severe trauma than arrays with similar vertical and horizontal stiffness.

Functional Organization and Hemispheric Comparison of Primary Auditory Cortex in the Common Marmoset (Callithrix jacchus)

Hemispheric fine‐grain maps of primary auditory cortex (AI) were derived from microelectrode penetrations in the temporal gyrus of the common marmoset (Callithrix jacchus) to 1) compare the functional organization of AI in the marmoset with other mammalian species and 2) compare the right and left AI maps in individual monkeys. Frequency receptive fields (FRFs) were recorded with pure tones. Five FRF parameters were analyzed: characteristic frequency, threshold, sharpness of tuning 10 dB and 40 dB above threshold, and minimum response latency. The present study confirms that the functional organization of AI is characterized by a robust tonotopic frequency gradient overlaid with spatially clustered distributions of other FRF parameters. Globally, this functional organization of AI in the common marmoset is similar to that in other mammalian species. With respect to within‐subject hemispheric comparisons of the five FRF parameters, a coherent pattern of asymmetry is not evident in marmoset AI. The overall results indicate that the basic functional organization between hemispheres is similar but not identical. J. Comp. Neurol. 487:391–406, 2005.

Localization by interaural time difference (ITD): Effects of interaural frequency mismatch

A commonly accepted physiological model for lateralization of low-frequency sounds by interaural time delay (ITD) stipulates that binaural comparison neurons receive input from frequency-matched channels from each ear. Here, the effects of hypothetical interaural frequency mismatches on this model are reported. For this study, the cats auditory system peripheral to the binaural comparison neurons was represented by a neurophysiologically derived model, and binaural comparison neurons were represented by cross-correlators. The results of the study indicate that, for binaural comparison neurons receiving input from one cochlear channel from each ear, interaural CF mismatches may serve to either augment or diminish the effective difference in ipsilateral and contralateral axonal time delays from the periphery to the binaural comparison neuron. The magnitude of this increase or decrease in the effective time delay difference can be up to 400 microseconds for CF mismatches of 0.2 octaves or less for binaural neurons with CFs between 250 Hz and 2.5 kHz. For binaural comparison neurons with nominal CFs near 500 Hz, the 25-microsecond effective time delay difference caused by a 0.012-octave CF mismatch is equal to the ITD previously shown to be behaviorally sufficient for the cat to lateralize a low-frequency sound source.

Design and Fabrication of Multichannel Cochlear Implants for Animal Research

The effectiveness of multichannel cochlear implants depends on the activation of perceptually distinct regions of the auditory nerve. Increased information transfer is possible as the number of channels and dynamic range are increased and electrical and neural interaction among channels is reduced. Human and animal studies have demonstrated that specific design features of the intracochlear electrode directly affect these performance factors. These features include the geometry, size, and orientation of the stimulating sites, proximity of the device to spiral ganglion neurons, shape and position of the insulating carrier, and the stimulation mode (monopolar, bipolar, etc.). Animal studies to directly measure the effects of changes in electrode design are currently constrained by the lack of available electrodes that model contemporary clinical devices. This report presents methods to design and fabricate species-specific customizable electrode arrays. We have successfully implanted these arrays in guinea pigs and cats for periods of up to 14 months and have conducted acute electrophysiological experiments in these animals. Modifications enabling long-term intracochlear drug infusion are also described. Studies using these scale model arrays will improve our understanding of how these devices function in human subjects and how we can best optimize future cochlear implants.

Realignment of Interaural Cortical Maps in Asymmetric Hearing Loss

Misalignment of interaural cortical response maps in asymmetric hearing loss evolves from initial gross divergence to near convergence over a 6 month recovery period. The evolution of left primary auditory cortex (AI) interaural frequency map changes is chronicled in squirrel monkeys with asymmetric hearing loss induced by overstimulating the right ear with a 1 kHz tone at 136 dB for 3 h. AI frequency response areas (FRAs), derived from tone bursts presented to the poorer or better hearing ears, are compared at 6, 12, and 24 weeks after acoustic overstimulation. Characteristic frequency (CF) and minimum threshold parameters are extracted from FRAs, and they are used to quantify interaural response map differences. A large interaural CF map misalignment of ΔCF ∼1.27 octaves at 6 weeks after overstimulation decreases substantially to ΔCF ∼0.62 octave at 24 weeks. Interaural cortical threshold map misalignment faithfully reflects peripheral asymmetric hearing loss at 6 and 12 weeks. However, AI threshold map misalignment essentially disappears at 24 weeks, primarily because ipsilateral cortical thresholds have become unexpectedly elevated relative to peripheral thresholds. The findings document that plastic change in central processing of sound stimuli arriving from the nominally better hearing ear may account for progressive realignment of both interaural frequency and threshold maps.

Acute changes in frequency responses of inferior colliculus central nucleus (ICC) neurons following progressively enlarged restricted spiral ganglion lesions.

Immediate effects of sequential and progressively enlarged spiral ganglion (SG) lesions were recorded from cochleas and inferior colliculi. Small SG-lesions produced modest elevations in cochlear tone-evoked compound action potential (CAP) thresholds across narrow frequency ranges; progressively enlarged lesions produced progressively higher CAP-threshold elevations across progressively wider frequency ranges. No comparable changes in distortion product otoacoustic emissions (DPOAEs) amplitudes were observed consistent with silencing of auditory nerve sectors without affecting organ of Corti function. Frequency response areas (FRAs) of inferior colliculus (IC) neurons were recorded before and immediately after SG-lesions using multi-site silicon arrays fixed in place with recording sites arrayed along IC frequency gradient. Individual post-lesion FRAs exhibited progressively elevated response thresholds and diminished response amplitudes at lesion frequencies, whereas responses at non-lesion frequencies were either unchanged or enhanced. Characteristic frequencies were shifted and silent areas were introduced within these FRAs. Sequentially larger lesions produced sequentially larger shifts in CF and/or enlarged silent areas within affected FRAs, producing immediate changes in IC frequency organization. These results contrast with those from the auditory nerve, extend previous reports of experience-induced plasticity in the auditory CNS, and support results indicating afferent convergence onto ICC neurons across broad frequency bands.

Perinatal asphyxia affects rat auditory processing: implications for auditory perceptual impairments in neurodevelopmental disorders.

Perinatal asphyxia, a naturally and commonly occurring risk factor in birthing, represents one of the major causes of neonatal encephalopathy with long term consequences for infants. Here, degraded spectral and temporal responses to sounds were recorded from neurons in the primary auditory cortex (A1) of adult rats exposed to asphyxia at birth. Response onset latencies and durations were increased. Response amplitudes were reduced. Tuning curves were broader. Degraded successive-stimulus masking inhibitory mechanisms were associated with a reduced capability of neurons to follow higher-rate repetitive stimuli. The architecture of peripheral inner ear sensory epithelium was preserved, suggesting that recorded abnormalities can be of central origin. Some implications of these findings for the genesis of language perception deficits or for impaired language expression recorded in developmental disorders, such as autism spectrum disorders, contributed to by perinatal asphyxia, are discussed.

Fast stimulus artifact recovery in a multichannel neural recording system

We describe a 32-channel recording system and software artifact blanking technique for recording neuronal responses to high-rate electrical stimulation. Each recording channel recovers from biphasic full-scale-input pulses (1.5 V) in less than 80 mus. Artifacts are blanked online in software, allowing flexibility in the choice of blanking period and the possibility of recovering neural data occurring simultaneously with non-saturating artifacts. The system has been used in-vivo to record central neuronal responses to intracochlear electrical stimulation at 2000 pulses per second. Simplicity of the hardware design makes the technique well suited to an implantable multi-channel recording system.

Representation of frequency modulation in the primary auditory cortex of New World monkeys

Vocalizations are the primary means of communication among non-human primates. Indeed, among New World monkeys, such as the squirrel monkey and owl monkey, vocalizations may take many forms, such as cackles, growls, trills, twitters, etc. (Winter et al. 1966; Jurgens 1986; Wang et al. 1995; Jurgens 1998). Thus each species has many stereotyped communication calls in its vocal repertoire, each communicating some unique information to other members of its social environment. In this study we quantitatively described the responses of the primary auditory cortex (AI) of the anesthetized squirrel monkey and awake owl monkey to tone bursts, random tone pips, and frequency modulated sinusoids (FM sweeps) - sounds whose frequency content is stationary or whose frequency content changes smoothly over time from one frequency to another, respectively. FM sweeps serve as simplifications of the frequency transitions that are present in many natural monkey calls. Discerning how these sweeps are represented across the auditory cortex allows us to see if there is a systematic and orderly representation of this parameter in AI. This study is unique in that it employs highly dense mapping of neurons throughout the extent of AI in the squirrel monkey and single unit recording in the awake owl monkey. While we previously showed that there is a precise and systematic map of CF and bandwidth across AI of the squirrel monkey (Cheung et al. 2001) the picture for FM sweep processing is less clear. We discuss the spatial organization of FM sweep responses as well as the population responses for both species.