Input compensation of dolphin and sea lion auditory brainstem responses using frequency-modulated up-chirps.

Frequency-modulated "chirp" stimuli that offset cochlear dispersion (i.e., input compensation) have shown promise for increasing auditory brainstem response (ABR) amplitudes relative to traditional sound stimuli. To enhance ABR methods with marine mammal species known or suspected to have low ABR signal-to-noise ratios, the present study examined the effects of broadband chirp sweep rate and level on ABR amplitude in bottlenose dolphins and California sea lions. "Optimal" chirps were designed based on previous estimates of cochlear traveling wave speeds (using high-pass subtractive masking methods) in these species. Optimal chirps increased ABR peak amplitudes by compensating for cochlear dispersion; however, chirps with similar (or higher) frequency-modulation rates produced comparable results. The optimal chirps generally increased ABR amplitudes relative to noisebursts as threshold was approached, although this was more obvious when sound pressure level was used to equate stimulus levels (as opposed to total energy). Chirps provided progressively less ABR amplitude gain (relative to noisebursts) as stimulus level increased and produced smaller ABRs at the highest levels tested in dolphins. Although it was previously hypothesized that chirps would provide larger gains in sea lions than dolphins-due to the lower traveling wave speed in the former-no such pattern was observed.

Output compensation of auditory brainstem responses in dolphins and sea lions.

Cochlear dispersion causes increasing delays between neural responses from high-frequency regions in the cochlear base and lower-frequency regions toward the apex. For broadband stimuli, this can lead to neural responses that are out-of-phase, decreasing the amplitude of farfield neural response measurements. In the present study, cochlear traveling-wave speed and effects of dispersion on farfield auditory brainstem responses (ABRs) were investigated by first deriving narrowband ABRs in bottlenose dolphins and California sea lions using the high-pass subtractive masking technique. Derived-band ABRs were then temporally aligned and summed to obtain the "stacked ABR" as a means of compensating for the effects of cochlear dispersion. For derived-band responses between 8 and 32 kHz, cochlear traveling-wave speeds were similar for sea lions and dolphins [∼2-8 octaves (oct)/ms for dolphins; ∼3.5-11 oct/ms for sea lions]; above 32 kHz, traveling-wave speed for dolphins increased up to ∼30 oct/ms. Stacked ABRs were larger than unmasked, broadband ABRs in both species. The amplitude enhancement was smaller in dolphins than in sea lions, and enhancement in both species appears to be less than reported in humans. Results suggest that compensating for cochlear dispersion will provide greater benefit for ABR measurements in species with better low-frequency hearing.

The offset auditory brainstem response in bottlenose dolphins (Tursiops truncatus): Evidence for multiple underlying processes.

The auditory brainstem response (ABR) to stimulus onset has been extensively used to investigate dolphin hearing. The mechanisms underlying this onset response have been thoroughly studied in mammals. In contrast, the ABR evoked by sound offset has received relatively little attention. To build upon previous observations of the dolphin offset ABR, a series of experiments was conducted to (1) determine the cochlear places responsible for response generation and (2) examine differences in response morphologies when using toneburst versus noiseburst stimuli. Measurements were conducted with seven bottlenose dolphins (Tursiops truncatus) using tonebursts and spectrally "pink" broadband noisebursts, with highpass noise used to limit the cochlear regions involved in response generation. Results for normal-hearing and hearing-impaired dolphins suggest that the offset ABR contains contributions from at least two distinct responses. One type of response (across place) might arise from the activation of neural units that are shifted basally relative to stimulus frequency and shares commonalities with the onset ABR. A second type of response (within place) appears to represent a "true" offset response from afferent centers further up the ascending auditory pathway from the auditory nerve, and likely results from synchronous activity beginning at or above the cochlear nucleus.

Role of the temporal window in dolphin auditory brainstem response onset.

Auditory brainstem responses (ABRs) to linear-enveloped, broadband noisebursts were measured in six bottlenose dolphins to examine relationships between sound onset envelope properties and the ABR peak amplitude. Two stimulus manipulations were utilized: (1) stimulus onset envelope pressure rate-of-change was held constant while plateau pressure and risetime were varied and (2) plateau duration was varied while plateau pressure and risetime were held constant. When the stimulus onset envelope pressure rate-of-change was held constant, ABR amplitudes increased with risetime and were fit well with an exponential growth model. The model best-fit time constants for ABR peaks P1 and N5 were 55 and 64 µs, respectively, meaning ABRs reached 99% of their maximal amplitudes for risetimes of 275-320 µs. When plateau pressure and risetime were constant, ABR amplitudes increased linearly with stimulus sound exposure level up to durations of ∼250 µs. The results highlight the relationship between ABR amplitude and the integral of some quantity related to the stimulus pressure envelope over the first ∼250 µs following stimulus onset-a time interval consistent with prior estimates of the dolphin auditory temporal window, also known as the "critical interval" in hearing.

Auditory brainstem responses during aerial testing with bottlenose dolphins (Tursiops truncatus): Effects of electrode and jawphone locations.

Transmission of sound to dolphins during electrophysiological hearing screening is conducted out of water in certain cases (e.g., strandings). This necessitates that sound be delivered using a contact transducer either pressed against the skin or affixed to the jaw using a suction cup (i.e., "jawphones"). This study examined how bottlenose dolphin (Tursiops truncatus, n = 3) auditory brainstem responses (ABRs) varied with electrode and jawphone location during aerial testing. Stimuli were tone bursts with center frequencies of 28 to 160 kHz. Regression-based thresholds were lowest with the jawphone on the posterior and middle parts of the mandible. Thresholds based on later ABR peaks-recorded using an electrode immediately behind the blowhole-suggested more similarity between the thresholds for the anterior tip of the rostrum and the posterior/middle mandible than those based on earlier monaural waves recorded near the meatus. This was likely a result of a summation of responses from both ears as opposed to a more efficient acoustic pathway to the ear. These patterns were independent of frequency. These findings provide guidance for jawphone and electrode locations when examining dolphin hearing and when interpreting relative acoustic sensitivity of the head in similar testing situations.

A novel intracochlear injection method for rapid drug delivery to vestibular end organs.

BACKGROUND: Injection into the inner ear through the round window (RW) or a cochleostomy is a reliable method for delivering drugs or viruses to the cochlea. This method has been less effective for fast deliveries to vestibular end organs. NEW METHOD: We describe a novel approach for rapid delivery of drugs to the vestibular end organ via the oval window (OW) and scala vestibuli in 1-3 month old C57BL/6 mice. The OW was directly accessed through the external ear canal after ablating the tympanic membrane and middle ear ossicles. A canalostomy in the superior canal provided a low pressure point for faster transit of injected solution from the OW to the vestibular neuroepithelia, allowing for higher rates of injection. RESULTS: The efficacy of this technique was shown by fast transit times of a colored artificial perilymph from the OW to the utricle and the ampullae of the horizontal and superior canals in ∼2 min. Following injection, the response of the vestibular nerve was preserved, as measured by the vestibular sensory evoked potentials (VsEP). COMPARISON WITH EXISTING METHODS: Previous studies have used posterior semicircular canals or the RW with canalostomy to gain access to vestibular end organs in mice. The OW with canalostomy, provides the means for high injection rates and fast and reliable delivery of drugs to vestibular hair cells and afferent terminals. CONCLUSIONS: The presented method for injections through the OW provides rapid delivery of solutions to vestibular end organs without adversely affecting vestibular nerve responses measured by VsEP.

Using Unidirectional Rotations to Improve Vestibular System Asymmetry in Patients with Vestibular Dysfunction.

The vestibular system provides information about head movement and mediates reflexes that contribute to balance control and gaze stabilization during daily activities. Vestibular sensors are located in the inner ear on both sides of the head and project to the vestibular nuclei in the brainstem. Vestibular dysfunction is often due to an asymmetry between input from the two sides. This results in asymmetrical neural inputs from the two ears, which can produce an illusion of rotation, manifested as vertigo. The vestibular system has an impressive capacity for compensation, which serves to rebalance how asymmetrical information from the sensory end organs on both sides is processed at the central level. To promote compensation, various rehabilitation programs are used in the clinic; however, they primarily use exercises that improve multisensory integration. Recently, visual-vestibular training has also been used to improve the vestibulo-ocular reflex (VOR) in animals with compensated unilateral lesions. Here, a new method is introduced for rebalancing the vestibular activity on both sides in human subjects. This method consists of five unidirectional rotations in the dark (peak velocity of 320°/s) toward the weaker side. The efficacy of this method was shown in a sequential, double-blinded clinical trial in 16 patients with VOR asymmetry (measured by the directional preponderance in response to sinusoidal rotations). In most cases, VOR asymmetry decreased after a single session, reached normal values within the first two sessions in one week, and the effects lasted up to 6 weeks. The rebalancing effect is due to both an increase in VOR response from the weaker side and a decrease in response from the stronger side. The findings suggest that unidirectional rotation can be used as a supervised rehabilitation method to reduce VOR asymmetry in patients with longstanding vestibular dysfunction.

Effects of stimulus cosine onset properties on bottlenose dolphin (Tursiops truncatus) auditory brainstem responses.

Although the auditory brainstem response (ABR) is known to be an onset response, the specific relationship between stimulus onset properties and the resulting ABR is not well understood. In this study, the effects of stimulus onset on dolphin ABR were examined by measuring ABRs in six bottlenose dolphins while systematically manipulating rise time and plateau sound pressure of cosine-enveloped noise bursts. Noise bursts were spectrally "pink" with frequency content from 10 to 160 kHz, rise times from 32 µs to 4 ms, and plateau sound pressure levels from 102 to 138 dB re 1 µPa. Envelope rise time and plateau sound pressure alone were found to be poor predictors for ABR peak amplitudes and latencies. Peak amplitudes were well described by the envelope sound pressure at the end of a 260-µs window; however, best-fits to the data across ABR peaks were obtained when the window start time was allowed to vary. Peak latencies were best described by the maximum value of the second derivative of the pressure envelope. These results are consistent with single-unit and nearfield response data for terrestrial mammals and indicate that stimuli with rise times greater than 260 µs are non-optimal with respect to maximizing ABR amplitudes.

Signal-to-noise ratio of auditory brainstem responses (ABRs) across click rate in the bottlenose dolphin (Tursiops truncatus).

Although the maximum length sequence (MLS) and iterative randomized stimulation and averaging (I-RSA) methods allow auditory brainstem response (ABR) measurements at high rates, it is not clear if high rates allow ABRs of a given quality to be measured in less time than conventional (CONV) averaging (i.e., fixed interstimulus intervals) at lower rates. In the present study, ABR signal-to-noise ratio (SNR) was examined in six bottlenose dolphins as a function of measurement time and click rate using CONV averaging at rates of 25 and 100 Hz and the MLS/I-RSA approaches at rates from 100 to 1250 Hz. Residual noise in the averaged ABR was estimated using (1) waveform amplitude following the ABR, (2) waveform amplitude after subtracting two subaverage ABRs (i.e., the "±average"), and (3) amplitude variance at a single time point. Results showed that high stimulus rates can be used to obtain dolphin ABRs with a desired SNR in less time than CONV averaging. Optimal SNRs occurred at rates of 500-750 Hz, but were only a few dB higher than that for CONV averaging at 100 Hz. Nonetheless, a 1-dB improvement in SNR could result in a 25% time savings in reaching criterion SNR.

Learning Effects and the Sensory Organization Test: Influence of a Unilateral Peripheral Vestibular Impairment.

PURPOSE: Healthy young controls exhibit a learning effect after undergoing repeated administrations of the sensory organization test (SOT). The primary objective of the present experiment was to determine if an SOT learning effect is present in individuals with a unilateral vestibular impairment (UVI), and if so, whether it is different from healthy controls. The secondary objective was to determine if the learning effect is dependent on the time frame of repeated SOT assessments. METHOD: Eleven individuals diagnosed with a UVI and 11 controls underwent 6 repetitions of the SOT over 2 visits (3 per visit all within 1 week). A second control group underwent 3 SOT repetitions, with each repetition separated by 1 week, to evaluate the time course of the SOT learning effect. RESULTS: No statistically significant differences were found between the UVI group and the control group. In addition, the magnitude of the learning effect was found to be similar regardless of the length of time that separated the repetitions. CONCLUSIONS: If the SOT is to be used as a measure of improvement, the learning effect should be exhausted (which typically occurs following the third administration) prior to the introduction of therapy. Future research should further investigate the results from those with other vestibular pathologies.

Effects of noise burst rise time and level on bottlenose dolphin (Tursiops truncatus) auditory brainstem responses.

Although the auditory brainstem response (ABR) is known to be an onset response, specific features of acoustic stimuli that affect the morphology of the ABR are not well understood. In this study, the effects of stimulus onset properties were investigated by measuring ABRs in seven bottlenose dolphins while systematically manipulating stimulus rise time and the amplitude of the sound pressure temporal envelope plateau. Stimuli consisted of spectrally pink (i.e., equal mean-square pressure in proportional frequency bands) noise bursts with linear rise (and fall) envelopes and frequency content from 10 to 160 kHz. Noise burst rise times varied from 32 µs to 4 ms and plateau sound pressure levels varied from 96 to 150 dB re 1 µPa. ABR peak latency was found to be a function of the rate of change of the sound pressure envelope, while ABR peak amplitude was a function of the envelope sound pressure at the end of a fixed integration window. The data support previous single-unit and nearfield response data from terrestrial mammals and a model where the rate of change of envelope sound pressure is integrated across a time window aligned with stimulus onset.

Vestibular evoked myogenic potential testing: Payment policy review for clinicians and payers.

PURPOSE OF REVIEW: A recent American Academy of Neurology Evidence-Based Practice Guideline on vestibular myogenic evoked potential (VEMP) testing has described superior canal dehiscence syndrome (SCDS) and evaluated the merits of VEMP in its diagnosis. SCDS is an uncommon but now well-recognized cause of dizziness and auditory symptoms. This article familiarizes health care providers with this syndrome and the utility and shortcomings of VEMP as a diagnostic test and also explores payment policies for VEMP. RECENT FINDINGS: In carefully selected patients with documented history compatible with the SCDS, both high-resolution temporal bone CT scan and VEMP are valuable aids for diagnosis. Payers might be unfamiliar with both this syndrome and VEMP testing. SUMMARY: It is important to raise awareness of VEMP and its possible indications and the rationale for coverage of VEMP testing. Payers may not be readily receptive to VEMP coverage if this test is used in an undifferentiated manner for all common vestibular and auditory symptoms.

Click reception in the harbor porpoise (Phocoena phocoena): Effects of electrode and contact transducer location on the auditory brainstem response.

Unlike terrestrial mammals that have unambiguous aerial sound transmission pathways via the outer ear and tympanum, sound reception pathways in most odontocetes are not well understood. Recent studies have used auditory brainstem response (ABR) measurements to examine sound reception pathways. This study sought to determine how sound source placements, recording electrode arrangements, and ABR peak analyses affect interpretations of sound reception in the harbor porpoise (Phocoena phocoena). Click stimuli were delivered in air from a contact transducer ("jawphone"). Early ABR peaks (representing auditory nerve responses), and later peaks reflecting higher brainstem activity, were analyzed across jawphone and recording electrode positions. Auditory nerve responses were similar for jawphone placements from the ipsilateral posterior mandible to the tip of the rostrum. Later peaks, however, suggested a possible region of highest sensitivity midway between the posterior mandible and the rostrum tip. These findings are generally similar to previous data for porpoises. In contrast to auditory nerve responses that were largest when recorded near the ipsilateral meatus, later ABR peaks were largest when recorded with a contralateral (opposing) electrode. These results provide information on the processes underlying peaks of the ABR, and inform stimulus delivery and ABR recording parameters in odontocete sound reception studies.

Glutamate is down-regulated and tinnitus loudness-levels decreased following rTMS over auditory cortex of the left hemisphere: A prospective randomized single-blinded sham-controlled cross-over study.

Using a prospective randomized single-blinded sham-controlled cross-over design, we studied the efficacy of low frequency (1-Hz) repetitive transcranial magnetic stimulation (rTMS) over auditory cortex of the left temporal lobe as an experimental treatment modality for noise-induced tinnitus. Pre/post outcome measures for sham vs. active rTMS conditions included differential changes in tinnitus loudness, self-perceived changes in the Tinnitus Handicap Questionnaire (THQ), and neurochemical changes of brain metabolite concentrations using single voxel proton magnetic resonance spectroscopy (1H-MRS) obtained from left and right auditory cortical areas. While no subject in our sample had complete abatement of their tinnitus percept, active but not sham rTMS significantly reduced the loudness level of the tinnitus perception on the order of 4.5 dB; improved subscales in several content areas on the THQ, and down regulated (reduced) glutamate concentrations specific to the auditory cortex of the left temporal lobe that was stimulated. In addition, significant pair-wise correlations were observed among questionnaire variables, metabolite variables, questionnaire-metabolite variables, and metabolite-loudness variables. As part of this correlation analysis, we demonstrate for the first time that active rTMS produced a down regulation in the excitatory neurotransmitter glutamate that was highly correlated (r = 0.77, p < 0.05) with a reduction in tinnitus loudness levels measured psychoacoustically with a magnitude estimation procedure. Overall, this study provides unique information on neurochemical, psychoacoustic, and questionnaire-related profiles which emphasizes the emerging fields of perceptual and cognitive MRS and provides a perspective on a new frontier in auditory and tinnitus-related research.

Bottlenose dolphin (Tursiops truncatus) auditory brainstem responses to frequency-modulated "chirp" stimuli.

Previous studies have demonstrated that increasing-frequency chirp stimuli (up-chirps) can enhance human auditory brainstem response (ABR) amplitudes by compensating for temporal dispersion occurring along the cochlear partition. In this study, ABRs were measured in two bottlenose dolphins (Tursiops truncatus) in response to spectrally white clicks, up-chirps, and decreasing-frequency chirps (down-chirps). Chirp durations varied from 125 to 2000 µs. For all stimuli, frequency bandwidth was constant (10-180 kHz) and peak-equivalent sound pressure levels (peSPLs) were 115, 125, and 135 dB re 1 µPa. Up-chirps with durations less than ∼1000 µs generally increased ABR peak amplitudes compared to clicks with the same peSPL or energy flux spectral density level, while down-chirps with durations from above ∼250 to 500 µs decreased ABR amplitudes relative to clicks. The findings generally mirror those from human studies and suggest that the use of chirp stimuli may be an effective way to enhance broadband ABR amplitudes in larger marine mammals.

The effects of click rate on the auditory brainstem response of bottlenose dolphins.

Rate manipulations can be used to study adaptation processes in the auditory nerve and brainstem. For this reason, rate effects on the click-evoked auditory brainstem response (ABR) have been investigated in many mammals, including humans. In this study, click-evoked ABRs were obtained in eight bottlenose dolphins (Tursiops truncatus) while varying stimulus rate using both conventional averaging and maximum length sequences (MLSs), which allow disentangling ABRs that overlap in time and thus permit the study of adaptation at high rates. Dolphins varied in age and upper cutoff frequency of hearing. Conventional stimulation rates were 25, 50, and 100 Hz and average MLS rates were approximately 50, 100, 250, 500, 1000, 2500, and 5000 Hz. Click peak-equivalent sound pressure levels for all conditions were 135 dB re 1 µPa. ABRs were observed in all dolphins, at all stimulus rates. With increasing rate, peak latencies increased and peak amplitudes decreased. There was a trend for an increase in the interwave intervals with increasing rate, which appeared more robust for the dolphins with a full range of hearing. For those rates where ABRs were obtained for both conventional and MLS approaches, the latencies of the mean data were in good agreement.

Place specificity of the click-evoked auditory brainstem response in the bottlenose dolphin (Tursiops truncatus).

Cochlear place specificity of the auditory brainstem response (ABR) was investigated in five bottlenose dolphins by measuring ABRs to broadband clicks presented simultaneously with masking noise having various high-pass cutoff frequencies. Click and noise stimuli were digitally compensated to account for the transmitting response of the piezoelectric transducers and any multipath propagation effects to achieve "white" or "pink" spectral characteristics. Narrowband evoked responses were derived by sequentially subtracting responses obtained with noise at lower high-pass cutoff frequencies from those obtained with noise having higher cutoff frequencies. The results revealed little contribution to the click-evoked brainstem response from frequency bands below 10 kHz and, in dolphins with full hearing bandwidth, the largest amplitude derived band evoked responses were obtained from the highest frequency bands. Narrowband latencies decreased with increasing frequency and were adequately fit with a power function exhibiting relatively large change in latency with frequency below ∼30 kHz and little change above ∼30 kHz. These data demonstrate that frequency bands below ∼10 kHz do not substantively contribute to the farfield ABR in the bottlenose dolphin when using place-specific approaches such as high-pass subtractive-masking techniques.

The effects of click and masker spectrum on the auditory brainstem response of bottlenose dolphins (Tursiops truncatus).

Two experiments were performed that investigated the effects of (1) click level and (2) continuous broadband noise on the binaural auditory brainstem response (ABR) of normal-hearing and hearing-impaired bottlenose dolphins (Tursiops truncatus). In addition to spectrally uncompensated clicks and noise, stimuli were digitally compensated to achieve "white" spectra (flat spectral density level) or "pink" spectra (spectral density level rolling off at -3 dB/octave). For experiment 1, in all spectral conditions, ABR peak latencies increased and peak amplitudes decreased with decreasing click level, but interwave intervals changed little. Latency-intensity function (LIF) slopes ranged from -3 to -11 µs/dB. The LIF slopes of ABR peaks evoked by uncompensated clicks were steeper in dolphins with hearing loss. Click level was held constant during experiment 2, and the effect of bilaterally delivered broadband masking noise on the ABR was investigated. Clicks and noise were filtered to create a pink click/noise condition and a white click/noise condition. With increasing levels of masking noise, peak latencies increased (although only P1-P4 white reached significance), peak amplitudes decreased, and interpeak intervals increased (although not significantly). These effects are compared to results reported for terrestrial mammals, and implications for auditory health assessment and biosonar function are discussed.

The influence of caffeine on the sensory organization test.

BACKGROUND: Clinicians often request that patients refrain from consuming caffeinated beverages 24 h before vestibular function testing. However, there is limited research regarding how caffeine may affect the results of these tests. The sensory organization test (SOT) evaluates how well an individual is able to maintain his or her balance during several different conditions that manipulate vestibular, visual, or somatosensory information. PURPOSE: This study evaluated whether caffeine consumption affects the results of the SOT in a group of healthy young adults. RESEARCH DESIGN: Individuals were evaluated under two conditions: (1) after consuming ∼300 mg of caffeine before testing, and (2) without consuming a caffeinated beverage for 24 h before testing. Regular caffeine intake and caffeine withdrawal symptoms were assessed in these individuals. Participants were stratified into a no/low or a moderate/high caffeine intake group through the use of a self-reported 1-week caffeine diary. STUDY SAMPLE: Thirty healthy control participants (mean age = 23.28 yr; males = 9) without any history of vestibular or balance impairment participated in the present study. DATA COLLECTION/ANALYSIS: The NeuroCom SMART Equitest was used to administer the SOT, whereas paired t-tests, completed with IBM SPSS Statistics 20, were used to analyze the data for statistical significance. RESULTS: Analysis of the data revealed a statistically significant difference between the caffeine and no-caffeine sessions during (1) condition 5 (C5): eyes closed, platform sway-referenced; and (2) the total composite score. Statistically significant differences were also noted for the vestibular and somatosensory preference ratios. In general, the participants performed better (i.e., higher equilibrium/composite scores) during the caffeine session. When significant results were found, the participants were stratified by weekly caffeine intake into a no/low caffeine (LC) intake group versus a moderate/high caffeine (HC) intake group. After this stratification, a statistically significant difference remained for C5, the composite score, and the somatosensory/vestibular preference ratios for the LC intake group, whereas no statistically significant results were found in the HC intake group. In addition, further analysis revealed less of a change in the equilibrium score as the amount of weekly caffeine intake increased. Despite these significant results, the mean differences were small in magnitude, and C5, the composite score, as well as the sensory analysis ratios, fell within normal limits for all participants during both sessions. CONCLUSIONS: The ingestion of caffeine did not produce a clinically significant effect in healthy young control participants. Future research is needed to determine if these same results occur in older adults, or in individuals with a history of vestibular impairment.