Temporal Pitch Sensitivity in an Animal Model: Psychophysics and Scalp Recordings : Temporal Pitch Sensitivity in Cat.

Cochlear implant (CI) users show limited sensitivity to the temporal pitch conveyed by electric stimulation, contributing to impaired perception of music and of speech in noise. Neurophysiological studies in cats suggest that this limitation is due, in part, to poor transmission of the temporal fine structure (TFS) by the brainstem pathways that are activated by electrical cochlear stimulation. It remains unknown, however, how that neural limit might influence perception in the same animal model. For that reason, we developed non-invasive psychophysical and electrophysiological measures of temporal (i.e., non-spectral) pitch processing in the cat. Normal-hearing (NH) cats were presented with acoustic pulse trains consisting of band-limited harmonic complexes that simulated CI stimulation of the basal cochlea while removing cochlear place-of-excitation cues. In the psychophysical procedure, trained cats detected changes from a base pulse rate to a higher pulse rate. In the scalp-recording procedure, the cortical-evoked acoustic change complex (ACC) and brainstem-generated frequency following response (FFR) were recorded simultaneously in sedated cats for pulse trains that alternated between the base and higher rates. The range of perceptual sensitivity to temporal pitch broadly resembled that of humans but was shifted to somewhat higher rates. The ACC largely paralleled these perceptual patterns, validating its use as an objective measure of temporal pitch sensitivity. The phase-locked FFR, in contrast, showed strong brainstem encoding for all tested pulse rates. These measures demonstrate the cat's perceptual sensitivity to pitch in the absence of cochlear-place cues and may be valuable for evaluating neural mechanisms of temporal pitch perception in the feline animal model of stimulation by a CI or novel auditory prostheses.

Development and validation of a method to record electrophysiological responses in direct acoustic cochlear implant subjects.

Acoustic hearing implants, such as direct acoustic cochlear implants (DACIs), can be used to treat profound mixed hearing loss. Electrophysiological responses in DACI subjects are of interest to confirm auditory processing intra-operatively, and to assist DACI fitting postoperatively. We present two related studies, focusing on DACI artifacts and electrophysiological measurements in DACI subjects, respectively. In the first study we aimed to characterize DACI artifacts, to study the feasibility of measuring frequency-specific electrophysiological responses in DACI subjects. Measurements of DACI artifacts were collected in a cadaveric head to disentangle possible DACI artifact sources and compared to a constructed DACI artifact template. It is shown that for moderate stimulation levels, DACI artifacts are mainly dominated by the artifact from the radio frequency (RF) communication signal, that can be modeled if the RF encoding protocol is known. In a second study, the feasibility of measuring intra-operative responses, without applying the RF artifact models, in DACI subjects is investigated. Auditory steady-state and brainstem responses were measured intra-operatively in three DACI subjects, immediately after implantation, to confirm proper DACI functioning and coupling to the inner ear. Intra-operative responses could be measured in two of the three tested subjects. Absence of intra-operative responses in the third subject can possibly be explained by the hearing loss, attenuation of intra-operative responses, the difference between electrophysiological and behavioral threshold, and a temporary threshold shift due to the DACI surgery. In conclusion, RF artifacts can be modeled, such that electrophysiological responses to frequency-specific stimuli could possibly be measured in DACI subjects, and intra-operative responses in DACI subjects can be obtained.

Independent component analysis for cochlear implant artifacts attenuation from electrically evoked auditory steady-state response measurements.

OBJECTIVE: Electrically evoked auditory steady-state responses (EASSRs) are potentially useful for objective cochlear implant (CI) fitting and follow-up of the auditory maturation in infants and children with a CI. EASSRs are recorded in the electro-encephalogram (EEG) in response to electrical stimulation with continuous pulse trains, and are distorted by significant CI artifacts related to this electrical stimulation. The aim of this study is to evaluate a CI artifacts attenuation method based on independent component analysis (ICA) for three EASSR datasets. APPROACH: ICA has often been used to remove CI artifacts from the EEG to record transient auditory responses, such as cortical evoked auditory potentials. Independent components (ICs) corresponding to CI artifacts are then often manually identified. In this study, an ICA based CI artifacts attenuation method was developed and evaluated for EASSR measurements with varying CI artifacts and EASSR characteristics. Artifactual ICs were automatically identified based on their spectrum. MAIN RESULTS: For 40 Hz amplitude modulation (AM) stimulation at comfort level, in high SNR recordings, ICA succeeded in removing CI artifacts from all recording channels, without distorting the EASSR. For lower SNR recordings, with 40 Hz AM stimulation at lower levels, or 90 Hz AM stimulation, ICA either distorted the EASSR or could not remove all CI artifacts in most subjects, except for two of the seven subjects tested with low level 40 Hz AM stimulation. Noise levels were reduced after ICA was applied, and up to 29 ICs were rejected, suggesting poor ICA separation quality. SIGNIFICANCE: We hypothesize that ICA is capable of separating CI artifacts and EASSR in case the contralateral hemisphere is EASSR dominated. For small EASSRs or large CI artifact amplitudes, ICA separation quality is insufficient to ensure complete CI artifacts attenuation without EASSR distortion.

Pile driving playback sounds and temporary threshold shift in harbor porpoises (Phocoena phocoena): Effect of exposure duration.

High intensity underwater sounds may cause temporary hearing threshold shifts (TTSs) in harbor porpoises, the magnitude of which may depend on the exposure duration. After exposure to playbacks of pile driving sounds, TTSs in two porpoises were quantified at 4 and 8 kHz with a psychophysical technique. At 8 kHz, the pile driving sounds caused the highest TTS. Pile driving sounds had the following: pulse duration 124 ms, rate 2760 strikes/h, inter-pulse interval 1.3 s, duty cycle ∼9.5%, average received single-strike unweighted broadband sound exposure level (SELss) 145 dB re 1 µPa(2)s, exposure duration range 15-360 min (cumulative SEL range: 173-187 dB re 1 µPa(2)s). Control sessions were also carried out. Mean TTS (1-4 min after sound exposure stopped in one porpoise, and 12-16 min in the other animal) increased from 0 dB after 15 min exposure to 5 dB after 360 min exposure. Recovery occurred within 60 min post-exposure. For the signal duration, sound pressure level (SPL), and duty cycle used, the TTS onset SELcum is estimated to be around 175 dB re 1 µPa(2)s. The small increase in TTS between 15 and 360 min exposures is due to the small amount of sound energy per unit of time to which the porpoises were exposed [average (over time) broadband SPL ∼144 dB re 1 µPa].

Hearing frequency thresholds of harbor porpoises (Phocoena phocoena) temporarily affected by played back offshore pile driving sounds.

Harbor porpoises may suffer hearing loss when exposed to intense sounds. After exposure to playbacks of broadband pile driving sounds for 60 min, the temporary hearing threshold shift (TTS) of a porpoise was quantified at 0.5, 1, 2, 4, 8, 16, 32, 63, and 125 kHz with a psychoacoustic technique. Details of the pile driving sounds were as follows: pulse duration 124 ms, rate 2760 strikes/h, inter-pulse interval 1.3 s, average received single strike unweighted sound exposure level (SEL) 146 dB re 1 µPa(2) s (cumulative SEL: 180 dB re 1 µPa(2) s). Statistically significant TTS only occurred at 4 and 8 kHz; mean TTS (1-4 min. after sound exposure stopped) was 2.3 dB at 4 kHz, and 3.6 dB at 8 kHz; recovery occurred within 48 min. This study shows that exposure to multiple impulsive sounds with most of their energy in the low frequencies can cause reduced hearing at higher frequencies in harbor porpoises. The porpoise's hearing threshold for the frequency in the range of its echolocation signals was not affected by the pile driving playback sounds.

Frequency of greatest temporary hearing threshold shift in harbor porpoises (Phocoena phocoena) depends on the noise level.

Harbor porpoises may suffer hearing loss when they are exposed to high level sounds. After exposure for 60 min to a 6.5 kHz continuous tone at average received sound pressure levels (SPLav.re.) ranging from 118 to 154 dB re 1µPa, the temporary hearing threshold shifts (TTSs) of a harbor porpoise were quantified at the center frequency (6.5 kHz), at 0.5, 1.0, and 1.3 octaves above the center frequency (9.2, 13.0, and 16.0 kHz), and at a frequency assumed to be ecologically important for harbor porpoises (125 kHz, the center frequency of their echolocation signals) by means of a psychoacoustic technique. The hearing frequency at which the maximum TTS occurred depended on the SPLav.re. The higher the SPLav.re., the higher the TTS induced at frequencies higher than the exposure frequency; below 148 dB re 1 µPa, the maximum TTS was at 6.5 kHz, whereas above 148 dB re 1 µPa, the maximum TTS was at 9.2 kHz. The hearing threshold of the harbor porpoise for the center frequency of its echolocation signals (125 kHz) was not affected at the highest SPLav.re. to which the animal was exposed.

Effect of level, duration, and inter-pulse interval of 1-2 kHz sonar signal exposures on harbor porpoise hearing.

Safety criteria for underwater low-frequency active sonar sounds produced during naval exercises are needed to protect harbor porpoise hearing. As a first step toward defining criteria, a porpoise was exposed to sequences consisting of series of 1-s, 1-2 kHz sonar down-sweeps without harmonics (as fatiguing noise) at various combinations of average received sound pressure levels (SPLs; 144-179 dB re 1 µPa), exposure durations (1.9-240 min), and duty cycles (5%-100%). Hearing thresholds were determined for a narrow-band frequency-swept sine wave centered at 1.5 kHz before exposure to the fatiguing noise, and at 1-4, 4-8, 8-12, 48, 96, 144, and 1400 min after exposure, to quantify temporary threshold shifts (TTSs) and recovery of hearing. Results show that the inter-pulse interval of the fatiguing noise is an important parameter in determining the magnitude of noise-induced TTS. For the reported range of exposure combinations (duration and SPL), the energy of the exposure (i.e., cumulative sound exposure level; SELcum) can be used to predict the induced TTS, if the inter-pulse interval is known. Exposures with equal SELcum but with different inter-pulse intervals do not result in the same induced TTS.

Hearing frequency thresholds of a harbor porpoise (Phocoena phocoena) temporarily affected by a continuous 1.5 kHz tone.

Harbor porpoises may suffer hearing loss when exposed to intense sounds. After exposure to a 1.5 kHz continuous tone without harmonics at a mean received sound pressure level of 154 dB re 1 µPa for 60 min (cumulative sound exposure level: 190 dB re 1 µPa(2) s), the temporary hearing threshold shift (TTS) of a porpoise was quantified at 1.5, 2, 4, 6.5, 8, 16, 32, 63, and 125 kHz with a psychoacoustic technique. Significant TTS only occurred at 1.5 and 2 kHz. Mean TTS (1-4 min after sound exposure stopped) was ~14 dB at 1.5 kHz and ~11 dB at 2 kHz, and recovery occurred within 96 min. Control hearing tests before and after a 60 min low ambient noise exposure showed that normal variation in TTS was limited (standard deviation: ± 1.0 dB). Ecological effects of TTS depend not only on the magnitude of the TTS, its duration (depending on the exposure duration), and the recovery time after the exposure stopped, but also on the hearing frequency affected by the fatiguing noise. The hearing thresholds of harbor porpoises for the frequencies of their echolocation signals are not affected by intense low frequency sounds, therefore these sounds are unlikely to affect foraging efficiency.

Hearing thresholds of a harbor porpoise (Phocoena phocoena) for playbacks of multiple pile driving strike sounds.

Pile driving is presently the most common method used to attach wind turbines to the sea bed. To assess the impact of pile driving sounds on harbor porpoises, it is important to know at what distance these sounds can be detected. Using a psychophysical technique, a male porpoise's hearing thresholds were obtained for series of five pile driving sounds (inter-pulse interval 1.2-1.3 s) recorded at 100 and 800 m from the pile driving site, and played back in a pool. The 50% detection threshold sound exposure levels (SELs) for the first sound of the series (no masking) were 72 (100 m) and 74 (800 m) dB re 1 µPa(2)s. Multiple sounds in succession (series) caused a ~5 dB decrease in hearing threshold; the mean 50% detection threshold SELs for any sound in the series were 68 (100 m) and 69 (800 m) dB re 1 µPa(2)s. Depending on the actual propagation conditions and background noise levels, the results suggest that pile driving sounds are audible to porpoises at least at tens of kilometers from pile driving sites.

Hearing thresholds of two harbor seals (Phoca vitulina) for playbacks of multiple pile driving strike sounds.

Pile driving, which creates high amplitude sounds with potentially negative impacts on the marine environment, is used to attach wind turbines to the sea bed. To quantify the distance at which pile driving sounds can be detected by harbor seals, unmasked hearing thresholds were obtained for series of five pile driving sounds recorded at 100 and 800 m from a pile driving location. The played back spectra resembled the spectra of sounds recorded under certain conditions 10-50 km from an offshore pile driving site. The lower the received level, the later within the series of sounds the harbor seals responded. The mean 50% detection threshold sound exposure levels for any sound in the series were: 40 (seal 01, 100 m), 39 (seal 01, 800 m), 43 (seal 02, 100 m), and 43 (seal 02, 800 m) dB re 1 µPa(2)s (add 9 dB for sound pressure level, dB re 1 µPa). The mean 50% detection thresholds based on detection of only the first sound of the series were ca. 5 dB higher. Detection at sea depends on the actual propagation conditions and on the degree of masking of the sounds by ambient noise, but the present study suggests that pile driving sounds are audible to harbor seals up to hundreds of kilometers from pile driving sites.

Hearing threshold shifts and recovery in harbor seals (Phoca vitulina) after octave-band noise exposure at 4 kHz.

Safety criteria for underwater sounds from offshore pile driving are needed to protect marine mammals. As a first step toward understanding effects of impulsive sounds, two harbor seals were exposed to octave-band white noise centered at 4 kHz at three mean received sound pressure levels (SPLs; 124, 136, and 148 dB re 1 µPa) at up to six durations (7.5, 15, 30, 60, 120, and 240 min); mean received sound exposure level (SEL) range was 166-190 dB re 1 µPa(2) s. Hearing thresholds were determined before and after exposure. Temporary hearing threshold shifts (TTS) and subsequent recovery were quantified as changes in hearing thresholds at 1-4, 4-8, 8-12, 48, and 96 min after noise exposure in seal 01, and at 12-16, 16-20, 20-24, 60, and 108 min after exposure in seal 02. Maximum TTS (1-4 min after 120 min exposure to 148 dB re 1 µPa; 187 dB SEL) was 10 dB. Recovery occurred within ~60 min. Statistically significant TTSs (>2.5 dB) began to occur at SELs of ~170 (136 SPL, 60 min) and 178 dB re 1 µPa(2) s (148 SPL, 15 min). However, SEL is not an optimal predictor of TTS for long duration, low SPL continuous noise, as duration and SPL play unequal roles in determining induced TTS.

The hearing threshold of a harbor porpoise (Phocoena phocoena) for impulsive sounds (L).

The distance at which harbor porpoises can hear underwater detonation sounds is unknown, but depends, among other factors, on the hearing threshold of the species for impulsive sounds. Therefore, the underwater hearing threshold of a young harbor porpoise for an impulsive sound, designed to mimic a detonation pulse, was quantified by using a psychophysical technique. The synthetic exponential pulse with a 5 ms time constant was produced and transmitted by an underwater projector in a pool. The resulting underwater sound, though modified by the response of the projection system and by the pool, exhibited the characteristic features of detonation sounds: A zero to peak sound pressure level of at least 30 dB (re 1 s(-1)) higher than the sound exposure level, and a short duration (34 ms). The animal's 50% detection threshold for this impulsive sound occurred at a received unweighted broadband sound exposure level of 60 dB re 1 µPa(2)s. It is shown that the porpoise's audiogram for short-duration tonal signals [Kastelein et al., J. Acoust. Soc. Am. 128, 3211-3222 (2010)] can be used to estimate its hearing threshold for impulsive sounds.

Threshold received sound pressure levels of single 1-2 kHz and 6-7 kHz up-sweeps and down-sweeps causing startle responses in a harbor porpoise (Phocoena phocoena).

Mid-frequency and low-frequency sonar systems produce frequency-modulated sweeps which may affect harbor porpoises. To study the effect of sweeps on behavioral responses (specifically "startle" responses, which we define as sudden changes in swimming speed and/or direction), a harbor porpoise in a large pool was exposed to three pairs of sweeps: a 1-2 kHz up-sweep was compared with a 2-1 kHz down-sweep, both with and without harmonics, and a 6-7 kHz up-sweep was compared with a 7-6 kHz down-sweep without harmonics. Sweeps were presented at five spatially averaged received levels (mRLs; 6 dB steps; identical for the up-sweep and down-sweep of each pair). During sweep presentation, startle responses were recorded. There was no difference in the mRLs causing startle responses for up-sweeps and down-sweeps within frequency pairs. For 1-2 kHz sweeps without harmonics, a 50% startle response rate occurred at mRLs of 133 dB re 1 µPa; for 1-2 kHz sweeps with strong harmonics at 99 dB re 1 µPa; for 6-7 kHz sweeps without harmonics at 101 dB re 1 µPa. Low-frequency (1-2 kHz) active naval sonar systems without harmonics can therefore operate at higher source levels than mid-frequency (6-7 kHz) active sonar systems without harmonics, with similar startle effects on porpoises.