Discrimination of double-click synthetic echoes by bottlenose dolphins: Effects of inter-highlight interval and phasea).

Two bottlenose dolphins (Tursiops truncatus) were trained to discriminate double-click synthetic "echoes" differing in inter-highlight interval (IHI). In the first experimental task, dolphins passively listened to background (S-) stimuli with constant IHI and responded on discriminating a change to target (S+) stimuli with a slightly increased IHI. The second task was similar, but the highlights were assigned random, frequency-independent phase angles. This phase randomization was designed to interfere with potential auditory cues from characteristic spectral interference patterns linked to IHI changes. Discrimination thresholds were higher with randomized phase when the S- stimuli had IHIs of 50-250 µs. Thresholds were highest and comparable at the longest S- IHIs of 375 and 500 µs and were independent of phase condition. Although dolphin detection of changes in highlight envelope timing can explain threshold patterns at 375 and 500 µs, this cue did not explain performance at IHIs less than the dolphin auditory temporal window of ∼250 µs. Modeling results suggested that phase manipulations eliminated the availability of a simple difference in spectral magnitudes at the shortest IHIs, but the perception of a time separation pitch cue may still explain the dolphins' observed threshold patterns.

Dolphin short-term auditory fatigue and self-mitigation.

Auditory brainstem responses (ABRs) were measured at 57 kHz in two dolphins warned of an impending intense tone at 40 kHz. Over the course of testing, the duration of the intense tone was increased from 0.5 to 16 s to determine if changes in ABRs observed after cessation of the intense sound were the result of post-stimulatory auditory fatigue or conditioned hearing attenuation. One dolphin exhibited conditioned hearing attenuation after the warning sound preceding the intense sound, but little evidence of post-stimulatory fatigue after the intense sound. The second dolphin showed no conditioned attenuation before the intense sound, but auditory fatigue afterwards. The fatigue was observed within a few seconds after cessation of the intense tone: i.e., at time scales much shorter than those in previous studies of marine mammal noise-induced threshold shifts, which feature measurements on the order of a few minutes after exposure. The differences observed between the two individuals (less auditory fatigue in the dolphin that exhibited the conditioned attenuation) support the hypothesis that conditioned attenuation is a form of "self-mitigation."

The effects of range and echo-phase on range resolution in bottlenose dolphins (Tursiops truncatus) performing a successive comparison taska).

Echolocating bats and dolphins use biosonar to determine target range, but differences in range discrimination thresholds have been reported for the two species. Whether these differences represent a true difference in their sensory system capability is unknown. Here, the dolphin's range discrimination threshold as a function of absolute range and echo-phase was investigated. Using phantom echoes, the dolphins were trained to echo-inspect two simulated targets and indicate the closer target by pressing a paddle. One target was presented at a time, requiring the dolphin to hold the initial range in memory as they compared it to the second target. Range was simulated by manipulating echo-delay while the received echo levels, relative to the dolphins' clicks, were held constant. Range discrimination thresholds were determined at seven different ranges from 1.75 to 20 m. In contrast to bats, range discrimination thresholds increased from 4 to 75 cm, across the entire ranges tested. To investigate the acoustic features used more directly, discrimination thresholds were determined when the echo was given a random phase shift (±180°). Results for the constant-phase versus the random-phase echo were quantitatively similar, suggesting that dolphins used the envelope of the echo waveform to determine the difference in range.

Temporary threshold shift in bottlenose dolphins exposed to steady-state, 1/6-octave noise centered at 0.5 to 80 kHza).

Temporary threshold shift (TTS) was measured in bottlenose dolphins after 1-h exposures to 1/6-octave noise centered at 0.5, 2, 8, 20, 40, and 80 kHz. Tests were conducted in netted ocean enclosures, with the dolphins free-swimming during noise exposures. Exposure levels were estimated using a combination of video-based measurement of dolphin position, calibrated exposure sound fields, and animal-borne archival recording tags. Hearing thresholds were measured before and after exposures using behavioral methods (0.5, 2, 8 kHz) or behavioral and electrophysiological [auditory brainstem response (ABR)] methods (20, 40, 80 kHz). No substantial effects of the noise were seen at 40 and 80 kHz at the highest exposure levels. At 2, 8, and 20 kHz, exposure levels required for 6 dB of TTS (onset TTS exposures) were similar to previous studies; however, at 0.5 kHz, onset TTS was much lower than predicted values. No clear relationships could be identified between ABR- and behaviorally measured TTS. The results raise questions about the validity of current noise exposure guidelines for dolphins at frequencies below ∼1 kHz and how to accurately estimate received noise levels from free-swimming animals.

Effects of echo phase on bottlenose dolphin jittered-echo detection.

The ability of bottlenose dolphins to detect changes in echo phase was investigated using a jittered-echo paradigm. The dolphins' task was to produce a conditioned vocalization when phantom echoes with fixed echo delay and phase changed to those with delay and/or phase alternated ("jittered") on successive presentations. Conditions included: jittered delay plus constant phase shifts, ±45° and 0°-180° jittered phase shifts, alternating delay and phase shifts, and random echo-to-echo phase shifts. Results showed clear sensitivity to echo fine structure, revealed as discrimination performance reductions when jittering echo fine structures were similar, but envelopes were different, high performance with identical envelopes but different fine structure, and combinations of echo delay and phase jitter where their effects cancelled. Disruption of consistent echo fine structure via random phase shifts dramatically increased jitter detection thresholds. Sensitivity to echo fine structure in the present study was similar to the cross correlation function between jittering echoes and is consistent with the performance of a hypothetical coherent receiver; however, a coherent receiver is not necessary to obtain the present results, only that the auditory system is sensitive to echo fine structure.

Bottlenose dolphin temporary threshold shift following exposure to 10-ms impulses centered at 8 kHza).

Studies of marine mammal temporary threshold shift (TTS) from impulsive sources have typically produced small TTS magnitudes, likely due to much of the energy in tested sources lying below the subjects' range of best hearing. In this study of dolphin TTS, 10-ms impulses centered at 8 kHz were used with the goal of inducing larger magnitudes of TTS and assessing the time course of hearing recovery. Most impulses had sound pressure levels of 175-180 dB re 1 µPa, while inter-pulse interval (IPI) and total number of impulses were varied. Dolphin TTS increased with increasing cumulative sound exposure level (SEL) and there was no apparent effect of IPI for exposures with equal SEL. The lowest TTS onset was 184 dB re 1 µPa2s, although early exposures with 20-s IPI and cumulative SEL of 182-183 dB re 1 µPa2s produced respective TTS of 35 and 16 dB in two dolphins. Continued testing with higher SELs up to 191 dB re 1 µPa2s in one of those dolphins, however, failed to result in TTS greater than 14 dB. Recovery rates were similar to those from other studies with non-impulsive sources and depended on the magnitude of the initial TTS.

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.

Auditory masking in odobenid and otariid carnivoresa).

As the only living species within the odobenid lineage of carnivores, walruses (Odobenus rosmarus) have no close relatives from which auditory information can be extrapolated. Sea lions and fur seals in the otariid lineage are the nearest evolutionary outgroup. To advance understanding of odobenid and otariid hearing, we conducted behavioral testing with two walruses and one California sea lion (Zalophus californianus). Detection thresholds for airborne sounds were measured from 0.08 to at least 16 kHz in ambient noise conditions and then re-measured in the presence of octave-band white masking noise. Walruses were more sensitive than the sea lion at lower frequencies and less sensitive at higher frequencies. Critical ratios for the walruses ranged from 20 dB at 0.2 kHz to 32 dB at 10 kHz, while critical ratios for the sea lion ranged from 16 dB at 0.2 kHz to 35 dB at 32 kHz. The masking values for these species are comparable to one another and to those of terrestrial carnivores, increasing by about 3 dB per octave with increasing frequency. Despite apparent differences in hearing range and sensitivity, odobenids and otariids have a similar ability to hear signals in noisy conditions.

Dolphin conditioned hearing attenuation in response to repetitive tones with increasing level.

All species of toothed whales studied to date can learn to reduce their hearing sensitivity when warned of an impending intense sound; however, the specific conditions under which animals will employ this technique are not well understood. The present study was focused on determining whether dolphins would reduce their hearing sensitivity in response to an intense tone presented at a fixed rate but increasing level, without an otherwise explicit warning. Auditory brainstem responses (ABRs) to intermittent, 57-kHz tone bursts were continuously measured in two bottlenose dolphins as they were exposed to a series of 2-s, 40-kHz tones at fixed time intervals of 20, 25, or 29 s and at sound pressure levels (SPLs) increasing from 120 to 160 dB re 1 µPa. Results from one dolphin showed consistent ABR attenuation preceding intense tones when the SPL exceeded ∼140-150 dB re 1 µPa and the tone interval was 20 s. ABR attenuation with 25- or 29-s intense tone intervals was inconsistent. The second dolphin showed similar, but more subtle, effects. The results show dolphins can learn the timing of repetitive noise and may reduce their hearing sensitivity if the SPL is high enough, presumably to "self-mitigate" the noise effects.

Classification of simulated complex echoes based on highlight time separation in the bottlenose dolphin (Tursiops truncatus).

Previous studies suggested that dolphins perceive echo spectral features on coarse (macrospectrum) and fine (microspectrum) scales. This study was based on a finding that these auditory percepts are, to some degree, dependent on the dolphin's ∼250-µs auditory temporal window (i.e., "critical interval"). Here, two dolphins were trained to respond on passively detecting a simulated "target" echo complex [a pair of echo "highlights" with a characteristic 120-µs inter-highlight interval (IHI)]. This target had unique micro- and macrospectral features and was presented among "distractor" echoes with IHIs from 50 to 500 µs (i.e., microspectra) and various highlight durations (i.e., macrospectra). Following acquisition of this discrimination task, probe echo complexes with the macrospectrum of the target but IHIs matching the distractors were infrequently presented. Both dolphins initially responded more often to probes with IHIs of 80-200 µs. Response strategies diverged with increasing probe presentations; one dolphin responded to a progressively narrower range of probe IHIs while the second increased response rates for probes with IHIs > 250 µs. These results support previous conclusions that perception of macrospectra for complex echoes is nonconstant as the IHI decreases below ∼100 µs, but results approaching and exceeding 250 µs-the temporal window upper boundary-were more ambiguous.

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.

Measuring auditory cortical responses in Tursiops truncatus.

Auditory neuroscience in dolphins has largely focused on auditory brainstem responses; however, such measures reveal little about the cognitive processes dolphins employ during echolocation and acoustic communication. The few previous studies of mid- and long-latency auditory-evoked potentials (AEPs) in dolphins report different latencies, polarities, and magnitudes. These inconsistencies may be due to any number of differences in methodology, but these studies do not make it clear which methodological differences may account for the disparities. The present study evaluates how electrode placement and pre-processing methods affect mid- and long-latency AEPs in (Tursiops truncatus). AEPs were measured when reference electrodes were placed on the skin surface over the forehead, the external auditory meatus, or the dorsal surface anterior to the dorsal fin. Data were pre-processed with or without a digital 50-Hz low-pass filter, and the use of independent component analysis to isolate signal components related to neural processes from other signals. Results suggest that a meatus reference electrode provides the highest quality AEP signals for analyses in sensor space, whereas a dorsal reference yielded nominal improvements in component space. These results provide guidance for measuring cortical AEPs in dolphins, supporting future studies of their cognitive auditory processing.

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.

Offset auditory brainstem response (ABR) amplitude in bottlenose dolphins.

Although commonly recorded as onset responses, the auditory brainstem response (ABR) can also be elicited at stimulus offset. The offset ABR has not been extensively investigated in marine mammals. Three normal hearing (NH) and three hearing impaired (HI) dolphins were assessed while fully submerged in sea water. Stimulus spectrum, level, rise/fall time (RFT), and plateau duration were manipulated. Onset and offset ABR amplitude were quantified as the rms voltage 1-7 ms following stimulus onset or offset, respectively. For the same stimulus conditions, onset and offset responses were often larger for NH than HI dolphins, and offset responses were typically smaller than onset responses. For the level series, offset response amplitude typically increased with increasing stimulus level, although offset responses were not 3 dB above the noisefloor for 113-kHz tonebursts. Increasing RFT decreased onset and offset response amplitude. For the 40-kHz tonebursts, a RFT of 32 µs produced a large amplitude offset ABR in NH dolphins. Offset responses for 113-kHz tonebursts were 3 dB above the noisefloor at the shortest RFTs. Offset responses were largest for 4 ms duration stimuli (likely due to overlapping onset and offset response analysis windows), but otherwise, offset responses changed little with increasing duration.

Classification of biosonar target echoes based on coarse and fine spectral features in the bottlenose dolphin (Tursiops truncatus).

Previous bottlenose dolphin studies suggest that the coarse envelope of an echo spectrum ("macrostructure") has hierarchical dominance over finer-scale spectral features ("microstructure") during synthetic echo discrimination tasks. In this study, two dolphins listened to and discriminated between underwater sound stimuli consisting of pairs of clicks with different micro- and macrostructures. After conditioning dolphins to reliably discriminate between two "anchor" stimuli with different micro- and macrostructures, probe stimuli, which contained a macrostructure identical to one of the anchor stimuli and the microstructure of the alternate anchor, were infrequently presented. Dolphins responded to probes in a manner consistent with macrostructure primacy.

Detection of simulated patterned echo packets by bottlenose dolphins (Tursiops truncatus).

Dolphins performing long-range biosonar tasks sometimes use "packets" of clicks, where inter-click-intervals within each packet are less than the two-way acoustic travel time from dolphin to target. The multi-echo nature of packets results in lower detection thresholds than single echoes; however, other potential benefits of packet use remain unexplored. The present study investigated whether structured temporal patterns observed in click packets impart some advantage in detecting echo-like signals embedded in noise. Two bottlenose dolphins were trained to passively listen and detect simulated packets of echoes in background noise consisting of either steady-state broadband Gaussian noise, or Gaussian noise containing randomly presented impulses similar to dolphin clicks. Four different inter-stimulus-interval (ISI) patterns (constant, random, increasing, or decreasing ISI within each packet) were tested. It was hypothesized that decreasing ISIs-found naturally in dolphin packets-would result in the lowest thresholds, while random, unlearnable patterns would result in the highest. However, no biologically significant differences in threshold were found among the four ISI patterns for either noise condition. Thus, the bottlenose dolphin's stereotypical pattern of decreasing ISI during active echolocation did not appear to provide an advantage in packet detection in this passive listening task.

Effects of dolphin hearing bandwidth on biosonar click emissions.

Differences in odontocete biosonar emissions have been reported for animals with hearing loss compared to those with normal hearing. For example, some animals with high-frequency hearing loss have been observed to lower the dominant frequencies of biosonar signals to better match a reduced audible frequency range. However, these observations have been limited to only a few individuals and there has been no systematic effort to examine how animals with varying degrees of hearing loss might alter biosonar click properties. In the present study, relationships between age, biosonar click emissions, auditory evoked potentials (AEPs), and hearing bandwidth were studied in 16 bottlenose dolphins (Tursiops truncatus) of various ages and hearing capabilities. Underwater hearing thresholds were estimated by measuring steady-state AEPs to sinusoidal amplitude modulated tones at frequencies from 23 to 152 kHz. Input-output functions were generated at each tested frequency and used to calculate frequency-specific thresholds and the upper-frequency limit of hearing for each subject. Click emissions were measured during a biosonar aspect change detection task using a physical target. Relationships between hearing capabilities and the acoustic parameters of biosonar signals are described here and compared to previous experiments with fewer subjects.

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.

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.

Directional hearing sensitivity for 2-30 kHz sounds in the bottlenose dolphin (Tursiops truncatus).

Bottlenose dolphins (Tursiops truncatus) depend on sounds at frequencies lower than 30 kHz for social communication, but little information on the directional dependence of hearing thresholds for these frequencies exists. This study measured underwater behavioral hearing thresholds for 2, 10, 20, and 30 kHz sounds projected from eight different positions around dolphins in both the horizontal and vertical planes. The results showed that the sound source direction relative to the dolphin affected hearing threshold, and that directional characteristics of the receiving beam pattern were frequency dependent. Hearing thresholds obtained from two adult dolphins demonstrated a positive relationship between directivity of hearing and stimulus frequency, with asymmetric receiving beam patterns in both the horizontal and vertical planes. Projecting sound from directly behind the dolphin resulted in frequency-dependent increases in hearing threshold up to 18.5 dB compared to when sound was projected in front. When the projector was situated above the dolphin thresholds were approximately 8 dB higher as compared to below. This study demonstrates that directional hearing exists for lower frequencies than previously expected.