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.

Temporal integration of tone signals by a killer whale (Orcinus orca).

A psychophysical procedure was used to measure pure-tone detection thresholds for a killer whale (Orcinus orca) as a function of both signal frequency and signal duration. Frequencies ranged between 1 and 100 kHz and signal durations ranged from 50 µs to 2 s, depending on the frequency. Detection thresholds decreased with an increase in signal duration up to a critical duration, which represents the auditory integration time. Integration times ranged from 4 ms at 100 kHz and increased up to 241 ms at 1 kHz. The killer whale data are similar to other odontocete species that have participated in similar experiments. The results have implications for noise impact predictions for signals with durations less than the auditory integration time.

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.

Physical effects of sound exposure from underwater explosions on Pacific mackerel (Scomber japonicus): Effects on the inner ear.

Studies of the effects of sounds from underwater explosions on fishes have not included examination of potential effects on the ear. Caged Pacific mackerel (Scomber japonicus) located at seven distances (between approximately 35 and 800 m) from a single detonation of 4.5 kg of C4 explosives were exposed. After fish were recovered from the cages, the sensory epithelia of the saccular region of the inner ears were prepared and then examined microscopically. The number of hair cell (HC) ciliary bundles was counted at ten preselected 2500 µm2 regions. HCs were significantly reduced in fish exposed to the explosion as compared to the controls. The extent of these differences varied by saccular region, with damage greater in the rostral and caudal ends and minimal in the central region. The extent of effect also varied in animals at different distances from the explosion, with damage occurring in fish as far away as 400 m. While extrapolation to other species and other conditions (e.g., depth, explosive size, and distance) must be performed with extreme caution, the effects of explosive sounds should be considered when environmental impacts are estimated for marine projects.

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.

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.

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.

Non-auditory, electrophysiological potentials preceding dolphin biosonar click production.

The auditory brainstem response to a dolphin's own emitted biosonar click can be measured by averaging epochs of the instantaneous electroencephalogram (EEG) that are time-locked to the emitted click. In this study, averaged EEGs were measured using surface electrodes placed on the head in six different configurations while dolphins performed an echolocation task. Simultaneously, biosonar click emissions were measured using contact hydrophones on the melon and a hydrophone in the farfield. The averaged EEGs revealed an electrophysiological potential (the pre-auditory wave, PAW) that preceded the production of each biosonar click. The largest PAW amplitudes occurred with the non-inverting electrode just right of the midline-the apparent side of biosonar click generation-and posterior of the blowhole. Although the source of the PAW is unknown, the temporal and spatial properties rule out an auditory source. The PAW may be a neural or myogenic potential associated with click production; however, it is not known if muscles within the dolphin nasal system can be actuated at the high rates reported for dolphin click production, or if sufficiently coordinated and fast motor endplates of nasal muscles exist to produce a PAW detectable with surface electrodes.

Connexin36 RNA Expression in the Cochlear Nucleus of the Echolocating Bat, Eptesicus fuscus.

PURPOSE: The echolocating bat is used as a model for studying the auditory nervous system because its specialized sensory capabilities arise from general mammalian auditory percepts such as pitch and sound source localization. These percepts are mediated by precise timing within neurons and networks of the lower auditory brainstem, where the gap junction protein Connexin36 (CX36) is expressed. Gap junctions and electrical synapses in the central nervous system are associated with fast transmission and synchronous patterns of firing within neuronal networks. The purpose of this study was to identify areas where CX36 was expressed in the bat cochlear nucleus to shed light on auditory brainstem networks in a hearing specialist animal model. METHODS: We investigated the distribution of CX36 RNA throughout the cochlear nucleus complex of the echolocating big brown bat, Eptesicus fuscus, using in situ hybridization. As a qualitative comparison, we visualized Gjd2 gene expression in the cochlear nucleus of transgenic CX36 reporter mice, species that hear ultrasound but do not echolocate. RESULTS: In both the bat and the mouse, CX36 is expressed in the anteroventral and in the dorsal cochlear nucleus, with more limited expression in the posteroventral cochlear nucleus. These results are generally consistent with previous work based on immunohistochemistry. CONCLUSION: Our data suggest that the anatomical substrate for CX36-mediated electrical neurotransmission is conserved in the mammalian CN across echolocating bats and non-echolocating mice.

Spike Train Similarity Space (SSIMS) Method Detects Effects of Obstacle Proximity and Experience on Temporal Patterning of Bat Biosonar.

Bats emit biosonar pulses in complex temporal patterns that change to accommodate dynamic surroundings. Efforts to quantify these patterns have included analyses of inter-pulse intervals, sonar sound groups, and changes in individual signal parameters such as duration or frequency. Here, the similarity in temporal structure between trains of biosonar pulses is assessed. The spike train similarity space (SSIMS) algorithm, originally designed for neural activity pattern analysis, was applied to determine which features of the environment influence temporal patterning of pulses emitted by flying big brown bats, Eptesicus fuscus. In these laboratory experiments, bats flew down a flight corridor through an obstacle array. The corridor varied in width (100, 70, or 40 cm) and shape (straight or curved). Using a relational point-process framework, SSIMS was able to discriminate between echolocation call sequences recorded from flights in each of the corridor widths. SSIMS was also able to tell the difference between pulse trains recorded during flights where corridor shape through the obstacle array matched the previous trials (fixed, or expected) as opposed to those recorded from flights with randomized corridor shape (variable, or unexpected), but only for the flight path shape in which the bats had previous training. The results show that experience influences the temporal patterns with which bats emit their echolocation calls. It is demonstrated that obstacle proximity to the bat affects call patterns more dramatically than flight path shape.