CETACEAN AUDITORY PSYCHOPHYSICS

ABSTRACT

The dolphin continues to capture the imagination of investigators because of its ability to echolocate. Echolocation is essentially a special extension and adaptation of the dolphin's hearing system, coupled with the animal's ability to generate special sounds. Humans have demonstrated the ability to judge room size based on reverberation from a voice, and some of the visually challenged use self-generated sounds to detect large reflective objects. Echolocation represents a highly refined acoustic ability on a broad acoustic sensory continuum. Research on the auditory and echolocation performance of cetaceans has moved forward slowly due to limited animal resources and the general high cost of maintaining these animals in a laboratory environment.

This paper reviews some of the more relevant psychoacoustic data on cetaceans, and concentrates on the bottlenose dolphin Tursiops truncatus. The information presented is not at all exhaustive. Early work with dolphins focused mainly on the animal's ability to use its echolocation system. Once echolocation capability was demonstrated using a blindfolded dolphin, the quest to understand dolphin sonar moved from qualifying the dolphin's echolocation skill to quantifying its basic capabilities.

Psychophysics, and more precisely psychoacoustics, provides the tools to study dolphin echolocation. The procedures, theories and even the apparatuses from the traditional psychoacoustics laboratory are adapted to the dolphin experimental setting to measure and analyze the sensory phenomenon of dolphin echolocation. Basic auditory phenomena such as the audiogram, the effects of masking, critical ratio and critical band, and interaural time and intensity discrimination capabilities have been explored in the dolphin. Additionally, special experiments investigating the psychoacoustics of the echolocation system in particular have been conducted.     

Passive hearing stability in the bottlenose dolphin Tursiops truncatus to low frequency noise spectrum deformation

In behavioral experiments on bottlenose dolphins there was evaluated efficiency of identification of the low frequency noises that represent a certain rhythmical sequence of impulses, at destabilization of their spectra by the method of frequency wobble. Results of the experiments have shown that disturbance of spectral structure at erosion of its discrete components does not lead to a decrease of efficiency of the noise identification, which indicates the greater significance of the time, rather than spectral mechanisms at processing of the complex acoustic signals by the dolphin auditory system.     

MY EXPERIENCE OF DIGITAL RECORDING

ABSTRACT

Object classifiers that attempt to mimic dolphin echolocation require an auditory weighting function representative of dolphin peripheral auditory processing. An evolutionary program (EvPg) was used to fit the frequency-dependent output of a bank of bandpass filters to the auditory sensitivity of the bottlenose dolphin, Tursiops truncatus. Pseudo-Gaussian (PG) and rounded exponential (ROEX) functions were used to describe individual filter shapes. Variables determining the number of filters per model, overall filter shape and amplitude scaling were submitted to the EvPg for optimization. Maximum deviation (P _e ) between model output and the sensitivity of the dolphin was used as a measure of similarity between the two, i.e., lower P _e indicated a greater similarity. The number of filters converged upon 37 for all ROEX models and ≤ 45 for all PG models. The P _e of the best-performing PG model was 0.08, and for all ROEX models was 0.13. Greatest deviations typically occurred below 5 kHz and above 130 kHz. Relative audiometric sensitivity of a dolphin ear model has been improved relative to previous models, thereby providing an auditory weighting function more representative of dolphin peripheral auditory processing. This model will be applied to further investigate how dolphins use echolocation to discriminate among objects.     

Diffusion tensor imaging of dolphin brains reveals direct auditory pathway to temporal lobe

The brains of odontocetes (toothed whales) look grossly different from their terrestrial relatives. Because of their adaptation to the aquatic environment and their reliance on echolocation, the odontocetes'' auditory system is both unique and crucial to their survival. Yet, scant data exist about the functional organization of the cetacean auditory system. A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of ‘associative′ regions in lateral and caudal directions. However, the precise location of the auditory cortex and its connections are still unknown. Here, we used a novel diffusion tensor imaging (DTI) sequence in archival post-mortem brains of a common dolphin (Delphinus delphis) and a pantropical dolphin (Stenella attenuata) to map their sensory and motor systems. Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1. But in addition to suprasylvian-A1, we report here, for the first time, the auditory cortex also exists in the temporal lobe, in a region near cetacean-A2 and possibly analogous to the primary auditory cortex in related terrestrial mammals (Artiodactyla). Using probabilistic tract tracing, we found a direct pathway from the inferior colliculus to the medial geniculate nucleus to the temporal lobe near the sylvian fissure. Our results demonstrate the feasibility of post-mortem DTI in archival specimens to answer basic questions in comparative neurobiology in a way that has not previously been possible and shows a link between the cetacean auditory system and those of terrestrial mammals. Given that fresh cetacean specimens are relatively rare, the ability to measure connectivity in archival specimens opens up a plethora of possibilities for investigating neuroanatomy in cetaceans and other species.     

Auditory temporal resolution of a wild white-beaked dolphin (<Emphasis Type="Italic">Lagenorhynchus albirostris</Emphasis>)

Adequate temporal resolution is required across taxa to properly utilize amplitude modulated acoustic signals. Among mammals, odontocete marine mammals are considered to have relatively high temporal resolution, which is a selective advantage when processing fast traveling underwater sound. However, multiple methods used to estimate auditory temporal resolution have left comparisons among odontocetes and other mammals somewhat vague. Here we present the estimated auditory temporal resolution of an adult male white-beaked dolphin, (Lagenorhynchus albirostris), using auditory evoked potentials and click stimuli. Ours is the first of such studies performed on a wild dolphin in a capture-and-release scenario. The white-beaked dolphin followed rhythmic clicks up to a rate of approximately 1,125–1,250 Hz, after which the modulation rate transfer function (MRTF) cut-off steeply. However, 10% of the maximum response was still found at 1,450 Hz indicating high temporal resolution. The MRTF was similar in shape and bandwidth to that of other odontocetes. The estimated maximal temporal resolution of white-beaked dolphins and other odontocetes was approximately twice that of pinnipeds and manatees, and more than ten-times faster than humans and gerbils. The exceptionally high temporal resolution abilities of odontocetes are likely due primarily to echolocation capabilities that require rapid processing of acoustic cues.     

Adaptive Changes of Spatial Characteristics of Hearing in the Dolphin Tursiops truncatus

Adaptive abilities of the dolphin auditory system at perception of tonal signals of different frequencies were studied under conditions of spatial uncertainty of their presentation in the noise field. It has been shown that a transition from the threshold to the suprathreshold detection is accompanied by adaptive changes of spatial characteristics of auditory perception: transformation of the one-lobe direction diagrams into the two-lobe ones is observed, as well as their broadening and a shift of the sensitivity maximum from the frontal direction to the side one. The dependence of direction characteristics on frequency of the perceived signal is lost.     

The modulation rate transfer function of a harbour porpoise (Phocoena phocoena)

During echolocation, toothed whales produce ultrasonic clicks at extremely rapid rates and listen for the returning echoes. The auditory brainstem response (ABR) duration was evaluated in terms of latency between single peaks: 5.5 ms (from peak I to VII), 3.4 ms (I–VI), and 1.4 ms (II–IV). In comparison to the killer whale and the bottlenose dolphin, the ABR of the harbour porpoise has shorter intervals between the peaks and consequently a shorter ABR duration. This indicates that the ABR duration and peak latencies are possibly related to the relative size of the auditory structures of the central nervous system and thus to the animal’s size. The ABR to a sinusoidal amplitude modulated stimulus at 125 kHz (sensitivity threshold 63 dB re 1 μPa rms) was evaluated to determine the modulation rate transfer function of a harbour porpoise. The ABR showed distinct envelope following responses up to a modulation rate of 1,900 Hz. The corresponding calculated equivalent rectangular duration of 263 μs indicates a good temporal resolution in the harbour porpoise auditory system similar to the one for the bottlenose dolphin. The results explain how the harbour porpoise can follow clicks and echoes during echolocation with very short inter click intervals.     

The dolphin cochlear nucleus: Topography,histology and functional implications

Despite the outstanding auditory capabilities of dolphins, there is only limited information available on the cytology of the auditory brain stem nuclei in these animals. Here, we investigated the cochlear nuclei (CN) of five brains of common dolphins (Delphinus delphis) and La Plata dolphins (Pontoporia blainvillei) using cell and fiber stain microslide series representing the three main anatomical planes. In general, the CN in dolphins comprise the same set of subnuclei as in other mammals. However, the volume ratio of the dorsal cochlear nucleus (DCN) in relation to the ventral cochlear nucleus (VCN) of dolphins represents a minimum among the mammals examined so far. Because, for example, in cats the DCN is necessary for reflexive orientation of the head and pinnae towards a sound source, the massive restrictions in head movability in dolphins and the absence of outer ears may be correlated with the reduction of the DCN. Moreover, the same set of main neuron types were found in the dolphin CN as in other mammals, including octopus and multipolar cells. Because the latter two types of neurons are thought to be involved in the recognition of complex sounds, including speech, we suggest that, in dolphins, they may be involved in the processing of their communication signals. Comparison of the toothed whale species studied here revealed that large spherical cells were present in the La Plata dolphin but absent in the common dolphin. These neurons are known to be engaged in the processing of low‐frequency sounds in terrestrial mammals. Accordingly, in the common dolphin, the absence of large spherical cells seems to be correlated with a shift of its auditory spectrum into the high‐frequency range above 20 kHz. The existence of large spherical cells in the VCN of the La Plata dolphin, however, is enigmatic asthis species uses frequencies around 130 kHz. J. Morphol. 2011. © 2011 Wiley Periodicals, Inc.     

Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal,frequency and amplitude discrimination

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus, and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius) and a potential predator (dolphin Tursiops truncatus). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.     

Cytoarchitecture of the formatio reticularis of the brain stem of the dolphin]

In the present study some qualitative and quantitative features of the reticular formation of the medulla oblongata, pons and midbrain have been elucidated by cytoarchitectonic methods in the dolphin (Tursiops truncatus). The studies have demonstrated that similar to land mammalia, the dolphin has a reticular formation made up of spatially open cell groups lying in the deepest parts of the brain stem. Cytoarchitectonically the component parts of the reticular formation show a number of peculiarities enabling us to distinguish separate nuclei. In the dolphin peculiar architectonics have been observed in the nucleus gigantocellularis medullae oblongatae, nucleus papillioformis or the nucleus reticularis tegmenti Bechterewi and the nucleus centralis superior medialis seu ventralis. Fairly poor in cells are the nucleus centralis caudalis pontis and the nucleus centralis oralis pontis. We failed to single out as autonomous nuclei cell groups corresponding to the nucleus funiculi lateralis and the nucleus paratrochlearis of the land mammalia. The size and density of cells in nuclei have a number of peculiarities. The analysis of the ratios of the brainstem volume to that of reticular structures has shown them to be the smallest in the dolphin as compared with land mammals. The smaller share held by the brain-stem reticular formation and its cytoarchitectonic features can be associated with the functional properties resulting from the greater specialization of some of brain-stem systems (e.g. auditory, vestibular, extrapyramidal etc.) in the dolphin in comparison with land mammals.     

Hearing loss in stranded odontocete dolphins and whales

The causes of dolphin and whale stranding can often be difficult to determine. Because toothed whales rely on echolocation for orientation and feeding, hearing deficits could lead to stranding. We report on the results of auditory evoked potential measurements from eight species of odontocete cetaceans that were found stranded or severely entangled in fishing gear during the period 2004 through 2009. Approximately 57% of the bottlenose dolphins and 36% of the rough-toothed dolphins had significant hearing deficits with a reduction in sensitivity equivalent to severe (70-90 dB) or profound (>90 dB) hearing loss in humans. The only stranded short-finned pilot whale examined had profound hearing loss. No impairments were detected in seven Risso's dolphins from three different stranding events, two pygmy killer whales, one Atlantic spotted dolphin, one spinner dolphin, or a juvenile Gervais' beaked whale. Hearing impairment could play a significant role in some cetacean stranding events, and the hearing of all cetaceans in rehabilitation should be tested.     

Characterization of beam patterns of bottlenose dolphin in the transversal plane

The characteristics of the absolute auditory sensitivity of the bottlenose dolphin (Tursiops truncatus p.) in the transverse plane have been measured using short broad-band stimuli simulating dolphin clicks (with energy maximum at frequencies 8, 16, 30, 50 and 100 kHz). Experiments were performed using the method of conditioned reflexes with food reinforcement. It was shown that, in the frequency range of 8-30 kHz, the absolute sensitivity of dolphin hearing in any ventral and lateral directions of the transverse plane is only by 2-8 dB worse than in the nasal direction. Moreover, it is approximately by 25-30 dB better than at frequencies of 50-100 kHz. At frequencies of 8-30 kHz, a pronounced dorsoventral asymmetry has been observed. In this frequency range, it reaches approximately 15-18 dB whereas at frequencies of 50-100 kHz, this asymmetry decreases to 2-3 dB. In the dorsal direction, the auditory sensitivity is by 18 dB worse than in the nasal one at frequencies of around 8 kHz, and the difference rises smoothly to 33 dB at frequencies of about 100 kHz. At frequencies of 50-100 kHz, the acoustical thresholds of the cross-section plane in comparison with thresholds for the with nasal direction get worse almost uniformly in all directions by 25-33 dB. As a result, in the transversal plane, the beam patterns have a nearly circular form, unlike the patterns at frequencies of 8-30 kHz. The results are discussed in terms of the model of sound perception through the left and right mental foramens. The biological expediency of the asymmetry is emphasized.     

Specialized sound reception in dolphins—a hint for the function of the dorsal cochlear nucleus in mammals

Dolphins have developed a specialized system for sound reception. Their pinnae are reduced and shifted under the skin, and sound is transduced via the lower jaw to the auditory ossicles. In line with their auditory functions (notably echolocation), most auditory nuclei in the brain stem of dolphins are extremely well‐developed. In contrast, the dorsal cochlear nucleus is drastically reduced. In the La Plata dolphin the volume of the dorsal cochlear nucleus is 4 mm³, while that of the ventral cochlear nucleus is 98 mm³. The reduction in size of the dorsal cochlear nucleus is also seen in baleen whales, which do not echolocate and are, in contrast to dolphins, tuned to deep frequencies. However, dolphins and baleen whales have the reduction of the outer ear in common. In humans, cats, bats and seals, there is a correlation between the development of pinnae and the dorsal cochlear nucleus. So, we conclude that the function of the dorsal cochlear nucleus in mammals could be to eliminate “auditory artifacts”; arising from the operation of the pinnae.     

Parallel evolution of auditory genes for echolocation in bats and toothed whales

The ability of bats and toothed whales to echolocate is a remarkable case of convergent evolution. Previous genetic studies have documented parallel evolution of nucleotide sequences in Prestin and KCNQ4, both of which are associated with voltage motility during the cochlear amplification of signals. Echolocation involves complex mechanisms. The most important factors include cochlear amplification, nerve transmission, and signal re-coding. Herein, we screen three genes that play different roles in this auditory system. Cadherin 23 (Cdh23) and its ligand, protocadherin 15 (Pcdh15), are essential for bundling motility in the sensory hair. Otoferlin (Otof) responds to nerve signal transmission in the auditory inner hair cell. Signals of parallel evolution occur in all three genes in the three groups of echolocators--two groups of bats (Yangochiroptera and Rhinolophoidea) plus the dolphin. Significant signals of positive selection also occur in Cdh23 in the Rhinolophoidea and dolphin, and Pcdh15 in Yangochiroptera. In addition, adult echolocating bats have higher levels of Otof expression in the auditory cortex than do their embryos and non-echolocation bats. Cdh23 and Pcdh15 encode the upper and lower parts of tip-links, and both genes show signals of convergent evolution and positive selection in echolocators, implying that they may co-evolve to optimize cochlear amplification. Convergent evolution and expression patterns of Otof suggest the potential role of nerve and brain in echolocation. Our synthesis of gene sequence and gene expression analyses reveals that positive selection, parallel evolution, and perhaps co-evolution and gene expression affect multiple hearing genes that play different roles in audition, including voltage and bundle motility in cochlear amplification, nerve transmission, and brain function.     

Mechanisms of sound reception and conduction in the dolphin

Morphology of the dolphin’s lower jaw, model and behavioral experiments are discussed with the aim of exploring the mechanisms of sound reception and conduction to the lower jaw canals, taking into account the known concepts of acoustics and the theory of grouped antennas. It is shown that the left and right rows of mental foramens with the respective mandibular canal and tissues of the canals are forming the new external ear and the new external auditory duct whereby sound (in the frequency band of 0.1–160 kHz) is transmitted into the middle ear, in contrast to the dolphin’s nonfunctional outer ear. This new external ear is created by nature as a receiving array of traveling-wave antennas located in the throat of an acoustic horn (the respective mandibular canal). The results give reason to assume the existence of a similar new external ear in Odontoceti.     

Characterization of beam patterns of bottlenose dolphin in the transverse plane

The characteristics of absolute auditory sensitivity of the bottlenose dolphin (Tursiops truncatus) in the transverse plane have been measured using short broadband stimuli simulating dolphin clicks (with energy maximum at frequencies 8, 16, 30, 50 and 100 kHz). Experiments were performed using the method of conditioned reflexes with food reinforcement. It is shown that, in the frequency range of 8–30 kHz, the absolute sensitivity of dolphin hearing in any ventral and lateral directions of the transverse plane is only 2–8 dB worse than in the rostral direction. Moreover, it is 25–30 dB better than at 50–100 kHz. At 8–30 kHz, pronounced dorsoventral asymmetry has been observed. In this frequency range, it reaches 15–18 dB whereas at 50–100 kHz this asymmetry decreases to 2–3 dB. In the dorsal direction, the auditory sensitivity is 18 dB worse than in the rostral one at ∼8 kHz, and the difference rises smoothly to 33 dB at ∼100 kHz. At 50–100 kHz, the acoustical thresholds in the transverse plane relative to those for the with rostral direction get worse almost uniformly in all directions by 25–33 dB. As a result, in the transverse plane the beam patterns are nearly circular, unlike those at 8–30 kHz. The results are discussed in terms of the model of sound perception through the left and right mental foramens. The biological relevance of such asymmetry is emphasized.     

Evolutionary strategies of odontocete brain development

The development of the brain was studied in several species of toothed whales (harbour porpoise, spotted dolphin, narwhal, and sperm whale). As embryos, odontocetes show the general mammalian bauplan. The olfactory bulb, lacking in adult toothed whales, forms in embryos but then disappears in early fetal development. In contrast, the terminal nerve persists and shows a great increase in neuron number. Some components of the limbic system are reduced while others grow to become relatively large. The pyramidal tract is inconspicuous. The auditory system and the extrapyramidal system show rapid size increase. In the sperm whale, growth of the telencephalic hemispheres relative to the size of the brain as a whole (telencephalization) and expansion of the cortical areas (neocorticalization) are greater than in other mammals. Increases in the diameters of the cranial nerves seem to be correlated with their presumed functional roles in the postnatal animal.     

ECHOLOCATION IN DOLPHINS WITH A DOLPHIN-BAT COMPARISON

ABSTRACT

Dolphins possess a highly sophisticated auditory system and a keen capability for echolocation. Signals are emitted in the form of high intensity, short duration, broadband exponentially decaying pulses. The frequency spectra of echolocation signals used by many dolphins are dependent on the output intensity of the signals and not on any fine tuning by the animals. When the output intensity is low, the center frequency of the click tends to be low. As the output intensity increases, the center frequency also tends to increase. The pulses propagate from the dolphin's melon in a relatively narrow beam, and echoes are received via the lower jaw, with a slightly wider beam. Echo- locating dolphins can detect targets at ranges of approximately 100 plus meters, depending on the size of the targets. Target discrimination experiments have shown that dolphins can discriminate the shape, size, material composition and internal structure of targets from the echoes. The broadband short duration properties of the signal allow the echoes to have high temporal resolution, so that within the structure of the echoes a considerable amount of information on the properties of the target can be conveyed. A brief comparison between the bat and dolphin sonar system will also be made. Bats typically emit much longer signals and a wider variety of different types of signals than dolphins. Signals used by some bats are suited to detecting Doppler shift, whereas the dolphin signal is designed to be tolerant of Doppler effects.     

白鱀豚的声训练

1982年4月—1983年4月对一头白暨豚进行了训练,目标识别实验的结果表明,白暨豚愿意满足训练员的要求,且记忆力较强。     

The use of auditory stimulants during swim encounters with Hector's dolphins (Cephalorhynchus hectori hectori) in Akaroa Harbour,New Zealand

The coastal distribution of Hector's dolphins and their attraction to vessels make them easily accessible to commercial tour operations. For over 25 yr, tour operators have been undertaking view and swim‐with‐dolphin trips in Akaroa Harbour, New Zealand. Since 2003, auditory stimulants, in particular stones, have been provided during such swim encounters. The potential effects associated with such stimulants have not, until now, been examined. Here, we investigate the effects of stones and other human‐induced noise on Hector's dolphin behavior. The use of stones significantly affected how dolphins interacted with swimmers. Specifically, swimmers who used stones had a greater probability of close approaches by dolphins than those who sang or simply floated on the surface of the water. The number of close and sustained approaches was also significantly higher for swimmers using stones. Dolphins were more interactive with active swimmers, approaching closer and engaging for longer than with nonactive swimmers. Dolphins socializing had a tendency to be engaged longer with swimmers. The use of stones as an auditory stimulant to sustain or enhance interactions with dolphins by artificial means may not be in the best interest of an endangered species, which already faces a range of challenges due to human activity.