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.

Auditory brainstem response (ABR) measurements are often used to assess hearing in marine mammals, especially when time and access for behavioral conditioning is limited, e.g., wild animals tested while stranded or rehabilitating or during capture-and-release efforts (e.g., Ridgway and Carder, 2001; Nachtigall et al., 2005; Cook et al., 2006; Mulsow et al., 2011b; Ruser et al., 2014; Ruser et al., 2016; Houser et al., 2018; Mooney et al., 2018). Although ABRs can be measured relatively easily in many marine mammal species, some species (e.g., orcas, Orcinus orca) are difficult to test, presumably because their small brain/body mass ratios result in low ABR signal-to-noise ratios (SNRs) when measured with surface electrodes (Szymanski et al., 1998; Lucke et al., 2016; Houser et al., 2019). Similar constraints are anticipated with baleen whales, where brain/body mass ratios are also comparatively small (Ridgway and Tarpley, 1996). For these situations, there is interest in understanding how stimulus characteristics might be manipulated to increase ABR SNR.

The amplitude of an ABR is affected not only by the number of neural elements that are activated, but also by the extent to which those elements fire synchronously. Clicks produce large ABRs not only because they are broadband (and thus stimulate a large number of neurons), but also because their short duration means the neural elements are activated closely in time. However, even for short-duration stimuli such as clicks, dispersion in the cochlea results in progressively increasing time delays between activation of high-frequency neural elements in the base and lower-frequency elements toward the apex (Teas et al., 1962). This can lead to neural responses that are out-of-phase, decreasing the amplitude of the farfield ABR and biasing broadband ABRs to reflect activity from primarily basal, high-frequency regions (Dau et al., 2000).

The effects of cochlear dispersion can be counteracted in two ways, referred to as input compensation and output compensation (Don et al., 2009). Input compensation is accomplished by using sound stimuli consisting of upward frequency sweeps, or “chirps” (Shore and Nuttall, 1985). In an upward chirp, lower-frequency stimulus components are presented before higher-frequency components since they need more time to travel to their respective sites of maximal activation in the cochlea. Input compensation of the ABR using chirp stimuli has been demonstrated in humans (e.g., Dau et al., 2000; Elberling and Don, 2008; Don et al., 2009; Elberling and Don, 2010), rats (Rattus norvegicus; Spankovich et al., 2008), bottlenose dolphins (Tursiops truncatus; Finneran et al., 2017b), and orcas (Houser et al., 2019).

In output compensation (Don et al., 1994), the broadband ABR is first decomposed into derived-band (cochlear place-specific) ABRs using the high-pass subtractive masking technique (Teas et al., 1962; Don and Eggermont, 1978; Parker and Thornton, 1978c; Finneran et al., 2016). First, ABRs are measured in the presence of a broadband stimulus presented with simultaneous masking noise. Over successive measurements, the masker high-pass cutoff frequency is varied across the ABR stimulus bandwidth. Derived-band ABRs are obtained by subtracting pairs of ABRs obtained with maskers with successive high-pass cutoffs. Derived-band ABRs are then temporally aligned, based on their individual peak latencies, and summed to produce the “stacked ABR” (Don et al., 1994; Don et al., 2009). The stacked ABR was developed to sensitize human ABR wave V amplitude measures to detect small vestibular schwannomas (Don et al., 1997; Don et al., 2005), following the observation that the variation in response times in the cochlea is a major contributor to the variability observed in ABR amplitude measures (Don et al., 1994). By temporally aligning and “stacking” the ABRs, ABR phase shifts arising from cochlear dispersion are avoided, and wave V amplitude increases compared to the unmasked ABR with an increase in the number of bands summed (Don et al., 1997; Don et al., 2005). Unlike chirp derivation, the stacked ABR does not rely upon a model of the cochlear traveling wave. The stacked ABR also has value because it represents the maximum ABR peak amplitude that may be obtained by compensating for cochlear dispersion since each derived-band ABR is adjusted using the peak latency actually measured for that individual (Don et al., 2009). Finally, comparisons between unmasked and stacked ABRs are based on the same stimulus and thus are not confounded by differences in stimulus duration as are comparisons between chirp- and click-evoked ABRs (see Finneran et al., 2017b). However, obtaining the stacked ABR is time-consuming since multiple ABR measurements are required to obtain the derived-band ABRs.

The main goal of the present study was to examine the effects of output compensation using the stacked ABR technique in dolphins and sea lions. Since this requires latencies for derived-band ABRs, a secondary goal was to use those latency measures to estimate and compare cochlear traveling-wave speed (TWS) in dolphins and sea lions. Sea lions are amphibious marine mammals whose ear and auditory system characteristics most resemble those of typical terrestrial mammals. In contrast, dolphins are fully aquatic mammals with a highly adapted ear and auditory system specialized for high-frequency (up to ∼150 kHz) underwater hearing and echolocation (Nummela, 2008). Given the anatomical, physiological, and ecological differences between the species, differences in cochlear mechanics and the effectiveness of output compensation might be expected. Cochlear TWS estimates in dolphins have been previously reported by Popov and Supin (2001), who used narrowband click stimuli without masking noise. The main limitation of this approach, as with tone bursts that vary in frequency, is that excitation may spread into adjacent frequency bands along the cochlear partition, especially higher-frequency bands. Finneran et al. (2016) also estimated cochlear TWS in five dolphins, but used broadband click stimuli with the high-pass subtractive noise method. The results of the two studies were similar, with cochlear TWS varying from ∼3–4 oct/ms in the apex to ∼20–30 oct/ms in the base. Cochlear TWS has not been measured in sea lions (or any other marine mammal besides dolphins). Stacked ABRs or the effects of output compensation have also not been described in any non-human mammal.

The high-pass subtractive masking technique has been previously utilized in studies with humans (e.g., Don and Eggermont, 1978; Parker and Thornton, 1978a,b,c,d; Don et al., 1979; Eggermont and Don, 1980; Burkard and Hecox, 1983; Hecox and Deegan, 1983; Burkard and Hecox, 1987; Donaldson and Ruth, 1993, 1996; Don et al., 1998), gerbils (Burkard and Voigt, 1989), guinea pigs (Teas et al., 1962), and dolphins (Finneran et al., 2016; Finneran et al., 2017a; Mulsow et al., 2021). While most studies have used the ABR to derive narrowband (cochlear place-specific) responses, some studies have used the compound action potential (Teas et al., 1962), the cochlear microphonic (Ponton et al., 1992), or the auditory steady-state response (Herdman et al., 2002). The method assumes that high-pass masking represents complete (or near complete) energetic masking of the cochlear regions basal (i.e., higher in frequency) to the masker cutoff frequency but does not allow substantial energetic masking in cochlear regions more apical (i.e., lower in frequency) to the masker cutoff. It is well demonstrated, perceptually, biomechanically, and electrophysiologically, that the spread of the traveling wave to more basal regions (for any stimulus) is far greater than the spread to more apical regions. This of course does not mean there is absolutely no spread of excitation (i.e., masking) apically, just that is it far smaller in magnitude than the spread seen basally. In support of this view, high-pass masking studies in numerous species have consistently shown an increase in ABR peak latency with decreasing derived-band frequency, thus demonstrating the frequency to cochlear place representation originally visually observed in the cochlea by von Békésy (1960).

The study followed a protocol approved by the Institutional Animal Care and Use Committee at the Naval Information Warfare Center Pacific and the Navy Bureau of Medicine and Surgery and followed all applicable United States Department of Defense guidelines. Subjects consisted of five Atlantic bottlenose dolphins (T. truncatus, codes: SHA, SPA, SPO, TRO, WHP) and two California sea lions (Zalophus californianus, codes: RMO, TPO). Four of the dolphins were considered to be “normal-hearing” animals, and one (SPA) was “hearing-impaired,” based on their upper-frequency limit of hearing [see Table I and Strahan et al. (2020)]. Both sea lions were believed to have normal hearing, based on previous psychophysical threshold testing with TPO (Mulsow et al., 2015) and amplitudes and morphologies of broadband noiseburst-evoked ABRs measured in both sea lions (present study) compared to broadband click-evoked ABRs measured in normal-hearing and hearing-impaired sea lions (Mulsow et al., 2014).

TABLE I.

Five dolphins and two sea lions participated in the experiments. For dolphins, the upper-frequency limit (UFL) was defined as the frequency where auditory steady-state response thresholds to amplitude modulated tones reached 120 dB re 1 μPa (Strahan et al., 2020). Dolphins with UFL ≤ 120 kHz were considered “hearing-impaired” (HI); those with UFL ≥ 120 kHz were considered “normal-hearing” (NH).

Subject IDSpeciesSexAge (years)UFL (kHz)Group
SHA Dolphin Female 39 142 NH 
SPA Dolphin Male 31 100 HI 
SPO Dolphin Male 147 NH 
TRO Dolphin Male 27 144 NH 
WHP Dolphin Male 15 143 NH 
RMO Sea lion Male ∼30 kHz NH 
TPO Sea lion Male 10 ∼30 kHz NH 
Subject IDSpeciesSexAge (years)UFL (kHz)Group
SHA Dolphin Female 39 142 NH 
SPA Dolphin Male 31 100 HI 
SPO Dolphin Male 147 NH 
TRO Dolphin Male 27 144 NH 
WHP Dolphin Male 15 143 NH 
RMO Sea lion Male ∼30 kHz NH 
TPO Sea lion Male 10 ∼30 kHz NH 

Dolphins were tested underwater, in a 9 m × 9 m floating, netted enclosure at the United States Navy Marine Mammal Program facility in San Diego Bay, California. During each trial, the dolphin positioned itself on an underwater “biteplate” attached to an aluminum frame at 1-m depth. Two piezoelectric, underwater sound projectors [LL916 (Lubell Labs, Columbus, OH) and ITC 1042 (International Transducer Corp., Santa Barbara, CA)] were located approximately 1 m from the biteplate, with the dolphin facing the transducers when positioned on the biteplate. The ITC 1042 was located at the center of the front face of the LL916. Underwater ambient noise at the test site was dominated by snapping shrimp, other dolphins, and passing vessels and aircraft. Typical median ambient noise pressure spectral density levels were ∼78 dB re 1 μPa2/Hz at 2.5 kHz and decreased linearly with the logarithm of frequency to ∼55 dB re 1 μPa2/Hz at 150 kHz.

Sea lions were tested in air while under general anesthesia in a veterinary clinic. Midazolam (0.3 mg/kg) and meperidine (1 mg/kg) were administered prior to intubation with sevoflurane gas (1.8%–2%). Ephedrine (0.05 mg/kg), dobutamine (0.1–0.2 μg/kg/min), and lithium chloride (0.01 mmol/kg) were intermittently administered during ABR recordings as directed by the attending veterinarian. Animals were positioned in ventral recumbence, and sounds were delivered to both ears via headphones (HDA300, Sennheiser Electronic, Wedemark, Germany). Typical ambient noise levels in the veterinary clinic setting were described by Mulsow et al. (2011a).

ABR stimuli consisted of broadband noisebursts. Noisebursts were used, rather than more traditional clicks, to allow better control of spectral and temporal characteristics when applying digital frequency compensation (see below). Noisebursts were created by multiplying continuous noise by an envelope function consisting of a linear rise, constant amplitude plateau, and linear fall. A separate, uncorrelated sequence of continuous noise was used as the masker. The two electronic signals were added together (SM5, Tucker-Davis Technologies, Alachua, FL) and used to simultaneously drive the two underwater sound projectors (dolphins) or headphones (sea lions). Both the noiseburst and masker were digitally compensated for the sound projector/headphone frequency response and multipath effects (underwater only) to obtain spectrally pink noise (see Au and Floyd, 1979; Finneran et al., 2018). Table II lists the noiseburst and masker frequency ranges and SPLs utilized with each animal. Representative examples of sound stimuli are shown in Fig. 1.

TABLE II.

Frequencies and sound pressure levels (SPLs) for the noiseburst and masker signals. Noiseburst 1/3-oct SPLs were calculated using 2-ms windows for frequency analysis. SPLs have units of dB re 1 μPa for dolphins (underwater) and 20 μPa for sea lions (in air).

NoiseburstMaskerSpeciesAnimal codes
Bandwidth (kHz)1/3-oct SPLPlateau SPLHP cutoffs (kHz)LP cutoff (kHz)1/3-oct SPL
1–152 95 115 1, 1.4, 2, 2.8, 4, 5.7, 8, 11, 16, 23, 32, 45, 64, 90, 128 152 110 Dolphin SHA, SPO, TRO, WHP 
4–152 105 125 4, 5.7, 8, 11, 16, 23, 32, 45, 64, 90, 128 152 120 Dolphin SHA, SPA, SPO, TRO 
0.5–32 53 65 0.5, 0.7, 1, 1.4, 2, 2.8, 4, 5.7, 8, 11, 16, 23 32 72 Sea lion RMO, TPO 
NoiseburstMaskerSpeciesAnimal codes
Bandwidth (kHz)1/3-oct SPLPlateau SPLHP cutoffs (kHz)LP cutoff (kHz)1/3-oct SPL
1–152 95 115 1, 1.4, 2, 2.8, 4, 5.7, 8, 11, 16, 23, 32, 45, 64, 90, 128 152 110 Dolphin SHA, SPO, TRO, WHP 
4–152 105 125 4, 5.7, 8, 11, 16, 23, 32, 45, 64, 90, 128 152 120 Dolphin SHA, SPA, SPO, TRO 
0.5–32 53 65 0.5, 0.7, 1, 1.4, 2, 2.8, 4, 5.7, 8, 11, 16, 23 32 72 Sea lion RMO, TPO 
TABLE III.

Best-fit values for the parameter k and goodness of fit (R2) resulting from nonlinear regression fits of Eq. (1) to the derived-band ABR peak latency versus derived-band upper-frequency data.

DolphinsSea lions
Subject IDkR2Subject IDkR2
SHA 6.6 0.974 RMO 3.5 0.954 
SPA 6.4 0.964 TPO 2.6 0.954 
SPO 5.7 0.974 Mean 3.4 0.979 
TRO 6.3 0.961    
WHP 8.0 0.969    
Mean 6.4 0.988    
DolphinsSea lions
Subject IDkR2Subject IDkR2
SHA 6.6 0.974 RMO 3.5 0.954 
SPA 6.4 0.964 TPO 2.6 0.954 
SPO 5.7 0.974 Mean 3.4 0.979 
TRO 6.3 0.961    
WHP 8.0 0.969    
Mean 6.4 0.988    
FIG. 1.

Representative acoustic stimulus characteristics for dolphins [(a) and (c)] and sea lions [(b) and (d)]. (a) and (b) show noiseburst 1/3-oct spectrum and temporal envelope (inset) for dolphins and sea lions, respectively. (c) and (d) show masker 1/3-oct spectra for dolphins and sea lions, respectively. The numbers near each trace indicate the noise high-pass cutoff frequency. Ambient noise peaks from 0.5 to 1.4 kHz in (d) reflect airborne ambient noise. Noiseburst and high-pass noise 1/3-oct calibration signal levels were 120 and 110 dB re 1 μPa, respectively, for dolphins and 78 and 74 dB re 20 μPa, respectively, for sea lions. Some overshoot of the dolphin noiseburst envelope was apparent at stimulus offset; however, the amount was small (∼20%, or 1.7 dB).

FIG. 1.

Representative acoustic stimulus characteristics for dolphins [(a) and (c)] and sea lions [(b) and (d)]. (a) and (b) show noiseburst 1/3-oct spectrum and temporal envelope (inset) for dolphins and sea lions, respectively. (c) and (d) show masker 1/3-oct spectra for dolphins and sea lions, respectively. The numbers near each trace indicate the noise high-pass cutoff frequency. Ambient noise peaks from 0.5 to 1.4 kHz in (d) reflect airborne ambient noise. Noiseburst and high-pass noise 1/3-oct calibration signal levels were 120 and 110 dB re 1 μPa, respectively, for dolphins and 78 and 74 dB re 20 μPa, respectively, for sea lions. Some overshoot of the dolphin noiseburst envelope was apparent at stimulus offset; however, the amount was small (∼20%, or 1.7 dB).

Close modal

For dolphins, noiseburst generation was identical to that described by Finneran et al. (2020). Continuous noise was generated at 500 kHz and 16-bit resolution using an NI PXIe-6368 data acquisition device (National Instruments, Austin, TX) and then enveloped using custom software on an NI PXI-7852R device (National Instruments) containing a Virtex-5 LX50 field-programmable gate array (FPGA) (Xilinx, San Jose, CA). Noiseburst total duration was 250 μs, which included 32-μs linear rise/fall envelopes. Analog noisebursts were filtered (0.2–200 kHz, eight-pole Butterworth, 3C module, Krohn-Hite Corporation, Brockton, MA), attenuated (PA5, Tucker-Davis Technologies), and input to the SM5 signal mixer. Noisebursts were presented at a rate of ∼20 s−1. Masking noise was generated at 500 kHz and 16-bit using an NI PXIe-6361 device (National Instruments). Analog masking noise was filtered (0.2–200 kHz, eight-pole Butterworth, 3C module, Krohn-Hite Corporation), attenuated (PA5, Tucker-Davis Technologies), and input to the SM5 mixer. The mixer output was amplified (Crest Audio CC4000 or Peavey PVi4B, Peavey Electronics Corporation, Meridian, MS) and used to drive the sound projectors. Stimuli were calibrated using a miniature hydrophone (TC4013, Reson, Slangerup, Denmark) placed at the “listening position,” estimated as the midpoint between the posterior region of the dolphin's mandible when on the biteplate, without the dolphin present.

For sea lions, noisebursts were generated at 500 kHz sampling rate and 16-bit resolution using an NI USB-6259 data acquisition device (National Instruments). Noiseburst total duration was 1.256 ms, which included 128-μs linear rise/fall envelopes. Analog noisebursts were low-pass filtered (120 kHz, FT5, Tucker-Davis Technologies), attenuated (PA4, Tucker-Davis Technologies), and input to an SM5 mixer. Noisebursts were presented at a rate of ∼20 s−1. Masking noise was generated at 500 kHz sampling rate and 16-bit using an NI PCI-6251 device (National Instruments). Analog masking noise was low-pass filtered (200 kHz, eight-pole Butterworth, 3C module, Krohn-Hite Corporation), attenuated (PA5, Tucker-Davis Technologies), and input to the SM5 mixer. The mixer output was amplified (HB5, Tucker-Davis Technologies) and used to drive the HDA300 headphones. Noisebursts and masking noise were equalized and calibrated using a probe microphone (ER7C, Etymotic Research, Elk Grove Village, IL) located under one of the earphones while not on the sea lion. The signals were low-pass filtered at 150 kHz (FT5, Tucker-Davis Technologies) prior to analog/digital (A/D) conversion at 500 kHz and 16 bit. Amplitude corrections were made for the probe microphone frequency response.

Dolphin ABRs were measured using three gold-cup surface electrodes embedded in suction cups. The non-inverting electrode was located on the midline, approximately 5 cm posterior to the blowhole, and the inverting electrode was located near the right external auditory meatus. A third, common electrode was located in the seawater near the dolphin. Sea lion ABR measurements utilized 14 mm × 0.38 mm stainless steel subdermal needle electrodes (Natus Neurology, Pleasanton, CA): a non-inverting electrode midway between the ears on the dorsal midline, an inverting electrode on the dorsal midline just posterior to the nape of the neck and near the scapula, and a common electrode placed near the left shoulder.

Electrode signals were filtered (dolphin: 0.3–3 kHz, sea lion: 0.03–3 kHz) and amplified (94 dB) using a biopotential amplifier (ICP511, Grass Technologies, West Warwick, RI). The differential voltage between the inverting and non-inverting electrodes, representing the instantaneous electroencephalogram (EEG), was digitized at 100 kHz with 16-bit resolution using the NI PXIe-6368 (dolphins) or NI USB-6259 (sea lions). The instantaneous EEG was recorded over a total of 4096 noiseburst presentations for each subject, noiseburst SPL, and masker combination, collected over 2–8 individual measurements (depending on subject).

ABRs were obtained by first filtering the EEG data (dolphins: bandpass 0.3–3 kHz, sea lions: low pass at 2.5 kHz) using a zero-phase implementation of a digital Butterworth filter. Epochs of EEG data, each 20 ms in duration and temporally aligned with the onset of a noiseburst presentation, were then synchronously averaged to produce a single averaged ABR (based on a total of 4096 epochs) for each condition as well as two “subaverages,” each based on 2048 sequential epochs.

Derived-band ABRs were obtained by subtracting pairs of ABRs obtained with different masker high-pass cutoff frequencies (Teas et al., 1962; Don and Eggermont, 1978). For dolphins, masker high-pass cutoff frequencies were separated by 1/2 octave (oct). For sea lions, SNRs were relatively low in RMO; thus, the masker cutoff separation was 1 oct for both individuals. Peaks P1, N2, P4, and N5 were then visually identified (consensus of all authors) in the narrowband ABRs (see Popov and Supin, 1990), and the latencies of P1, P4, and N5 were determined. For bifid P1 waves, latencies were based on the positive peak closest to the P1-N2 zero crossing. Latencies were corrected by subtracting the time of arrival measured at the listening position for an acoustic click projected from the same apparatus.

Effects of cochlear dispersion were described by fitting derived-band ABR peak latencies with the function

τ(f)=τ0+k/f,
(1)

where τ is latency (in ms), f is the upper frequency of the derived band (in kHz), and k and τ0 are fitting parameters. Equation (1) is a special case of the power function τ(f)=τ0+kfd, with the parameter d = 1 (see Finneran et al., 2016; Finneran et al., 2017a). The definition of the parameter f as the upper band frequency assumes that the contributions from the more basal portions of each derived band most strongly influence the derived-band ABR. Equation (1) was first fitted to the P4 and N5 data for each animal. Fits to the data for all available SPLs were done simultaneously, using a shared value for the parameter k. The resulting best-fit value for k was then held constant, and Eq. (1) was fitted to the P1 latencies when available (i.e., only τ0 adjusted when fitting P1). This procedure was used because of the low SNR typically found in ABR peak P1. Cochlear TWS was estimated as the inverse of the rate of change of latency with frequency (Popov and Supin, 2001),

v(f)=(dτ/df)1=fkln2,
(2)

where v is the TWS (in oct/ms).

To obtain the stacked ABR for an individual, the relative latency of each frequency band was defined as the difference between the derived-band ABR N5 peak latency and the N5 peak latency for the derived-band ABR with the largest N5 peak amplitude (i.e., the latency of the derived-band ABR contributing most to the broadband ABR was used as a reference latency). If the N5 peak was not visible, the relative latency was set to zero for that frequency band. Stacked ABRs were obtained by shifting each derived-band ABR by the relative latency for that frequency band and then summing the time-shifted ABRs (Don et al., 2009).

Figure 2 shows examples of unmasked and masked ABRs for a dolphin (SPO) and sea lion (TPO). Derived-band ABRs for these same animals are shown in Fig. 3, with the masking noise condition associated with each ABR indicated by each trace. Note that the sea lion derived bands are 1 oct in width but are spaced at 1/2-oct intervals (i.e., they overlap). Also, note that high-pass or derived-band ABRs can be seen down to 1–2 kHz in sea lions but only down to 8–11 kHz in bottlenose dolphins.

FIG. 2.

Example broadband noiseburst ABRs measured for the dolphin SPO (left) and sea lion TPO (right) unmasked and in the presence of masking noise with various high-pass cutoff frequencies (denoted with each series). The thick line shows the averaged ABR based on 4096 sweeps; the shading shows two subaverages, each with 2048 sweeps, overlaid. The ABR peaks P1, N2, P4, and N5 are indicated for the unmasked noiseburst ABR.

FIG. 2.

Example broadband noiseburst ABRs measured for the dolphin SPO (left) and sea lion TPO (right) unmasked and in the presence of masking noise with various high-pass cutoff frequencies (denoted with each series). The thick line shows the averaged ABR based on 4096 sweeps; the shading shows two subaverages, each with 2048 sweeps, overlaid. The ABR peaks P1, N2, P4, and N5 are indicated for the unmasked noiseburst ABR.

Close modal
FIG. 3.

Derived-band ABRs for the dolphin SPO (left) and sea lion TPO (right) obtained by subtracting ABRs measured with combinations of high-pass noise. The text near each trace indicates the bandwidth for the derived-band ABR, e.g., the trace for SPO labeled 1–1.4 kHz represents the difference between ABRs measured with high-pass noise cutoffs of 1 and 1.4 kHz. The highest-cutoff frequency (152 and 32 kHz for dolphins and sea lions, respectively) was obtained using the unmasked ABR as the minuend. The thick line shows the averaged ABR based on 4096 sweeps; the shading shows two subaverages, each with 2048 sweeps, overlaid. Note the sea lion derived bands are 1 oct wide, while the dolphin bandwidths are 1/2 oct wide, except the highest dolphin derived band, 128–152 kHz, which is only 1/4 oct wide.

FIG. 3.

Derived-band ABRs for the dolphin SPO (left) and sea lion TPO (right) obtained by subtracting ABRs measured with combinations of high-pass noise. The text near each trace indicates the bandwidth for the derived-band ABR, e.g., the trace for SPO labeled 1–1.4 kHz represents the difference between ABRs measured with high-pass noise cutoffs of 1 and 1.4 kHz. The highest-cutoff frequency (152 and 32 kHz for dolphins and sea lions, respectively) was obtained using the unmasked ABR as the minuend. The thick line shows the averaged ABR based on 4096 sweeps; the shading shows two subaverages, each with 2048 sweeps, overlaid. Note the sea lion derived bands are 1 oct wide, while the dolphin bandwidths are 1/2 oct wide, except the highest dolphin derived band, 128–152 kHz, which is only 1/4 oct wide.

Close modal

Figure 4 shows derived-band ABR peak latencies for P1, P4, and N5 for each dolphin as well as the mean latencies across the five dolphins in the lower right panel. For SPA and WHP, recordings were only made at one noiseburst level, while both SPLs (115 and 125 dB re 1 μPa) were used for SHA, SPO, and TRO. Latency data for SPA were limited to ≤ 90 kHz because SPA had a high-frequency hearing loss, with an upper cutoff of hearing ∼100 kHz (see Table I). The remaining, normal-hearing dolphins had visible derived-band responses for the 90–128 kHz and 128–152 kHz bands. Derived-band ABRs and thus P1, P4, and N5 were not observed below 8 or 11 kHz, depending on the dolphin. Relative changes in ABR peak latency with frequency were larger for frequency bands with upper cutoffs below ∼32 kHz, which matches previous results for dolphins (Finneran et al., 2016).

FIG. 4.

Derived-band ABR peak latencies for dolphins as functions of the derived band upper frequency. The panel labeled “Mean” shows averaged latencies [and standard deviations (SDs)] for frequencies with n ≥ 2 data points. Symbols are only displayed for visually identifiable peaks in the averaged ABR. The stars indicate the unmasked ABR latencies. The solid and dashed lines show the best fit of Eq. (1) to the 115 and 125 dB re 1 μPa data points, respectively. Best-fit values for the parameter k are listed in Table III.

FIG. 4.

Derived-band ABR peak latencies for dolphins as functions of the derived band upper frequency. The panel labeled “Mean” shows averaged latencies [and standard deviations (SDs)] for frequencies with n ≥ 2 data points. Symbols are only displayed for visually identifiable peaks in the averaged ABR. The stars indicate the unmasked ABR latencies. The solid and dashed lines show the best fit of Eq. (1) to the 115 and 125 dB re 1 μPa data points, respectively. Best-fit values for the parameter k are listed in Table III.

Close modal

Figure 5 shows sea lion derived-band latencies for P1, P4, and N5. P1 was consistently seen only in one sea lion (TPO), and derived-band responses below ∼4 kHz are only observed for P4 and N5 in TPO. The mean data are shown in the right-most panel. Lines indicate best fits of Eq. (1), with shared parameter k.

FIG. 5.

Derived-band ABR peak latencies for sea lions as functions of the derived-band upper frequency. The panel labeled “Mean” shows averaged latencies (and SDs) for frequencies with n = 2 data points. Symbols are only displayed for visually identifiable peaks in the averaged ABR. The stars indicate the unmasked ABR latencies. Noiseburst 1/3-oct SPL was 65 dB re 20 μPa. The lines show the best fit of Eq. (1) to the data points. Best-fit values for the parameter k are listed in Table III.

FIG. 5.

Derived-band ABR peak latencies for sea lions as functions of the derived-band upper frequency. The panel labeled “Mean” shows averaged latencies (and SDs) for frequencies with n = 2 data points. Symbols are only displayed for visually identifiable peaks in the averaged ABR. The stars indicate the unmasked ABR latencies. Noiseburst 1/3-oct SPL was 65 dB re 20 μPa. The lines show the best fit of Eq. (1) to the data points. Best-fit values for the parameter k are listed in Table III.

Close modal

Figure 6(a) compares mean peak delays for dolphins (open circles) and sea lions (filled circles), defined as the peak latency minus the best-fit value of τ0 in Eq. (1). Figure 6(b) shows the cochlear TWS estimates, derived from Eq. (2) using k values from the best fits of Eq. (1) to the mean latency data. Cochlear TWSs for the sea lions and dolphins from 8 to 32 kHz were similar (∼2–8 oct/ms for dolphins; ∼3.5–11 oct/ms for sea lions). For dolphins, the TWSs above 32 kHz continue to increase up to ∼30 oct/ms.

FIG. 6.

(a) Comparison of mean derived-band ABR peak delays for dolphins and sea lions as functions of the derived band upper frequency for conditions with n ≥ 2 data points. Peak delay is defined as the peak latency relative to the best-fit value of τ0 from Eq. (1). Symbols indicate mean values; error bars represent the SD. The lines are obtained from Eq. (1), with k from Table III and τ0 = 0. (b) Cochlear traveling wave speeds for dolphins and sea lions derived with Eq. (2) and the best-fit values of the parameter k (Table III).

FIG. 6.

(a) Comparison of mean derived-band ABR peak delays for dolphins and sea lions as functions of the derived band upper frequency for conditions with n ≥ 2 data points. Peak delay is defined as the peak latency relative to the best-fit value of τ0 from Eq. (1). Symbols indicate mean values; error bars represent the SD. The lines are obtained from Eq. (1), with k from Table III and τ0 = 0. (b) Cochlear traveling wave speeds for dolphins and sea lions derived with Eq. (2) and the best-fit values of the parameter k (Table III).

Close modal

Figure 7 illustrates the stacked ABR derivation by replotting the data in Fig. 3 with the ABRs temporally aligned using the approach specified in Sec. II D. The dotted lines show the original derived-band ABRs, which exhibit cochlear dispersion (i.e., increasing traveling-wave delay with decreasing derived-band frequency), while the solid lines show the temporally adjusted waveforms, (i.e., the output compensated ABRs) that serve as the basis for the stacked ABR approach (e.g., Don et al., 1997; Don et al., 2005; Don and Kwong, 2009).

FIG. 7.

Examples of temporally aligned derived-band ABR waveforms for a dolphin (SPO, left column) and sea lion (TPO, right column). The dotted lines show the original derived-band ABRs, and the solid lines show the temporally aligned ABRs. The vertical shaded line indicates the N5 latency for the frequency band with the largest N5 peak amplitude.

FIG. 7.

Examples of temporally aligned derived-band ABR waveforms for a dolphin (SPO, left column) and sea lion (TPO, right column). The dotted lines show the original derived-band ABRs, and the solid lines show the temporally aligned ABRs. The vertical shaded line indicates the N5 latency for the frequency band with the largest N5 peak amplitude.

Close modal

Figure 8 superimposes the stacked ABR (solid line) and the unmasked, broadband ABR (dotted line) for dolphins and sea lions. The ABR peak amplitudes for the stacked and unmasked ABRs are shown in Table IV. In all cases, P1-N2 and P4-N5 amplitudes for the stacked ABR were larger than the unmasked ABR. In dolphins, using mean data across animals, the amplitude increase was greater for the higher stimulus level, and P4-N5 increase was greater than P1-N2 increase. In sea lions, P1-N2 amplitude increase was greater than the P4-N5 increase for the stacked versus the unmasked ABR. Overall, the proportional amplitude increase for the stacked versus the unmasked ABR was greater for sea lions than dolphins.

FIG. 8.

Comparison of stacked ABR waveforms (solid lines) with unmasked, broadband ABRs (dotted lines) for individual dolphins and sea lions. Noiseburst plateau SPLs were 115 and 125 dB re 1 μPa for dolphins and 65 dB re 20 μPa for sea lions.

FIG. 8.

Comparison of stacked ABR waveforms (solid lines) with unmasked, broadband ABRs (dotted lines) for individual dolphins and sea lions. Noiseburst plateau SPLs were 115 and 125 dB re 1 μPa for dolphins and 65 dB re 20 μPa for sea lions.

Close modal
TABLE IV.

Comparison of stacked ABR and unmasked, broadband ABR peak amplitudes for P1-N2 and P4-N5.

SubjectSPL (dB re 1 μPa)P1-N2 ampP4-N5 amp
Stacked (μV)Unmasked (μV)Increase (%)Stacked (μV)Unmasked (μV)Increase (%)
SHA 115 1.2 1.1 11 2.1 1.8 20 
SPO 115 1.0 0.71 41 3.0 2.2 40 
TRO 115 0.84 0.81 2.3 1.6 42 
WHP 115 1.3 1.1 23 2.3 1.7 35 
   Mean 20  Mean 34 
SHA 125 1.9 1.3 43 2.8 1.8 53 
SPA 125 1.7 1.2 41 1.7 0.94 84 
SPO 125 1.6 1.4 13 5.3 3.3 63 
TRO 125 1.4 1.1 24 2.8 2.2 28 
   Mean 30  Mean 57 
RMO 65 0.31 0.12 151 1.0 0.63 57 
TPO 65 0.56 0.30 87 3.5 2.0 71 
   Mean 119  Mean 64 
SubjectSPL (dB re 1 μPa)P1-N2 ampP4-N5 amp
Stacked (μV)Unmasked (μV)Increase (%)Stacked (μV)Unmasked (μV)Increase (%)
SHA 115 1.2 1.1 11 2.1 1.8 20 
SPO 115 1.0 0.71 41 3.0 2.2 40 
TRO 115 0.84 0.81 2.3 1.6 42 
WHP 115 1.3 1.1 23 2.3 1.7 35 
   Mean 20  Mean 34 
SHA 125 1.9 1.3 43 2.8 1.8 53 
SPA 125 1.7 1.2 41 1.7 0.94 84 
SPO 125 1.6 1.4 13 5.3 3.3 63 
TRO 125 1.4 1.1 24 2.8 2.2 28 
   Mean 30  Mean 57 
RMO 65 0.31 0.12 151 1.0 0.63 57 
TPO 65 0.56 0.30 87 3.5 2.0 71 
   Mean 119  Mean 64 

The present derived-band results with dolphins are consistent with previous data with spectrally pink stimuli and maskers that showed little contribution to the ABR from frequency bands <10 kHz, cochlear TWS decreasing from ∼25 oct/ms at 113 kHz to ∼3 oct/ms at 14 kHz, and a best-fit value of k from Eq. (1) of 6.4 (Finneran et al., 2016). Dolphin cochlear TWSs in the present study are also similar to those estimated by Popov and Supin (2001) using narrowband click stimuli (without high-pass noise): TWS decreased from 32 oct/ms at 108 kHz to 4 oct/ms at ∼14 kHz. Derived-band ABRs and cochlear TWSs have not been previously measured in sea lions. In the present study, sea lion derived-band ABRs were qualitatively similar to those from dolphins, e.g., derived-band amplitude increased and latency decreased with increasing derived-band frequency; however, sea lion P4 and N5 latencies were substantially longer than those from dolphins. It is also important to note the different frequency ranges that contribute to the broadband ABR: >8–11 kHz in dolphins, but >1–2 kHz for sea lions, i.e., the broadband ABR primarily reflects contributions from the basal region of the cochlea in both cases, but the specific corresponding frequencies vary by species.

Cochlear TWSs were similar for sea lions and dolphins for frequencies from 8 to 32 kHz (∼2–8 oct/ms for dolphins; ∼3.5–11 oct/ms for sea lions), which extends up to the normal upper limit of sea lion hearing. However, dolphin TWS for higher frequencies, which are used in echolocation, increases up ∼30 oct/ms. For humans, cochlear TWSs estimated from derived-band latencies range from approximately 0.3–0.7 oct/ms for frequencies below 2 kHz up to ∼1.3–2.5 oct/ms above 2 kHz (Don and Eggermont, 1978; Hecox and Deegan, 1983). In gerbils, estimated TWS was ∼3.0 oct/ms from 4 to 16 kHz (Burkard and Voigt, 1989). Although comparisons across studies should be treated with caution because of differences in stimulus and masker conditions, cochlear TWSs between ∼2 and 32 kHz appear similar across species, while TWSs for humans below 2 kHz are lower, and those for dolphins >32 kHz are higher. It therefore appears that TWS is largely determined by the frequency band of interest with high-frequency/low-frequency variations across species likely due to specializations in the cochlear morphology, i.e., basilar membrane stiffness and mass. At frequencies extending up to the lower range of echolocation frequencies (∼20–30 kHz), the dolphin cochlea appears to behave similarly to the amphibious sea lions and terrestrial mammals, but at higher frequencies—the primary echolocation frequencies, which are mapped to the base of the cochlea—the cochlear TWS is much higher. High TWS in the base of the dolphin cochlea is consistent with anatomical features reported for dolphins (as well as other echolocators) that increase basilar membrane stiffness, e.g., very small basilar membrane width, increased thickness, and presence of an external osseous spiral lamina that supports the basilar membrane within the base of the cochlea (Wever et al., 1971; Ketten, 2000; Ketten et al., 2021).

It is well known that the ABR strongly depends on the acoustic stimulus used to elicit the response (e.g., the stimulus envelope, spectrum, and level) as well as the high-pass masking noise used to limit cochlear place. In the present investigation, we used a pink noiseburst stimulus (fixed in level) and pink masking noise (fixed in level but varied in bandwidth) for a given derived-band series in a specific animal. An investigation of the effects of spectrally white click stimulus level (and pink noise level) on derived-band ABRs in humans showed that ABR peak amplitude across derived-band frequency patterns differed across ABR peak (wave I, III, V) and click level but that the change in ABR peak latency across derived-band frequency varied little across ABR peak and click level (Eggermont and Don, 1980). These results suggest that cochlear travel time estimates do not strongly depend on the specific ABR peak investigated. Don et al. (1998) assessed cochlear travel time using the derived-band technique in normal-hearing and hearing-impaired human subjects. They concluded that cochlear latency depends on cochlear transport time, cochlear filter buildup time, the synaptic delay from inner hair cells to auditory nerve fibers, and nerve conduction velocity (including synaptic delays) to the generator of a given ABR peak. In humans at least, ABR peak latencies are affected by sex, while cochlear hearing loss appears to affect cochlear filter buildup time, but likely has little effect on synaptic delay or neural conduction times. For the purposes of the present study, where a broadband stimulus (pink noiseburst) was used, it would appear that any hearing loss would have affected the latency of the derived bands from that frequency region, due to changes in cochlear filter buildup time. While we believe such effects would likely have been modest, it is not practicable for us to quantify such possible effects in the present investigation. Since ABR peak latency is affected by stimulus level, the use of a different stimulus in the present investigation (e.g., a white noiseburst) could affect the ABR peak latency across derived-band frequency (due to within-band changes in cochlear filter buildup time) and therefore would have affected the TWS estimates. This is specifically why we chose to use spectrally pink noisebursts and pink high-pass masking noise for both species.

In the present study, stacked ABRs in both dolphins and sea lions were larger than unmasked ABRs, as has been observed in humans (Don et al., 1997; Don et al., 2005). This observation is not particularly surprising, as it is unlikely the stacked ABR would be less than the unmasked ABR, and a worst-case expectation would be that the two ABRs would be equal in amplitude (i.e., if there were little or no temporal dispersion in the cochlea). The observed amplitude increase resulted from better alignment between ABR peaks across frequency bands after latency adjustments, e.g., N5 for the original derived-band waveforms (Fig. 7) for dolphins from 8 to 16 kHz and sea lions from ∼1 to 8 kHz are out-of-phase with the high-frequency components. After temporal adjustment, the components are more closely in-phase, and thus summing increases the overall amplitude.

In dolphins, the mean increase in amplitude of the stacked ABR over the unmasked ABR was larger for P4-N5 compared to P1-N2. This likely resulted from using N5 latencies for the temporal adjustment of the derived-band ABRs. Although the derived-band latency-frequency functions obtained by fitting P4 and N5 latencies fit the P1 data well, it is possible that larger stacked ABR P1 amplitudes could have been obtained by using measured P1 latencies for the temporal adjustment. However, in practice, this would be difficult to perform due to the relatively low SNR for P1. The mean amplitude increase was also larger for the higher stimulus SPL, which may be related to the higher derived-band ABR SNR and reduced variability in latency estimates with the higher SPL stimulus. In contrast to the dolphins, the proportional amplitude increase in sea lions was larger in P1-N2 than in P4-N5; however, this may be an artifact related to the very small magnitude of P1-N2 in sea lions, which may exaggerate percentage changes, e.g., in dolphins, the ratio of P4-N5 amplitude to P1-N2 amplitude varied from 0.8 to 3, while in sea lions, the ratios were 5–7.

Overall, sea lion stacked ABRs were on average more enhanced (compared to unmasked ABRs) than those in dolphins, although the increase is small when considering only P4-N5. The lower effectiveness of the stacked ABR in dolphins may be a result of the relatively smaller contribution to the broadband ABR from the lower-frequency bands, where the effects of temporal alignment are greatest, i.e., the dolphin broadband ABR is dominated by basal contributions that are already largely in-phase because of the very high cochlear TWS. This is in contrast to the more substantial latency shifts observed for the higher-amplitude, lower-frequency derived bands in sea lions that likely contributed to a larger ABR peak amplitude increase. Based on quantitative reports in several individual subjects (Don and Kwong, 2009) and an ordinal representation of wave V amplitude for a group of unmasked and stacked ABRs (Don et al., 1997), the stacked ABR approach appears to enhance wave V amplitude in humans by 100%–300% compared to the unmasked ABR. This suggests that the increase in stacked ABR amplitude (relative to the unmasked ABR) may be larger in mammals with better lower-frequency hearing, where cochlear dispersion is expected to be more pronounced. Since the stacked ABR represents the optimal benefit from compensating for cochlear dispersion, this same relationship would be expected for input compensation using chirp stimuli as well, i.e., chirp stimuli may provide greater benefits for animals with better low-frequency hearing compared to dolphins.

As in any cross-species comparisons, differences across those animal species (in terms of, e.g., their hearing thresholds across frequency, morphology of the ABR, and optimal recording parameters for obtaining a replicable ABR) are always possible confounding factors. In this specific study, while both sea lions and bottlenose dolphins are marine mammals, ABR measurements in sea lions have been limited to anesthetized animals in air, while dolphins have been extensively tested underwater. There are significant differences between dolphin outer/middle ears and those of terrestrial mammals (and sea lions) as well as differences in hearing thresholds and bandwidths; thus, the bandwidth of the noiseburst stimuli and high-pass masking noise differed across the two species in the present study. To optimize the number of derived-band responses observed in sea lions, we assessed octave-wide derived bands in 1/2-oct steps rather than the 1/2-oct derived bands (in 1/2-oct steps) reported for the bottlenose dolphins. Any of the differences listed above could have affected the ABR results shown in this investigation. However, ABRs are not dramatically affected by subject state, including anesthesia, and the main dependent variable of interest—ABR peak latency across cochlear place—behaved in a manner reported by many previous ABR studies, i.e., ABR peak latency increased with decreasing derived-band frequency, reflecting increasing traveling-wave delay to more apical cochlear regions. We believe it is most parsimonious to interpret the present results as reflecting true differences in the hydrodynamic responses of the cochleae of the two marine mammals rather than the result of some possible confounding variables reflecting the differences in ABR stimulation and recording variables.

As in humans and terrestrial mammals, the high-pass subtractive masking technique can be used to derive narrowband ABRs in dolphins and sea lions. Between ∼8 and 32 kHz, cochlear TWSs are similar for dolphins and sea lions. Above 32 kHz, TWSs in dolphins reach substantially higher values. The temporal-shift and sum approach used to create the stacked ABR led to amplitude increases (compared to the unmasked ABR) in both marine mammal species. Sea lion stacked ABR amplitude enhancement was on average larger than that for dolphins, but both were smaller than that reported for humans. Since the stacked ABR represents the optimal benefit that could be obtained by compensating for cochlear dispersion, this suggests that input/output compensation may be more effective in species with better low-frequency hearing and larger variation in cochlear TWS in the base of the cochlea. If the patterns of frequency-specific TWS variability observed here and in humans persist across species, the stacked ABR approach (as well as upward-sweeping chirp stimuli) will be more effective (i.e., result in a relatively greater amplitude increase) for species with better low-frequency hearing.

The authors thank R. Dear, M. Wilson, H. Bateman, R. Breitenstein, K. Christman, C. Espinoza, G. Goya, M. Graves, D. Ram, T. Wu, and the animal care staff, training staff, and interns at the U.S. Navy Marine Mammal Program. Financial support was provided by the United States Navy Living Marine Resources (LMR) Program.

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