Interclick Interval Research Articles

How toothed whales echolocate to find and capture prey

Sperm and beaked whales are deep-diving toothed whales whose echolocation behavior has been studied using tags that record sound and whale orientation. Combining orientation data from tagged clicking whales with acoustic localization data from a towed hydrophone array allowed measurement of the three-dimensional beam pattern of regular clicks from sperm whales. These data confirm Mohl’s bent horn hypothesis for sound production in sperm whales. During deep foraging dives, beaked whales produce several thousand regular clicks with interclick intervals (ICI) between 0.2 and 0.4 s. These search clicks have a distinctive FM upsweep from 25 to 55 kHz and a pulse length of 200–250 μs. The process of echolocating on prey can be divided into search, approach, and capture phases. The approach phase starts when a series of echoes from prey is detected. The capture phase starts when the target is about 2–5 m away, with a terminal buzz with click rates to ICIs of about 0.01 s. Tagged whales do not adjust their ICI to match range to target, nor do they adjust click level to maintain a constant echo level, but rather have a bimodal echolocation pattern using two kinds of clicks each with a typical ICI.

Click-evoked vestibulo-ocular reflex

An enlarged, low-threshold click-evoked vestibulo-ocular reflex (VOR) can be averaged from the vertical electro-oculogram in a superior canal dehiscence (SCD), a temporal bone defect between the superior semicircular canal and middle cranial fossa. To determine the origin and quantitative stimulus-response properties of the click-evoked VOR. Three-dimensional, binocular eye movements evoked by air-conducted 100-microsecond clicks (110 dB normal hearing level, 145 dB sound pressure level, 2 Hz) were measured with dual-search coils in 11 healthy subjects and 19 patients with SCD confirmed by CT imaging. Thresholds were established by decrementing loudness from 110 dB to 70 dB in 10-dB steps. Eye rotation axis of click-evoked VOR computed by vector analysis was referenced to known semicircular canal planes. Response characteristics were investigated with regard to enhancement using trains of three to seven clicks with 1-millisecond interclick intervals, visual fixation, head orientation, click polarity, and stimulation frequency (2 to 15 Hz). In subjects and SCD patients, click-evoked VOR comprised upward, contraversive-torsional eye rotations with onset latency of approximately 9 milliseconds. Its eye rotation axis aligned with the superior canal axis, suggesting activation of superior canal receptors. In subjects, the amplitude was less than 0.01 degrees, and the magnitude was less than 3 degrees/second; in SCD, the amplitude was up to 60 times larger at 0.66 degrees, and its magnitude was between 5 and 92 degrees/second, with a threshold 10 to 40 dB below normal (110 dB). The click-evoked VOR magnitude was enhanced approximately 2.5 times with trains of five clicks but was unaffected by head orientation, visual fixation, click polarity, and stimulation frequency up to 10 Hz; it was also present on the surface electro-oculogram. In superior canal dehiscence, clicks evoked a high-magnitude, low-threshold, 9-millisecond-latency vestibulo-ocular reflex that aligns with the superior canal, suggesting superior canal receptor hypersensitivity to sound.

Development of the 40 Hz steady state auditory evoked magnetic field from ages 5 to 52

Objective Adults exhibit strong auditory 40 Hz magnetic steady state responses (SSR). Although EEG measured SSR has been studied in children, the developmental course of the magnetic SSR is unknown. Methods Sixty-nine healthy subjects ranging in age from 5 to 52 years participated in a magnetoencephalographic (MEG) study. Stimuli were monaural 500 ms duration click trains with a 25 ms inter-click interval. Contralateral magnetic responses for both hemispheres were recorded with a 37-channel MEG system. Responses were averaged and examined using wavelet-based time-frequency analysis. Source analyses were also conducted on a subset of the data. Results Gamma power from 200 to 500 ms post-stimulus onset was computed and was significantly related to subject age in both hemispheres. Hemispheric asymmetry was observed for the anterior–posterior SSR source locations, suggestive of asymmetry similar to that previously described for the SSR and other auditory evoked magnetic field components. Conclusions The 40 Hz power findings are generally consistent with previous EEG studies of steady state responses in children showing age-related changes in the 40 Hz SSR. Significance Age-related changes in the strength of the magnetic 40 Hz SSR may continue to develop well beyond early childhood, which should be taken into consideration in planning future studies using adolescents and young adults.

Male sperm whale acoustic behavior observed from multipaths at a single hydrophone

Sperm whales generate transient sounds (clicks) when foraging. These clicks have been described as echolocation sounds, a result of having measured the source level and the directionality of these signals and having extrapolated results from biosonar tests made on some small odontocetes. The authors propose a passive acoustic technique requiring only one hydrophone to investigate the acoustic behavior of free-ranging sperm whales. They estimate whale pitch angles from the multipath distribution of click energy. They emphasize the close bond between the sperm whale's physical and acoustic activity, leading to the hypothesis that sperm whales might, like some small odontocetes, control click level and rhythm. An echolocation model estimating the range of the sperm whale's targets from the interclick interval is computed and tested during different stages of the whale's dive. Such a hypothesis on the echolocation process would indicate that sperm whales echolocate their prey layer when initiating their dives and follow a methodic technique when foraging.

Echolocation clicks of free-ranging Cuvier’s beaked whales (Ziphius cavirostris)

Strandings of beaked whales of the genera Ziphius and Mesoplodon have been reported to occur in conjunction with naval sonar use. Detection of the sounds from these elusive whales could reduce the risk of exposure, but descriptions of their vocalizations are at best incomplete. This paper reports quantitative characteristics of clicks from deep-diving Cuvier's beaked whales (Ziphius cavirostris) using a unique data set. Two whales in the Ligurian Sea were simultaneously tagged with sound and orientation recording tags, and the dive tracks were reconstructed allowing for derivation of the range and relative aspect between the clicking whales. At depth, the whales produced trains of regular echolocation clicks with mean interclick intervals of 0.43 s (+/- 0.09) and 0.40 s (+/- 0.07). The clicks are frequency modulated pulses with durations of approximately 200 micros and center frequencies around 42 kHz, -10 dB bandwidths of 22 kHz, and Q(3 dB) of 4. The sound beam is narrow with an estimated directionality index of more than 25 dB, source levels up to 214 dB(pp) re: 1 microPa at 1 m, and energy flux density of 164 dB re: 1 microPa2 s. As the spectral and temporal properties are different from those of nonziphiid odontocetes the potential for passive detection is enhanced.

Auditory Saltation in the Vertical Midsagittal Plane

Auditory saltation is an illusion in which a train of clicks, the first half of which is presented at one location and the other half of which is presented from a second location, is perceived as originating not only from the anchor points, but also from locations between them. That is, intermediate members of the series of clicks have their spatial locations systematically misperceived. In the present study, auditory saltation was examined for the first time in the vertical midsagittal plane. Subjects rated the perceived continuity of motion for 8-click trains systematically varied in inter-click interval (ICI), direction of motion (up, down), and trial type ('saltation' versus 'real' motion). In all listeners, saltation stimuli supported robust saltation, but only for trials with ICIs less than about 120 ms. Real motion was rated as continuous for all ICIs. These data indicate that the auditory-saltation illusion can exploit monaural stimulus cues for source location in the generation of the illusory motion percept.

Recovery of human compound action potential using a paired-click stimulation paradigm

The recovery process from adaptation of the compound action potential (CAP) was studied using an equilevel paired click stimulation paradigm in humans with normal hearing. The CAP amplitude to the second click of paired clicks was normalized to the amplitude to the first click. The second-click CAP amplitude recovered as a function of interclick interval (ICI) between the first and the second click of a pair. A regression line fitted to the recovered amplitude data demonstrated the logarithmic function of the ICI. Full recovery times changed from 118 to 278 ms with increasing click intensity. The regression lines for higher click intensities exhibited two different slopes in two ICI ranges: from 3 to 100 and 120 to 300 ms. We suppose that the CAP recovery for ICI <100 ms is attributable to both the relative refractoriness of auditory nerve and the short-term adaptation mechanisms, while, for ICI >100 ms chiefly to the short-term adaptation mechanisms. The recovery process of the second-click CAP slowed with increasing intensity, which is a similar result to that obtained in the animal experiments by Parham et al. The input–output (I–O) curve of the second-click CAP amplitudes exhibited a different slopes above and below 60 dB normal hearing level (nHL). We assume that the mechanisms underlying this characteristic curve pattern differ from those for the I–O curve of the CAP in response to single-click stimuli. We expect that investigating the CAP recovery in pathological ears will provide clinically useful information on cochlear synaptic function.

Biosonar performance of foraging beaked whales (Mesoplodon densirostris)

Toothed whales (Cetacea, odontoceti) emit sound pulses to probe their surroundings by active echolocation. Non-invasive, acoustic Dtags were placed on deep-diving Blainville's beaked whales (Mesoplodon densirostris) to record their ultrasonic clicks and the returning echoes from prey items, providing a unique view on how a whale operates its biosonar during foraging in the wild. The process of echolocation during prey capture in this species can be divided into search, approach and terminal phases, as in echolocating bats. The approach phase, defined by the onset of detectable echoes recorded on the tag for click sequences terminated by a buzz, has interclick intervals (ICI) of 300-400 ms. These ICIs are more than a magnitude longer than the decreasing two-way travel time to the targets, showing that ICIs are not given by the two-way-travel times plus a fixed, short lag time. During the approach phase, the received echo energy increases by 10.4(+/-2) dB when the target range is halved, demonstrating that the whales do not employ range-compensating gain control of the transmitter, as has been implicated for some bats and dolphins. The terminal/buzz phase with ICIs of around 10 ms is initiated when one or more targets are within approximately a body length of the whale (2-5 m), so that strong echo returns in the approach phase are traded for rapid updates in the terminal phase. It is suggested that stable ICIs in the search and approach phases facilitate auditory scene analysis in a complex multi-target environment, and that a concomitant low click rate allows the whales to maintain high sound pressure outputs for prey detection and discrimination with a pneumatically driven, bi-modal sound generator.

DIEL VARIATION IN ECHOLOCATION BEHAVIOR OF WILD HARBOR PORPOISES

The echolocation rate and behavior of wild harbor porpoises were studied using a harbor porpoise click detector (POD) deployed close to the bottom at 40 m depth in Scottish waters, UK, April—June 2001. Echolocation variables were compared among four diel phases; morning, day, evening, and night. The echolocation encounter rate, the minimum interclick interval per train, and the proportion of echolocation click trains with a minimum interclick interval below 10 msec were all significantly higher at night than during the day. The variation in echolocation rate implies that porpoises increased their echolocation rate and/or visited the depth of the POD more often at night than during the day. Further, the changes in minimum interclick interval per train suggest that they used their echolocation for foraging or investigating objects at a close range to a higher extent, and acoustically explored the environment at greater distances at night than during the day.

Recovery and refractoriness of auditory evoked fields after gaps in click trains

When clicks are presented in a train at a rate above approximately 5 Hz, they evoke a sustained field in human auditory cortex that can be recorded by magnetoencephalography. In this study we evaluated how this sustained field continues when a click train is interrupted by a silent gap. The stimuli were click trains with interclick intervals of either 12 or 24 ms, which produce pitches of 83.3 or 41.7 Hz, respectively. The click trains were 996 ms in duration with a gap of 12, 24, 48, 96, or 192 ms beginning 504 ms post-stimulus onset. The sustained field for click trains with short gaps was similar to the one evoked by a continuous click train. Subtraction of the response evoked by a solitary click train of 504 ms enabled estimation of the sustained field in the interval after the gap. The comparison revealed that the sustained field amplitude after the gap was larger than that at the onset of the initial click train in the interval from 150 to 350 ms after onset, and the difference decreased with gap duration. In contrast, the transient P1m was refractory for gaps up to 48 ms, but had nearly recovered its initial amplitude for gaps of 192 ms. We discuss how these results might relate to the perception, i.e. if an interrupted click train is perceived as one continuous sound with a transient gap or as two successive events.

Echolocation in wild toothed whales

Don Griffin showed more than 50 years ago that bats echolocate for orientation and to capture prey. Experiments also demonstrated that captive dolphins can echolocate; more recent work parallels Griffin’s work with bats in the wild. Digital acoustic recording tags were attached to sperm and beaked whales, Ziphius cavirostris and Mesoplodon densirostris, to record outgoing clicks and incoming echoes. The sperm whale data show echoes from the sea surface and seafloor, which are probably used for orientation and obstacle avoidance. When diving, sperm whales adjust their interclick interval as they change their pitch angle, consistent with the hypothesis that they are echolocating on a horizontal layer at the depth at which they will feed. This suggests that they may be listening for volume reverberation to select a prey patch. The beam pattern of sperm whales includes a narrow, forward-directed high-frequency beam probably used for prey detection, and a broader, backward-directed lower-frequency beam probably used for orientation. Beaked whales produce directional clicks with peak frequencies in the 25–40-kHz region. Echoes from individual prey items have been detected from clicks of beaked whales. This opens a new window into the study of how animals use echolocation to forage in the wild.

The combined effects of forward masking by noise and high click rate on monaural and binaural human auditory nerve and brainstem potentials

Objective: To study effects of forward masking and rapid stimulation on human monaurally- and binaurally-evoked brainstem potentials and suggest their relation to synaptic fatigue and recovery and to neuronal action potential refractoriness. Methods: Auditory brainstem evoked potentials (ABEPs) were recorded from 12 normally- and symmetrically hearing adults, in response to each click (50 dB nHL, condensation and rarefaction) in a train of nine, with an inter-click interval of 11 ms, that followed a white noise burst of 100 ms duration (50 dB nHL). Sequences of white noise and click train were repeated at a rate of 2.89 s −1. The interval between noise and first click in the train was 2, 11, 22, 44, 66 or 88 ms in different runs. ABEPs were averaged (8000 repetitions) using a dwell time of 25 μs/address/channel. The binaural interaction components (BICs) of ABEPs were derived and the single, centrally located equivalent dipoles of ABEP waves I and V and of the BIC major wave were estimated. Results: The latencies of dipoles I and V of ABEP, their inter-dipole interval and the dipole magnitude of component V were significantly affected by the interval between noise and clicks and by the serial position of the click in the train. The latency and dipole magnitude of the major BIC component were significantly affected by the interval between noise and clicks. Interval from noise and the click's serial position in the train interacted to affect dipole V latency, dipole V magnitude, BIC latencies and the V–I inter-dipole latency difference. Most of the effects were fully apparent by the first few clicks in the train, and the trend (increase or decrease) was affected by the interval between noise and clicks. Conclusions: The changes in latency and magnitude of ABEP and BIC components with advancing position in the click train and the interactions of click position in the train with the intervals from noise indicate an interaction of fatigue and recovery, compatible with synaptic depletion and replenishing, respectively. With the 2 ms interval between noise and the first click in the train, neuronal action potential refractoriness may also be involved.

Temporal dynamics of pitch in human auditory cortex

Recent functional imaging studies have shown that sounds with temporal pitch produce selective activation in anterolateral Heschl's gyrus. This paper reports a magnetoencephalographic (MEG) study of the temporal dynamics of this activation. The cortical response specific to pitch was isolated from the intensity-related response in Planum temporale using a ‘continuous stimulation’ paradigm in which regular and irregular click trains alternate without interruption. The mean interclick interval (ICI) was 6, 12, 24, or 48 ms; the train length was 720 ms. The auditory sustained field serves as a level-dependent baseline that enhances the signal-to-noise ratio over previous techniques. The onset of pitch was accompanied by a prominent transient field, followed by a strong sustained field, both of which were associated with sources in lateral Heschl's gyrus. The sustained field rose from baseline about 70 ms after the onset of temporal regularity, asymptoted at about 450 ms, and commenced its return to baseline about 70 ms after pitch offset. The peak of the transient field occurred between 130 and 190 ms after regularity onset depending on the ICI. The latencies of the cortical pitch response are substantially longer than might be anticipated from temporal models of pitch perception. This finding suggests that the temporal integration associated with periodicity processing occurs in a subcortical structure, and that the cortical responses reflect subsequent processes involving the measurement of pitch values and changes in pitch.

A population study of the precedence effect

Data are reported from a population of untrained individuals under lag- and single-click conditions in a discrimination suppression precedence-effect task. The cue to be discriminated was an interaural level-difference (ILD). Each of 91 observers completed 10 runs in a two-interval forced-choice design under a lag-click condition and three runs under a single-click condition. Stimuli were 125-μs rectangular pulses and the interclick interval was 2 ms. Observers were randomly assigned to three groups of approximately 30. Each group was then tested at one stimulus intensity (43, 58, or 73 dB). Mean threshold within each group was greater than 15 dB for the lag-click condition and 6 dB for the single-click condition, although there was substantial interobserver variability. In contrast to [J. Acoust. Soc. Am. 114 (2003) 420] who reported a strong effect of intensity on lag-click ITD discrimination, no effect of intensity was observed on lag-click ILD thresholds. Analysis of over 50,000 near-threshold trials from 302 observers pooled across studies showed a spatial asymmetry in response patterns and a small, but statistically significant effect of gender. A model is proposed which shows that decay of sensory memory and increases in auditory filter bandwidths with intensity may predict the different findings for ILD versus ITD lag-click thresholds.

Precedence-effect thresholds for a population of untrained listeners as a function of stimulus intensity and interclick interval

Data are reported from 127 untrained individuals under lag- and single-click conditions in a precedence-effect task. In experiment I, each subject completed ten runs in a two-interval forced-choice design under a lag-click condition and three runs under a single-click condition. The cue to be discriminated was an interaural time difference (ITD). Stimuli were 125-micros rectangular pulses and the interclick interval (ICI) was 2 ms. Subjects were randomly assigned to three groups of approximately 30. Each group was tested at one stimulus intensity (43, 58, or 73 dB). Mean threshold within each group was greater than 500 micros for lag-click ITD conditions, although substantial intersubject variability and a clear effect of stimulus intensity on lag-click ITD thresholds were observed, with lower thresholds for higher intensities. In experiment II, the ICI was varied from 0.3 to 10 ms, and thresholds were obtained from groups of approximately 20 untrained subjects. Data were also collected from three highly experienced observers as a function of ICI. The best naive subject produced mean thresholds near, but not as low as those obtained from experienced subjects. Analysis of adaptive-track patterns revealed abrupt irregularities in threshold tracking, consistent with either losing the cue or listening to the wrong cue in an ambiguous stimulus.

Changes in CAP adaptation in experimentally induced endolymphatic hydrops

Objective: To determine the effect of experimentally induced endolymphatic hydrops (ELHs) on compound action potential (CAP) adaptation. Methods: The CAP was recorded 1 month after surgical treatment to produce ELH. The CAP threshold in response to click stimuli showed no significant differences between the hydropic and control groups. The CAP was elicited from the retroauricular-exposed round window using a silver ball electrode. Click trains consisting of 10 clicks with an interclick interval (Δ t) of either 4 or 8 ms were delivered through a loudspeaker placed in front of the animals' ears. The patterns of adaptation to these click trains were evaluated as functions of Δ t and intensity level. Results: An abnormal pattern of CAP adaptation was observed in hydropic ears. Conclusions: These findings suggest that early ELH influences CAP adaptation.

HORIZONTAL ANGULAR DISCRIMINATION BY AN ECHOLOCATING BOTTLENOSE DOLPHIN TURSIOPS TRUNCATUS

ABSTRACT A bottlenose dolphin was tested on its ability to echoically discriminate horizontal angular differences between two arrays of vertical, air-filled, PVC rods. The blindfolded dolphin was required to station in a submerged, vertically-oriented hoop, 2 radial metres from the stimuli, and indicate whether an array with four rods (S+) was to the left or the right of an array with two rods (S-), by pressing a corresponding paddle. The angular separation between the rods within each array (θw) was maintained at 2 degrees but the angular separation between the two arrays (θb) was varied to produce angular differences (δθ = θb-θw)ranging from 0.25 degrees to 4 degrees. A modified method of constant stimuli was used to test for angular discrimination ability, and yielded a psychometric function having a 75% correct threshold of 1.6 degrees. This threshold fell between the passive listening minimum audible angle thresholds of 0.9 degrees for click signals and 2.1 degrees for a pure tone signal (Renaud & Popper 1975). Analyses of response times, number of clicks and inter-click intervals failed to detect any significant adaptive behaviour occurring as the task became more difficult. These results help to define angular resolution capabilities of dolphin sonar that may play an important role in representing spatial information in the dolphin's environment.

Combining data from a multisensor tag and passive sonar to determine the diving behavior of a sperm whale (physeter macrocephalus)

Reports on the diving behavior of a sperm whale tagged and tracked on September 6, 2000 during the Sirena 2000 cruise in the Ligurian Sea. A total of about 4.5 h of acoustic and nonacoustic sensor data were recorded when a sperm whale was tagged with a Woods Hole Oceanographic Institution developed tag with a hydrophone, motion, and pressure sensors. The animal was simultaneously tracked with a passive sonar system deployed from the NATO research vessel NRV Alliance. By combining data from the tag and passive sonar, we were able to reconstruct a three-dimensional track of the whale, along with its orientation and vocal behavior. While it was tagged, the whale carried out three deep dives to a depth of about 900 m in an area with a bottom depth of about 2600 m. The inter-click intervals of the diving whale were not consistent with ranging on the bottom, but were consistent with the hypothesis that the whale was possibly echolocating on some target(s) near the depth at which it dove to feed. This study demonstrated an ability to track subtle changes in the behavior of diving whales. This ability is important for three areas: 1) basic research, 2) studies of the responses of these animals to controlled exposures of man-made noise, and 3) studies to infer the biological significance of behavioral disruption.

Auditory nerve recordings in Xenopus laevis

The South African clawed frog X. laevis communicates using a rich repertoire of underwater calls made up of clicks. Two calls, rapping and ticking, differ only by interclick interval [Tobias et al., PNAS (1998)]. To begin to explore rate coding in the auditory system, extracellular recordings were obtained in vivo from the auditory nerve of frogs stimulated with both pure tones and recorded calls. To avoid problems of impedance matching, acoustic stimuli were delivered via vibration-excited probe directly to the frog’s tympanum. Preferred frequencies across the population of 104 recorded fibers (taken from 5 females) fell into 2 or 3 groups: 1500, 600, and 200 Hz. Cells of all preferred frequencies fired in phase with clicks of the various calls. [Work supported by an NSF graduate fellowship to TME.]

The acoustic behaviour of diving sperm whales observed with a hydrophone array

Clicks of male sperm whales ( Physeter catodon Linneaus) were recorded off Northern Norway using a hydrophone array. The 3-D diving behaviour in one complete (34 min) and four incomplete (6–36 min) dives was observed using passive acoustic localization. The vertical swim speed was 0.8–1.4 m/s, and the horizontal swim speed was 0.2–2.6 m/s. The maximum dive depth of an individual track ranged from 358 to 1494 m. The bottom depth was 500 to 1600 m and a scattering layer was present at 250 m. Clicks were usually emitted with inter-click intervals (ICI) of 0.5–2 s in blocks of 29–249 clicks, interspaced by pauses of 6–117 s. The length of blocks decreased with depth in a manner predictable from a pneumatic sound generator. Click sequences with shorter inter-click intervals, denoted creaks and believed to indicate feeding events, were located at depths from 278 to 1245 m. This study suggests that sperm whales exploit prey in a large part of the water column below the scattering layer and use an air-driven sound production system.