Saccular potentials of the vocal plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The plainfin midshipman fish, Porichthys notatus, is a vocal species of teleost fish that generates acoustic signals for intraspecific communication during social and reproductive behaviors. All adult morphs (females and males) produce single short duration grunts important for agonistic encounters, but only nesting males produce trains of grunts and growls in agonistic contexts and long duration multiharmonic advertisement calls to attract gravid females for spawning. The midshipman fish uses the saccule as the main acoustic endorgan for hearing to detect and locate vocalizing conspecifics. Here, I examined the response properties of evoked potentials from the midshipman saccule to determine the frequency response and auditory threshold sensitivity of saccular hair cells to behaviorally-relevant single tone stimuli. Saccular potentials were recorded from the rostral, medial and caudal regions of the saccule while sound was presented by an underwater speaker. Saccular potentials of the midshipman, like other teleosts, were evoked greatest at a frequency that was twice the stimulus frequency. Results indicate that midshipman saccular hair cells of non-reproductive adults had a peak frequency sensitivity that ranged from 75 (lowest frequency tested) to 145 Hz and were best suited to detect the low frequency components (≤105 Hz) of midshipman vocalizations.     

Auditory saccular sensitivity of the vocal Lusitanian toadfish: low frequency tuning allows acoustic communication throughout the year

A novel form of auditory plasticity for enhanced detection of social signals was described in a teleost fish, Porichthys notatus (Batrachoididae, Porichthyinae). The seasonal onset of male calling coincides with inshore migration from deep waters by both sexes and increased female sensitivity to dominant frequencies of male calls. The closely related Lusitanian toadfish, Halobatrachus didactylus, (Batrachoididae, Halophryninae) also breeds seasonally and relies on acoustic communication to find mates but, instead, both sexes stay in estuaries and show vocal activity throughout the year. We investigated whether the sensitivity of the inner ear saccule of H. didactylus is seasonally plastic and sexually dimorphic. We recorded evoked potentials from populations of saccular hair cells from non-reproductive and reproductive males and females in response to 15–945 Hz tones. Saccular hair cells were most sensitive at 15–205 Hz (thresholds between 111 and 118 dB re. 1 μPa). Both sexes showed identical hearing sensitivity and no differences were found across seasons. The saccule was well suited to detect conspecific vocalizations and low frequencies that overlapped with lateral line sensitivity. We showed that the saccule in H. didactylus has major importance in acoustic communication throughout the year and that significant sensory differences may exist between the two batrachoidid subfamilies.     

Response properties and biological function of the skate electrosensory system during ontogeny

This study examined the response properties of skate electrosensory primary afferent neurons of pre-hatch embryo (8–11 weeks), post-hatch juvenile (1–8 months), and adult (>2 year) clearnose skates (Raja eglanteria) to determine whether encoding of electrosensory information changes with age, and if the electro-sense is adapted to encode natural bioelectric stimuli across life history stages. During ontogeny, electrosensory primary afferents increase resting discharge rate, spike regularity, and sensitivity at best frequency. Best frequency was at 1–2 Hz for embryos, showed an upwards shift to 5 Hz in juveniles, and a downward shift to 2–3 Hz in adults. Encapsulated embryos exhibit ventilatory movements that are interrupted by a “freeze response”” when presented with weak uniform fields at 0.5 and 1 Hz. This phasic electric stimulus contains spectral information found in potentials produced by natural fish predators, and therefore indicates that the embryo electrosense can efficiently mediate predator detection and avoidance. In contrast, reproductively active adult clearnose skates discharge their electric organs at rates near the peak frequency sensitivity of the adult electrosensory system, which; facilitates electric communication during social behavior. We suggest that life-history-dependent functions such as these may shape the evolution of the low-frequency response properties for the elasmobranch electrosensory system. Accepted: 19 February 1998     

Directionality and frequency tuning of primary saccular afferents of a vocal fish, the plainfin midshipman (Porichthys notatus)

While particle motion is thought to directly stimulate the inner ear of most fish species, it is difficult to measure and might not be predictable from pressure measurements in a small tank. It is therefore important to replicate experiments conducted relative to pressure measurements using stimuli of known particle motion, to ensure that unmeasured components of the stimulus field do not produce misleading frequency response profiles. The frequency sensitivity of the inner ear of the plainfin midshipman fish, Porichthys notatus, in response to isopressure stimuli has been described. This study now examines the frequency and directional response properties of midshipman saccular afferents in response to whole-body displacements simulating acoustic particle motion. Best frequencies were distributed bimodally, with peaks at 50 Hz and 100 Hz. Most units had cosinusoidally shaped directional response profiles in the horizontal and vertical planes, though some units showed slight deviations from this pattern. A few units (probably saccular efferents) had omnidirectional directional response profiles and did not phase lock to the stimulus waveform. These results are consistent with responses of the midshipman saccular nerve to isopressure stimuli, and strengthen the hypothesis that the frequency sensitivity of the midshipman ear matches the frequency content of behaviorally relevant vocalizations.     

Development of the Acoustically Evoked Behavioral Response in Larval Plainfin Midshipman Fish,Porichthys notatus

The ontogeny of hearing in fishes has become a major interest among bioacoustics researchers studying fish behavior and sensory ecology. Most fish begin to detect acoustic stimuli during the larval stage which can be important for navigation, predator avoidance and settlement, however relatively little is known about the hearing capabilities of larval fishes. We characterized the acoustically evoked behavioral response (AEBR) in the plainfin midshipman fish, Porichthys notatus, and used this innate startle-like response to characterize this species'' auditory capability during larval development. Age and size of larval midshipman were highly correlated (r² = 0.92). The AEBR was first observed in larvae at 1.4 cm TL. At a size ≥1.8 cm TL, all larvae responded to a broadband stimulus of 154 dB re1 µPa or −15.2 dB re 1 g (z-axis). Lowest AEBR thresholds were 140–150 dB re 1 µPa or −33 to −23 dB re 1 g for frequencies below 225 Hz. Larval fish with size ranges of 1.9–2.4 cm TL had significantly lower best evoked frequencies than the other tested size groups. We also investigated the development of the lateral line organ and its function in mediating the AEBR. The lateral line organ is likely involved in mediating the AEBR but not necessary to evoke the startle-like response. The midshipman auditory and lateral line systems are functional during early development when the larvae are in the nest and the auditory system appears to have similar tuning characteristics throughout all life history stages.     

Seismic and auditory tuning curves from bullfrog saccular and amphibian papular axons

We present seismic and auditory frequency tuning curves of individual bullfrog, Rana catesbeiana, saccular and amphibian papilla axons that responded to both seismic and auditory stimuli. In this study we found: 1) most saccular axons respond well to auditory stimuli with moderate signal strength (50-70 dB SPL) as well as to seismic stimuli; 2) most amphibian papilla axons respond well to seismic stimuli as well as to auditory stimuli, and their seismic sensitivities are comparable to those of saccular axons (responding to sinusoidal stimuli with peak accelerations in the range 0.001 to 0.1 cm/S2); 3) the responses to both seismic and auditory stimuli from both saccule and amphibian papilla are tuned, i.e. the strength of the response varies with the frequency of the stimulus; and this tuning is clearly not the result of second order resonance; 4) in individual axons the tuning properties for seismic stimuli often are not the same as those for auditory stimuli, a fact that may provide clues about how the stimulus signal energy is transferred to the hair cells in each case.     

Catecholaminergic Innervation of Central and Peripheral Auditory Circuitry Varies with Reproductive State in Female Midshipman Fish,Porichthys notatus

In seasonal breeding vertebrates, hormone regulation of catecholamines, which include dopamine and noradrenaline, may function, in part, to modulate behavioral responses to conspecific vocalizations. However, natural seasonal changes in catecholamine innervation of auditory nuclei is largely unexplored, especially in the peripheral auditory system, where encoding of social acoustic stimuli is initiated. The plainfin midshipman fish, Porichthys notatus, has proven to be an excellent model to explore mechanisms underlying seasonal peripheral auditory plasticity related to reproductive social behavior. Recently, we demonstrated robust catecholaminergic (CA) innervation throughout the auditory system in midshipman. Most notably, dopaminergic neurons in the diencephalon have widespread projections to auditory circuitry including direct innervation of the saccule, the main endorgan of hearing, and the cholinergic octavolateralis efferent nucleus (OE) which also projects to the inner ear. Here, we tested the hypothesis that gravid, reproductive summer females show differential CA innervation of the auditory system compared to non-reproductive winter females. We utilized quantitative immunofluorescence to measure tyrosine hydroxylase immunoreactive (TH-ir) fiber density throughout central auditory nuclei and the sensory epithelium of the saccule. Reproductive females exhibited greater density of TH-ir innervation in two forebrain areas including the auditory thalamus and greater density of TH-ir on somata and dendrites of the OE. In contrast, non-reproductive females had greater numbers of TH-ir terminals in the saccule and greater TH-ir fiber density in a region of the auditory hindbrain as well as greater numbers of TH-ir neurons in the preoptic area. These data provide evidence that catecholamines may function, in part, to seasonally modulate the sensitivity of the inner ear and, in turn, the appropriate behavioral response to reproductive acoustic signals.     

Sound reception in two anabantid fishes

1. Pure tone displacement sensitivity and bandwidth were measured from the saccule of the ear in two anabantid species (Trichogaster trichopterus and Helostoma temincki) using microphonic potentials with a 1 microV RMS threshold for the second harmonic of the stimulus frequency. 2. Saccular microphonics were recorded in both species from 80 to 1600 Hz, with lowest thresholds between 100 and 200 Hz. The overall microphonic response curves (sensitivity and bandwidth) of the two species were statistically similar to one another with an analysis of variance, although there were statistically different thresholds at 100 and 800 Hz. 3. The hair cell orientation patterns of the saccular epithelia differ in the two species. Consequently, the comparative sizes of the saccular sensory epithelium and numbers of sensory hair cells were examined. The saccular sensory epithelium of Helostoma is about 40% larger and contains nearly 50% more hair cells than the saccular epithelium of a comparably sized Trichogaster. 4. An extracranial air bubble, located in the suprabranchial chamber, is found in both species. The bubble has direct access to the saccular chamber in Trichogaster through a foramen which is absent in Helostoma. Despite the difference in morphology and the larger numbers of sensory hair cells in Helostoma, hearing sensitivity and bandwidth is similar in the two species. Although the structural differences in the auditory periphery do not affect pure tone sensitivity and bandwidth, other aspects of fish hearing such as frequency discrimination, discrimination of signals in the presence of noise, and/or sound localization ability may be affected by these structural differences.     

Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: single tones

The midshipman fish, Porichthys notatus, generates acoustic signals for intraspecific communication. Nesting males produce long-duration “hums” which attract gravid females and can be effectively mimicked by pure tones. In this study we examine the encoding of tonal signals by the midshipman peripheral auditory system. Single-unit recordings were made from afferents innervating the sacculus while presenting sounds via an underwater loudspeaker. Units were characterized by iso-intensity spike rate and vector strength of synchronization curves, as well as by peri-stimulus time histograms. Additionally, response-intensity curves and responses to long-duration (up to 10 s) stimuli were obtained. As has been seen in other teleosts, afferents had highly variable activity profiles. Excitatory frequencies ranged from 60 to over 300 Hz with most units responding best around 70 or 140 Hz. Thresholds at 90 Hz ranged from 95 to 145 dB re 1 μPa. Strong synchronization provided a robust temporal code of frequency, comparable to that described for goldfish. Spike rate showed varying degrees of adaptation but high rates were generally maintained even for 10-s stimuli. The midshipman peripheral auditory system is well suited to encoding conspecific communication signals, but nonetheless shares many response patterns with the auditory system of other teleosts. Accepted: 10 February 1999     

Effects of saccular otolith removal on hearing sensitivity of the sleeper goby (<Emphasis Type="Italic">Dormitator latifrons</Emphasis>)

It is not known to what extent the entire saccule contributes to overall hearing sensitivity in any fish species. Here we report directional and frequency sensitivity in a teleost fish (Dormitator latifrons) and effects of unilateral and bilateral removal of saccular otoliths on its hearing sensitivity. The fish had different hearing thresholds in the horizontal (-54.4 to -50.3 dB re: 1 micro m) and mid-sagittal (-58.6 to -53.1 dB) planes. At 100 Hz, unilateral otolith removal did not significantly change hearing sensitivity in the mid-sagittal plane, but caused selective reductions of auditory sensitivity by 3-7 dB in the azimuthal axes that are consistent with the longitudinal axis of the damaged saccule. Along the fish's longitudinal axis, unilateral otolith removal significantly decreased auditory sensitivity at 50 Hz and 400 Hz, but not at 100 Hz, 200 Hz, and 345 Hz. At 100 Hz, bilateral otolith removal resulted in robust hearing loss of 27-35 dB at different axes in both horizontal and mid-sagittal planes. Along the fish's longitudinal axis, the bilateral removal reduced auditory sensitivity by 13-27 dB at the different frequencies. Therefore, these results demonstrate that the saccule plays important roles in directional hearing and frequency responses.     

Encoding properties of auditory neurons in the brain of a soniferous damselfish: response to simple tones and complex conspecific signals

The fish auditory system encodes important acoustic stimuli used in social communication, but few studies have examined response properties of central auditory neurons to natural signals. We determined the features and responses of single hindbrain and midbrain auditory neurons to tone bursts and playbacks of conspecific sounds in the soniferous damselfish, Abudefduf abdominalis. Most auditory neurons were either silent or had slow irregular resting discharge rates <20 spikes s⁻¹. Average best frequency for neurons to tone stimuli was ~130 Hz but ranged from 80 to 400 Hz with strong phase-locking. This low-frequency sensitivity matches the frequency band of natural sounds. Auditory neurons were also modulated by playbacks of conspecific sounds with thresholds similar to 100 Hz tones, but these thresholds were lower than that of tones at other test frequencies. Thresholds of neurons to natural sounds were lower in the midbrain than the hindbrain. This is the first study to compare response properties of auditory neurons to both simple tones and complex stimuli in the brain of a recently derived soniferous perciform that lacks accessory auditory structures. These data demonstrate that the auditory fish brain is most sensitive to the frequency and temporal components of natural pulsed sounds that provide important signals for conspecific communication.     

Pupillary dilation response as an indicator of auditory discrimination in the barn owl

The pupil of an awake, untrained, head-restrained barn owl was found to dilate in response to sounds with a latency of about 25 ms. The magnitude of the dilation scaled with signal-to-noise ratio. The dilation response habituated when a sound was repeated, but recovered when stimulus frequency or location was changed. The magnitude of the recovered response was related to the degree to which habituating and novel stimuli differed and was therefore exploited to measure frequency and spatial discrimination. Frequency discrimination was examined by habituating the response to a reference tone at 3 kHz or 6 kHz and determining the minimum change in frequency required to induce recovery. We observed frequency discrimination of 125 Hz at 3 kHz and 250 Hz at 6 kHz – values comparable to those reported by others using an operant task. Spatial discrimination was assessed by habituating the response to a stimulus from one location and determining the minimum horizontal speaker separation required for recovery. This yielded the first measure of the minimum audible angle in the barn owl: 3° for broadband noise and 4.5° for narrowband noise. The acoustically evoked pupillary dilation is thus a promising indicator of auditory discrimination requiring neither training nor aversive stimuli. Accepted: 28 February 2000     

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.     

Dynamics of heart rate response in sleeping infants exposed to tone stimuli

Heart rate, EEG, and motor responses were recorded following presentation of a series of 6–10 sound stimuli (2.5-s tones of 1000, 4000, and 250 Hz, 70 dB, interstimulus intervals 18–25 s) in neonates aged 9 to 22 weeks during stage 2–3 sleep. The infants (17 of 19) revealed heart rate (HR) changes in response to tone stimuli that consisted in an expanded form of three phases: (1) short-latency (at 1 s after tone presentation) HR deceleration, (2) HR acceleration with a maximum at 3–5 s, and (3) late HR deceleration at 6–9 s of the poststimulus interval. The occurrence rate of the first two phases of cardiac response is relatively constant during a series of stimuli, whereas the likelihood of late HR deceleration is the highest following the first tone presentation and decreases significantly when the stimulus is repeated. Differences in the dynamics and statistical analysis allow a relative independence of all the three response phases to be suggested. The HR acceleration phase is dramatically enhanced in association with the motor response elicited by the sound stimulus. The late HR deceleration phase occurs not only after the first presentation of stimuli, but also when they are repeated if they evoke EEG reaction (vertex potentials) in response to both the beginning and end of the tone sound. Possible mechanisms of the three phases of poststimulus HR changes are: the vagal cardiac reflex associated with the acoustic (adaptive) reflex, activation of sympathetic efferents in combination with the startle reflex, and secondary vagal deceleration of sinus rhythm likely to be associated with the processes of perception (detection) of a “novel” stimulus and to serve as an indirect sign of an orienting reaction.     

Larvae and juveniles of Leptoderma lubricum and L. retropinnum (Argentiformes: Alepocephalidae) collected from Suruga Bay, Japan

Larvae and juveniles of the alepocephalid fishes, Leptoderma lubricum [26.9–69.0 mm in standard length (SL)] and Leptoderma retropinnum (21.1–67.2 mm SL), collected within 1–8 m of the seafloor in Suruga Bay, southern Japan, are described. They can be easily distinguished from each other by the following adult-like characters: membrane morphology between the vertical fin rays and procurrent caudal-fin rays (separated in L. lubricum vs. continuous in L. retropinnum), numbers of dorsal-fin rays (34–40 vs. 45–52) and anal-fin rays (50–57 vs. 65–72), and caudal peduncle length (11.7–13.4% SL vs. 4.5–5.9% SL), in addition to several other body proportional differences. Unique characters in the larval stages of Leptoderma include a translucent occipital region, horizontally elongated eye, and head below the upper margin of the orbit and abdominal cavity densely covered by melanophores, ontogeny being characterized by the acquisition of general adult characters to the postflexion stage, indistinct transformation, and the retention of few larval characters until almost the end of the juvenile stage, as in other known alepocephalids. In addition to the near-bottom larval and juvenile collections of both species, the occurrences of benthic or near-bottom taxa, including Harpacticoida, in their gut contents confirmed the early life history dependence of the former on the near-bottom.     

A study of the time and frequency characteristics of the potentials evoked in the acoustical cortex

Evoked potentials in the auditory cortex of the cat are measured by applying auditory stimulations in the form of tone bursts of 700 Hz. Transient evoked potentials obtained in this way are transformed to the frequency domain using a Laplace Transform. The amplitude frequency characteristic obtained with this semi-empirical method depicts maxima of EEG-amplitude in frequency ranges of 10–13 Hz and 60–80 Hz. The correlation between the time course of evoked potentials and spontaneous activity of the brain and the efficiency of the method used are pointed out.     

Acoustic response properties of lagenar nerve fibers in the sleeper goby,<Emphasis Type="Italic"> Dormitator latifrons</Emphasis>

Auditory and vestibular functions of otolithic organs vary among vertebrate taxa. The saccule has been considered a major hearing organ in many fishes. However, little is known about the auditory role of the lagena in fishes. In this study we analyzed directional and frequency responses from single lagenar fibers of Dormitator latifrons to linear accelerations that simulate underwater acoustic particle motion. Characteristic frequencies of the lagenar fibers fell into two groups: 50 Hz and 80–125 Hz. We observed various temporal response patterns: strong phase-locking, double phase-locking, phase-locked bursting, and non-phase-locked bursting. Some bursting responses have not been previously observed in vertebrate otolithic nerve fibers. Lagenar fibers could respond to accelerations as small as 1.1 mm s^–2. Like saccular fibers, lagenar fibers were directionally responsive and decreased directional selectivity with stimulus level. Best response axes of the lagenar fibers clustered around the lagenar longitudinal axis in the horizontal plane, but distributed in a diversity of axes in the mid-sagittal plane, which generally reflect morphological polarizations of hair cells in the lagena. We conclude that the lagena of D. latifrons plays a role in sound localization in elevation, particularly at high stimulus intensities where responses of most saccular fibers are saturated.Abbreviations BRA best response axis/axes - BS best sensitivity - CF characteristic frequency - CV coefficient of variation - DI directionality index - ISIH inter-spike interval histogram - PSTH peri-stimulus time histogram - SR spontaneous rate     

Temporal resolution for calling song signals by female crickets, <Emphasis Type="Italic">Gryllus bimaculatus</Emphasis>

A behavioural gap detection paradigm was used to determine the temporal resolution for song patterns by female crickets, Gryllus bimaculatus. For stimuli with a modulation depth of 100% the critical gap duration was 6–8 ms. A reduction of the modulation depth of gaps to 50% led either to an increase or a decrease of the critical gap duration. In the latter case, the critical gap duration dropped to 3–4 ms indicating a higher sensitivity of auditory processing. The response curve for variation of pulse period was not limited by temporal resolution. However, the reduced response to stimuli with a high duty cycle, and thus short pause durations, was in accordance with the limits of temporal resolution. The critical duration of masking pulses inserted into pauses was 4–6 ms. An analysis of the songs of males revealed that gaps (5.8 ms) and masking pulses (6.9 ms) were at detectable time scales for the auditory pathway of female crickets. However, most of the observed temporal variation of song patterns was tolerated by females. Critical cues such as pulse period and pulse duty cycle provided little basis for inter-individual selection by females.