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.     

Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The auditory system of the plainfin midshipman fish, Porichthys notatus, is an important sensory receiver system used to encode intraspecific social communication signals in adults, but the response properties and function of this receiver system in pre-adult stages are less known. In this study we examined the response properties of auditory-evoked potentials from the midshipman saccule, the main organ of hearing in this species, to determine whether the frequency response and auditory threshold of saccular hair cells to behaviorally relevant single tone stimuli change during ontogeny. Saccular potentials were recorded from three relative sizes of midshipman fish: small juveniles [1.9–3.1 cm standard length (SL), large juveniles (6.8–8.0 cm SL) and non-reproductive adults (9.0–22.6 cm SL)]. The auditory evoked potentials were recorded from the rostral, middle and caudal regions of the saccule while single tone stimuli (75–1,025 Hz) were presented via an underwater speaker. We show that the frequency response and auditory threshold of the midshipman saccule is established early in development and retained throughout ontogeny. We also show that saccular sensitivity to frequencies greater than 385 Hz increases with age/size and that the midshipman saccule of small and large juveniles, like that of non-reproductive adults, is best suited to detect low frequency sounds (<105 Hz) in their natural acoustic environment.     

Hearing in the eel (Anguilla anguilla)

Summary The auditory sensitivity in the European eel (Anguilla anguilla) was measured using an acoustic tube producing sound stimuli with different ratios between sound pressure and particle motion. The upper audible frequency limit in the eel was about 300 Hz. At low frequencies the relevant stimulus parameter was particle motion, excluding involvement of the swimbladder. At the higher frequencies within the audible range the swimbladder conveyed an auditory advantage for stimuli with a high ratio between pressure and particle motion. The eel has an extremely long distance between the swimbladder and the ear. An auditory function of the swimbladder in this species therefore indicates an efficient transmission channel for the reradiated swimbladder pulsations between the bladder and the ear, although specialized anatomical adaptations for this purpose are lacking.     

Auditory physiology and anatomy of octavolateral efferent neurons in a teleost fish

Vertebrate hair cell systems receive innervation from efferent neurons in the brain. Here we report the responses of octavolateral efferent neurons that innervate the inner ear and lateral lines in a teleost fish, Dormitator latifrons, to directional linear accelerations, and compare them with the afferent responses from the saccule, the main auditory organ in the inner ear of this species. Efferent neurons responded to acoustic stimuli, but had significantly different response properties than saccular afferents. The efferents produced uniform, omnidirectional responses with no phase-locking. Evoked spike rates increased monotonically with stimulus intensity. Efferents were more broadly tuned and responsive to lower frequencies than saccular afferents, and efferent modulation of the otolithic organs and lateral lines is likely more pronounced at lower frequencies. The efferents had wide dynamic ranges, shallow rate-level function slopes, and low maximum discharge rates. These findings support the role of the efferent innervation of the otolithic organs as part of a general arousal system that modulates overall sensitivity of the peripheral octavolateral organs. In addition, efferent feedback may help unmask biologically relevant directional stimuli, such as those emitted by a predator, prey, or conspecific, by reducing sensitivity of the auditory system to omnidirectional ambient noise.     

Directional selectivity and frequency tuning of midbrain cells in the oyster toadfish, Opsanus tau

Single-unit recordings were made from areas in the midbrain (torus semicircularis) of the oyster toadfish. We evaluated frequency tuning and directional responses using whole-body oscillation to simulate auditory stimulation by particle motion along axes in the horizontal and mid-sagittal planes. We also tested for bimodality in responses to auditory and hydrodynamic stimuli. One recording location in each animal was marked by a neurobiotin injection to confirm the recording site. Recordings were made in nucleus centralis, nucleus ventrolateralis, and the deep cell layer. Most units were frequency-selective with best frequencies between 50 and 141 Hz. Suppression of activity was apparent in 10% of the cells. Bimodality was common, including inhibition and suppression of background activity by auditory or hydrodynamic stimulation. The majority of the cells were directionally selective with directional response patterns that were sharpened compared with those of primary saccular afferents. The best directional axes were arrayed widely in spherical space, covering most azimuths and elevations. This representation is adequate for the computation of the motional axis of an auditory stimulus for sound source localization.Abbreviations BF best frequency - DCL deep cell layer - DON descending octaval nucleus - DRP directional response pattern - FFT fast Fourier transform - LL lateral lemniscus - NC nucleus centralis - NVL nucleus ventrolateralis - PVC periventricular cells - R coefficient of synchronization - TS torus semicircularis - Z Rayleigh statistic     

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     

Colour and luminance interactions in the visual perception of motion

We sought to determine the extent to which red-green, colour-opponent mechanisms in the human visual system play a role in the perception of drifting luminance-modulated targets. Contrast sensitivity for the directional discrimination of drifting luminance-modulated (yellow-black) test sinusoids was measured following adaptation to isoluminant red-green sinusoids drifting in either the same or opposite direction. When the test and adapt stimuli drifted in the same direction, large sensitivity losses were evident at all test temporal frequencies employed (1-16 Hz). The magnitude of the loss was independent of temporal frequency. When adapt and test stimuli drifted in opposing directions, large sensitivity losses were evident at lower temporal frequencies (1-4 Hz) and declined with increasing temporal frequency. Control studies showed that this temporal-frequency-dependent effect could not reflect the activity of achromatic units. Our results provide evidence that chromatic mechanisms contribute to the perception of luminance-modulated motion targets drifting at speeds of up to at least 32 degrees s(-1). We argue that such mechanisms most probably lie within a parvocellular-dominated cortical visual pathway, sensitive to both chromatic and luminance modulation, but only weakly selective for the direction of stimulus motion.     

Neural representations of the axis of acoustic particle motion in nucleus centralis of the torus semicircularis of the goldfish, <Emphasis Type="Italic">Carassius auratus</Emphasis>

Experiments examined differential coding of acoustic particle motion axis in the auditory midbrain of goldfish. Animals were exposed to vibratory stimuli varying in axis orientation as action potentials were recorded from single units in the central neuropil of nucleus centralis in the torus semicircularis. Response magnitudes as a function of stimulation axis were visualized in three dimensional plots called directional response profiles. These are generally comparable to directional responses observed among primary saccular afferents in having substantially vertical orientations. Distortions in shape from the peripheral patterns indicate neural information processing. A three-dimensional model was used to evaluate the hypothesis that responses in the auditory midbrain reflect the convergence of excitatory and inhibitory primary afferent-like responses. Model afferent inputs were generated and combined arithmetically. This analysis gives insight into the mechanisms of information processing that appear to occur in brainstem nuclei. The lack of diversity in best axis directions suggests that this mechanism alone cannot account for directional hearing abilities in this species. The roles that this directional representation and processing may play in directional hearing and sound source localization are not yet clear. Implications of these data on current models of fish directional hearing are discussed.     

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     

Stimulus change detection in phasic auditory units in the frog midbrain: frequency and ear specific adaptation

Neural adaptation, a reduction in the response to a maintained stimulus, is an important mechanism for detecting stimulus change. Contributing to change detection is the fact that adaptation is often stimulus specific: adaptation to a particular stimulus reduces excitability to a specific subset of stimuli, while the ability to respond to other stimuli is unaffected. Phasic cells (e.g., cells responding to stimulus onset) are good candidates for detecting the most rapid changes in natural auditory scenes, as they exhibit fast and complete adaptation to an initial stimulus presentation. We made recordings of single phasic auditory units in the frog midbrain to determine if adaptation was specific to stimulus frequency and ear of input. In response to an instantaneous frequency step in a tone, 28 % of phasic cells exhibited frequency specific adaptation based on a relative frequency change (delta-f = ±16 %). Frequency specific adaptation was not limited to frequency steps, however, as adaptation was also overcome during continuous frequency modulated stimuli and in response to spectral transients interrupting tones. The results suggest that adaptation is separated for peripheral (e.g., frequency) channels. This was tested directly using dichotic stimuli. In 45 % of binaural phasic units, adaptation was ear specific: adaptation to stimulation of one ear did not affect responses to stimulation of the other ear. Thus, adaptation exhibited specificity for stimulus frequency and lateralization at the level of the midbrain. This mechanism could be employed to detect rapid stimulus change within and between sound sources in complex acoustic environments.     

Coding of acoustic particle motion by utricular fibers in the sleeper goby, <Emphasis Type="Italic">Dormitator latifrons</Emphasis>

It is unknown whether the fish utricle contributes to directional hearing. Here, we report response properties of single utricular fibers in a teleost fish (Dormitator latifrons) to linear accelerations at various stimulus frequencies and axes. Characteristic frequencies ranged from 50–400 Hz (median=80 Hz), and best frequencies shifted from 50 to 250 Hz with stimulus level. Best sensitivity of utricular fibers was distributed from –70 to –40 dB re: 1 g (mean=–52 dB), which is about 30 dB less sensitive than saccular fibers. Q_50% fell between 0.16 and 11.50 (mean=2.04) at 15 dB above threshold. We observed temporal response patterns of entrained phase-locking, double phase-locking, phase-locked bursting, and non-phase-locked bursting. Most utricular fibers were directionally selective with various directional response profiles, and directional selectivity was stimulus-level dependent. Horizontal best-response axes were distributed in a 152° range while mid-sagittal best-response axes were clustered around the fish longitudinal axis, which is consistent with the horizontal orientation of the utricle and morphological polarizations of utricular hair cells. Therefore, results of this study indicate that the utricle in this vertebrate plays an auditory role in azimuth and that utricular fibers extend the response dynamic range of this species in directional hearing.     

Encoding of acoustic directional information by saccular afferents of the sleeper goby, Dormitator latifrons

This paper reports on directional response properties of saccular afferents of the sleeper goby, Dormitator latifrons, to 100-Hz acoustic particle motions with a focus on testing the hypothesis that the response directionality of a fish's auditory afferents derives from the morphological polarity of sensory hair cells in the otolithic organs. Spontaneous rates (SR) and best sensitivities (BS) of saccular afferents ranged from 0 to 162 spikes/sec and from 0.2- to 100-nm RMS displacement. SR did not vary with BS. Most saccular afferents were phase-locked to sinusoidal stimulation and had sustained temporal response patterns with some adaptation. All saccular afferents were directionally sensitive to the stimulus, and the sharpness of directional response curves was determined by a directionality index (DI). The DI ranged from 0.64 to 1.50 (mean=1.02, SE=0.02, n=100) and gradually decreased with stimulus level throughout afferents' response dynamic range. Many afferents had approximately symmetric directional response curves relative to their best response axes (BRA). BRA of most afferents remained constant with stimulus level. The BRA distribution had a peak along an axis that correlates closely with the morphological polarity of saccular hair cells. Therefore, our results strongly support the hypothesis. Accepted: 19 December 1997     

Sea snakes (Lapemis curtus) are sensitive to low-amplitude water motions

The sea snake Lapemis curtus is a piscivorous predator that hunts at dusk. Like land snakes, sea snakes have scale sensillae that may be mechanoreceptive, i.e. that may be useful for the detection of water motions produced by prey fish. In addition, inner ear hair cells of sea snakes may also be involved in the detection of hydrodynamic stimuli. We generated water motions and pressure fluctuations with a vibrating sphere. In the test range 50-200 Hz evoked potentials were recorded from the midbrain of L. curtus in response to vibrating sphere stimuli. In terms of water displacement the lowest threshold amplitudes were in the frequency range 100-150 Hz. In this range peak-to-peak water displacement amplitudes of 1.8 microm (at 100 Hz) and 2.0 microm (150 Hz) generated a neural response in the most sensitive animal. Although this low sensitivity may be sufficient for the detection of fish-generated water motions, it makes it unlikely that L. curtus has a special hydrodynamic sense.     

Acoustic response properties of single units in the torus semicircularis of the goldfish,Carassius auratus

Single units of the goldfish torus semicircularis (TS) were recorded in response to pure tones. Response areas (RA) were obtained by recording the number of spikes evoked by tones in a range of frequencies and levels within the units' dynamic range. RAs gave estimates of best sensitivity (BS), characteristic frequency (CF), most excitatory frequency at each level (BF), and Q_10dB. Peri-stimulus-time histograms (PSTH), interspike interval histograms (ISIH), and period histograms were obtained at various frequencies and levels to describe the units' temporal response patterns.The distribution of CF is nonuniform with modes at 155, 455, and 855 Hz. The distribution of the coefficient of synchronization to standard tones is also nonuniform, revealing a dichotomy between units with little or no phase-locking and those that phase-lock strongly. PSTHs for units without significant phase-locking vary widely and include patterns resembling those of the mammalian auditory brainstem. Compared with saccular afferents, torus units tend to have lower spontaneous rates, greater sensitivity, and sharper tuning. Unlike saccular afferents, BF is independent of level for most torus units. Some torus units are similar to saccular afferents while others reveal significant transformations of information between the periphery and the midbrain.Abbreviations BF best frequency - BS best sensitivity - CF characteristic frequency - ISIH inter-spike interval histogram - PSTH peri-stimulus-time histogram - RA response area - TS torus semicircularis     

Intra‐ and Intersexual swim bladder dimorphisms in the plainfin midshipman fish (Porichthys notatus): Implications of swim bladder proximity to the inner ear for sound pressure detection

The plainfin midshipman fish, Porichthys notatus , is a nocturnal marine teleost that uses social acoustic signals for communication during the breeding season. Nesting type I males produce multiharmonic advertisement calls by contracting their swim bladder sonic muscles to attract females for courtship and spawning while subsequently attracting cuckholding type II males. Here, we report intra‐ and intersexual dimorphisms of the swim bladder in a vocal teleost fish and detail the swim bladder dimorphisms in the three sexual phenotypes (females, type I and II males) of plainfin midshipman fish. Micro‐computerized tomography revealed that females and type II males have prominent, horn‐like rostral swim bladder extensions that project toward the inner ear end organs (saccule, lagena, and utricle). The rostral swim bladder extensions were longer, and the distance between these swim bladder extensions and each inner‐ear end organ type was significantly shorter in both females and type II males compared to that in type I males. Our results revealed that the normalized swim bladder length of females and type II males was longer than that in type I males while there was no difference in normalized swim bladder width among the three sexual phenotypes. We predict that these intrasexual and intersexual differences in swim bladder morphology among midshipman sexual phenotypes will afford greater sound pressure sensitivity and higher frequency detection in females and type II males and facilitate the detection and localization of conspecifics in shallow water environments, like those in which midshipman breed and nest.     

Directional encoding by fish auditory systems

This paper reviews and discusses several investigations of the peripheral neural code for the directional axis of acoustical particle motion in the saccule of two fishes: goldfish (Carassius auratus) and toadfish (Opsanus tau). Most saccular afferents are directional in the manner of hair cells, having a cosine-shaped directional response pattern. The saccular sensory epithelia are orientated almost vertically in a parasagittal plane. In the horizontal plane, these epithelia are orientated obliquely with respect to the midline. Hair-cell stereocilia project perpendicularly. Thus, directional response patterns of saccular afferents tend to be orientated in azimuth parallel to the orientation of the epithelia in the head. The oblique angle of the toadfish saccule is greater than that of the goldfish, and the range of best directions in the horizontal plane for each species reflects those differing orientations. The azimuth of acoustical particle motion could be computed by comparing the relative activation of the two saccules, as is the case for the ears of most terrestrial vertebrates. The spatial patterns of saccular hair-cell orientation of most fishes thus appear to have little function in azimuthal source location, but for toadfish are probably most important for determining the elevation of monopole sources.     

Frequency-intensity characteristics of cricket cercal interneurons: broadband units

The bilateral pairs of cercal interneurons 10-2a and 10-3a in the cricket terminal ganglion are supposed to constitute a functional system for measuring the direction of air-borne signals, based on their phase-locked responses and selective directional sensitivity. The purpose of this study was to obtain information on the frequency and intensity characteristics and thus the potential working range of this system. By recording intracellularly from the axons of the interneurons we measured responses for stimuli of varying frequency, intensity, and direction. Typically, the stimulus frequency range examined extended from 5 to 600 Hz, at intensities of 0.03–30 mm s⁻¹ (peak-to-peak air-particle velocity). The results show that interneurons 10-2a and 10-3a preserved their level of activity, response type, and direction tuning in the whole frequency range tested. Stimulus-response cross-correlograms revealed that spike trains were synchronized with stimulus waves at even higher frequencies, at least up to 1000 Hz. At a given air-particle velocity in the range of about 2–2.5 logarithmic units, the spike number responses of the interneurons were nearly constant over a wide frequency range. Directional diagrams appeared to be independent of stimulus frequency, both in orientation and in amplitude. Accepted: 14 October 1998     

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.     

Low frequency hearing in cephalopods

Summary Classical conditioning was employed to test the sensitivity of cephalopods to vibrations between 1 and 100 Hz generated in a standing wave acoustic tube. The animals were trained to associate sound stimuli with a weak electric shock, and the recorded conditioned responses were changes in breathing and jetting activity. Five specimens of Sepia officinalis were tested, and all responded to these low frequency sounds. The relevant stimulus parameter was particle motion rather than sound pressure. The threshold values (measured as particle acceleration) decreased towards lower frequencies in the tested range, reaching values below 4 × 10^-3 m/s². The thresholds in the most sensitive range may have been masked by the considerable background noise at the experimental site (Naples). Two individuals of Octopus vulgaris and one Loligo vulgaris were also tested, and showed a similar sensitivity to low frequency sound.