Randy Zelick

Lateral line system of fish

The lateral line is a sensory system that allows fishes to detect weak water motions and pressure gradients. The smallest functional unit of the lateral line is the neuromast, a sensory structure that consists of a hair cell epithelium and a cupula that connects the ciliary bundles of the hair cells with the water surrounding the fish. The lateral line of most fishes consists of hundreds of superficial neuromasts spread over the head, trunk and tail fin. In addition, many fish have neuromasts embedded in lateral line canals that open to the environment through a series of pores. The present paper reviews some more recent aspects of the morphology, behavioral relevance and physiology of the fish lateral line. In addition, it reports some new findings with regard to the coding of bulk water flow.

Intensity discrimination and the precision of call timing in two species of neotropical treefrogs

Summary1.Field acoustic playback experiments were conducted with maleEleutherodactylus coqui andE. portoricensis. Periodic tone bursts of intensities similar to natural sounds in the habitat of the frogs were used to create sonic interference. The period between tone bursts, the ‘time window’, was varied in duration and in intensity relative to the tone burst.2.Males of both species suppressed vocalizations during the stimulus tone bursts. The amount of suppression decreased as the tone burst was lengthened.3.Males of bothE. coqui andE. portoricensis suppressed calling in response to tone bursts of 0.40 to 2.0 kHz, a range which encompasses the principal frequency components present in their vocalizations.4.BothE. coqui andE. portoricensis initiated significantly (P<0.01) more calls within the time windows between stimulus tone bursts than would be expected by chance when the window duration was as short as 0.25 s and 0.10 s, respectively. These durations are approximately 10% of the spontaneous call repetition periods for each species.5.E. coqui initiated significantly (P<0.01) more calls than would be expected by chance in tone-filled time ‘windows’ which were only 4 to 6 dB less intense than the tone bursts. This ability of intensity discrimination under sonically adverse natural field conditions indicates a level of performance in the same range as that of mammals.6.The ability of frogs to call preferentially during very brief silent periods or during periods of slight intensity reductions is viewed as an adaptation for avoiding acoustic interference, and thus improves the efficiency of acoustic communication in an intense and complex sonic environment.

Analysis of acoustically evoked call suppression behaviour in a neotropical treefrog

Abstract We broadcast synthetic call notes to male Eleutherodactylus coqui treefrogs in their natural habitat. The frogs avoided acoustic overlap with relatively long duration tone stimuli by calling only within the short silent interval between tones. We also observed a temporal change in call pattern in response to tone stimuli of various frequencies and intensities. This response is the basis for construction of a behavioural auditory threshold function for this species. This function does not show a sensitivity maximum at frequencies corresponding to those in the advertisement call, and demonstrates that the frogs are capable of behaviourally responding to sounds over a frequency range which is greater than that required for detection of the species-specific vocalizations and sufficient for detection of at least one sympatric anuran species.

Characterization of the advertisement call oscillator in the frogEleutherodactylus coqui

Summary1.Eleutherodactylus coqui treefrogs spontaneously produce advertisement calls. Intercall intervals are typically between 2 and 3 s.2.When periodic tone burst stimuli were broadcast to individual frogs in the wild, their calling became entrained such that each vocalization occurred in the silent interval between stimulus tones.3.For stimulus repetition periods similar to the nominal call repetition period (2.5 s), the mode of the distribution of intercall intervals (preferred interval) matched the interstimulus interval (1∶1 locking or entrainment). The preferred interval continued to match the interstimulus interval when the latter was varied over a range of approximately 1 s, or 40% of the nominal spontaneous intercall interval. Faster stimulus rates (shorter interstimulus intervals) resulted in 1∶2 locking, in which calls were produced for every second tone burst.4.For each frog, the transition between 1∶1 and 1∶2 locking appeared to positively co-vary with the spontaneous preferred interval.5.The frogs were able to track a pseudorandom sequence of long and short duration tones. Long duration tones tended to be spanned by long intercall intervals while short duration tones were spanned with shorter intervals. Cueing to tone offset is the most parsimonious explanation for such tracking ability.6.These findings suggest that calling behavior inE. coqui is driven by an internal oscillator, the period of which may be adjusted over a considerable range in order to entrain to an external acoustic stimulus. Furthermore, the period of the oscillator may be changed within a single call cycle in response to a pseudorandom sequence of stimuli.

The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.

BEHAVIORAL EVIDENCE OF A LATENCY CODE FOR STIMULUS INTENSITY IN MORMYRID ELECTRIC FISH

Mormryid electric fish (Gnathonemus petersii) respond to novel stimuli with an increase in the rate of the electric organ discharge (EOD). These novelty responses were used to measure the fishs ability to detect small changes in the amplitude and latency of an electrosensory stimulus. Responses were evoked in curarized fish in which the EOD was blocked but in which the EOD motor command continued to be emitted. An artificial EOD was provided to the fish at latencies of 2.4 to 14.4 ms following the EOD motor command.Novelty responses were evoked in response to transient changes in artificial EOD amplitude as small as 1% of baseline amplitude, and in latency as small as 0.1 ms. Changes in latency were effective only at baseline delays of less than 12.4 ms.The sensitivity to small changes in latency supports the hypothesis that latency is used as a code for stimulus intensity in the active electrolocation system of mormyrid fish. The results also indicate that a corollary discharge signal associated with the EOD motor command is used to measure latency.

Sex recognition and neuronal coding of electric organ discharge waveform in the pulse-type weakly electric fish, Hypopomus occidentalis.

Summary1.Hypopomus occidentalis, a weakly electric gymnotiform fish with a pulse-type discharge, has a sexually dimorphic electric organ discharge (Hagedorn 1983). The electric organ discharges (EODs) of males in the breeding season are longer in duration and have a lower peak-power frequency than the EODs of females. We tested reproductively mature fish in the field by presenting electronically generated stimuli in which the only cue for sex recognition was the waveshape of individual EOD-like pulses in a train. We found that gravid females could readily discriminate male-like from female-like EOD waveshapes, and we conclude that this feature of the electric signal is sufficient for sex recognition.2.To understand the possible neural bases for discrimination of male and female EODs byH. occidentalis, we conducted a neurophysiological examination of both peripheral and central neurons. Our studies show that there are sets of neurons in this species which can discriminate male or female EODs by coding either temporal or spectral features of the EOD.3.Temporal encoding of stimulus duration was observed in evoked field potential recordings from the magnocellular nucleus of the midbrain torus semicircularis. This nucleus indirectly receives pulse marker electroreceptor information. The field potentials suggest that comparison is possible between pulse marker activity on opposite sides of the body.4.From standard frequency-threshold curves, spectral encoding of stimulus peak-power frequency was measured in burst duration coder electroreceptor afferents. In both male and female fish, the best frequencies of the narrow-band population of electroreceptors were lower than the peak-power frequency of the EOD. Based on this observation, and the presence of a population of wide-band receptors which can serve as a frequency-independent amplitude reference, a slope-detection model of frequency discrimination is advanced.5.Spectral discrimination of EOD peak-power frequency was also shown to be possible in a more natural situation similar to that present during behavioral discrimination. As the fishs EOD mimic slowly scanned through and temporally coincided with the neighbors EOD mimic, peak spike rate in burst duration coder afferents was measured. Spike rate at the moment of coincidence changed predictably as a function of the neighbors EOD peak-power frequency.6.Single-unit threshold measurements were made on afferents from peripheral burst duration coder receptors in the amplitude-coding pathway, and midbrain giant cells in the time-coding pathway. The amplitude-coding pathway was more sensitive to a transverse signal mimicking the EOD of a neighbor than the time-coding pathway, despite, in the latter case, increased convergence at the midbrain level.7.Measurements of the sensitivity and spectral tuning characteristics of afferents from burst duration coder electroreceptors show that elements of the amplitude-coding pathway, when considered on a population level, are capable of encoding EOD peak-power frequencies to the extent necessary to account for our behavioral observations. We conclude thatH. occidentalis has the capability to discriminate male from female EOD pulse shape using both temporal and spectral cues, but that frequency discrimination based on spectral tuning of electroreceptors is the most likely neuronal mechanism.

Temporary threshold shift, adaptation, and recovery characteristics of frog auditory nerve fibers

While recording from single auditory nerve fibers in a frog, a monaural 3 min pure tone stimulus at CF was used to induce temporary threshold shift (TTS). TTS magnitude was correlated with the exposure tone intensity relative to the pre-exposure best threshold of the neuron, but not with exposure tone absolute intensity. CF and spontaneous spike rate were also uncorrelated with TTS magnitude. Comparison of frequency-threshold curves (FTCs) made before and successively after exposure revealed either a maximum sensitivity loss at the tip of the FTC or an equal shift at all frequencies. Neurons tended to recover from TTS within 3 min post-exposure, regardless of the initial TTS. Thus, recovery from TTS was more rapid for larger shifts. Recovery dynamics followed single or a double negative exponential functions.

Behavioral detection of electric signal waveform distortion in the weakly electric fish, Gnathonemus petersii

The “novelty response” of weakly electric mormyrids is a transient acceleration of the rate of electric organ discharges (EOD) elicited by a change in stimulus input. In this study, we used it as a tool to test whether Gnathonemus petersii can perceive minute waveform distortions of its EOD that are caused by capacitive objects, as would occur during electrolocation. Four predictions of a hypothesis concerning the mechanism of capacitance detection were tested and confirmed: (1) G. petersii exhibited a strong novelty response to computer-generated (synthetic) electric stimuli that mimic both the waveform and frequency shifts of the EOD caused by natural capacitive objects (Fig. 3). (2) Similar responses were elicited by synthetic stimuli in which only the waveform distortion due to phase shifting the EOD frequency components was present (Fig. 4). (3) Novelty responses could reliably be evoked by a constant amplitude phase shifted EOD that effects the entire body of the fish evenly, i.e., a phase difference across the body surface was lacking (Figs. 3, 4). (4) Local presentation of a phase-shifted EOD mimic that stimulated only a small number of electroreceptor organs at a single location was also effective in eliciting a behavioral response (Fig. 5).Our results indicate that waveform distortions due to phase shifts alone, i.e. independent of amplitude or frequency cues, are sufficient for the detection of capacitive, animate objects. Mormyrids perceive even minute waveform changes of their own EODs by centrally comparing the input of the two types of receptor cells within a single mormyromast electroreceptor organ. Thus, no comparison of differentially affected body regions is necessary. This shows that G. petersii indeed uses a unique mechanism for signal analysis, which is different from the one employed by gymnotiform wavefish.

The effect of sound level, temperature and dehydration on the brainstem auditory evoked potential in anuran amphibians

Brainstem auditory evoked potentials (BAEPs) were used to examine the effects of sound level, temperature, and dehydration on the auditory pathway of three species of anuran amphibians: Rana pipiens, Bufo americanus and B. terrestris. BAEP latency, amplitude and a measure of threshold were determined for all stimulus and test conditions. Threshold values obtained with this technique were similar to other neural measures of threshold in anurans, and were stable for repeated measures within 12 h and over three days. Transient changes in temperature caused non-linear changes in BAEP threshold and latency. Above 20 degrees C small threshold shifts were elicited, while below 20 degrees C we observed rapid deterioration of threshold. Animals acclimated to a cold temperature (14 degrees C) were acoustically less sensitive than warm (21 degrees C) animals, even when both groups were tested at colder temperatures. Because peripheral components of the BAEP were most affected by both transient and acclimation (longer term) cooling and warming, the sensory epithelium appears to be the most temperature-sensitive component of the auditory pathway. Dehydrated frogs showed no auditory dysfunction until a critical level of dehydration was reached. More dehydration-resistant species (B. terrestris and B. americanus) were less susceptible to BAEP degradation near their critical dehydration level.