The detection of pressure fluctuations, sonic audition, is the dominant mode of dipole-source detection in goldfish (Carassius auratus)

Abstract

Behavioral detection of a low-frequency (40 Hz) vibratory dipole at source distances of 1.5-24 cm was measured by classically conditioned respiratory suppression in goldfish (Carassius auratus). Detection thresholds were compared across distances and before and after ablation of individual octavolateralis sensory channels. Detection thresholds, expressed in units of pressure (SPL), remained roughly constant as distance between the stimulus source and animal increased. Lateral line inactivation, using CoCl2, had no measurable effect on sensitivity, although some other results can be construed as weak evidence for a small contribution of the lateral line to dipole detection when source distances are <or=6 cm (<1 body length). Gas bladder deflation resulted in a large increase in threshold (17 dB), demonstrating that the gas bladder contributes to audition at low frequencies. The present study confirms an auditory role for the gas bladder-enhanced inner ear of goldfish in the detection of low-frequency vibratory sources. Sonic audition (detection of pressure fluctuations) appears to be the dominant mode of dipole-source detection for goldfish when measured by conditioned behaviors in psychophysical experiments.

Figure 1

Schematic diagram of the experimental arena, vibration isolation table, positioning system slides (x and y axes) and the vibrator (minishaker)/dipole complex. Also depicted are the wire mesh electrodes used to deliver the unconditioned stimulus and the carbon-rod electrodes used to monitor the animal's respiration.

Figure 2

Respiratory waveforms of a single animal during four stimulus presentations. Each trace represents the respiration occurring during a single trial, indicated at the left of the figure. The first 5 s of each trial is designated as the “Pre” period. The conditioned stimulus (CS) is presented during the next 5-s period, as shown schematically at the bottom. The last CS tone burst is immediately followed by the unconditioned stimulus (US; shock), indicated by the upward pointing arrow. The corresponding suppression ratio (SR) for each trial is shown on the right. The large oscillations during the first second following the US (shock) are artifacts of the relay protecting the amplifier.

Figure 3

Suppression ratios from a single animal plotted as a function of trial number, over the course of a single training session. Each data marker represents the animal's suppression ratio for a given trial. The horizontal dashed line represents the .40 suppression ratio criterion for detecting and responding to the conditioned stimulus. The sloped line is the regression line, y = − .011(x) + .62, calculated for the 40 data points.

Figure 4

Behavioral responses plotted as a function of signal attenuation and trial number during the first detection test session for a representative animal. Two successive correct detections of the same test stimulus resulted in a 3-dB decrease of signal strength for the next stimulus presentation. Any failure to detect a single test stimulus resulted in an increase of 3 dB for the next stimulus presentation. Reversals in the trend of responding and signal amplitude are marked by arrows. Twelve reversals are shown in this test session.

Figure 5

Sound pressure level at the threshold of detection using a pulsed 40-Hz vibratory stimulus, plotted as a function of distance from the animal. The bold line and solid black markers represent the average for groups of animals tested at 1.5, 3, 6, 12, and 24 cm. Open circles represent thresholds for individual animals tested at each location. Some markers represent multiple animals with identical thresholds and these are indicated with the numbers of individuals to the right of each marker.

Figure 6

Hydrophone records (at the position of the fish) for (panels A and B) both the 95- dB dipole stimulus (polyvinyl bead and shaft) and for (panels C–H) the minishaker- alone source (with the shaft and bead removed) at three source levels (85–95 dB). The corresponding amplitude spectra are shown to the right of each hydrophone recording. The minishaker was positioned in the 3-cm position.

Figure 7

Mean detection thresholds for a 40-Hz pulsed dipole source consisting of a minishaker attached to a shaft and bead within the water (open bars) in comparision with thresholds for a source that consisted of the minishaker alone, without a shaft in the water (solid bars). At the 3-cm and 6-cm distances there was a significant difference (asterisk) between these conditions. There was no significant difference between positions in the minishaker-alone condition. Error bars represent ±1 SEM. Note that responses to the in-water source (open bars) are replotted from Figure 5.

Figure 8

Sound pressure level thresholds, for detection of a pulsed 40-Hz vibratory stimulus, plotted as a function of distance from the animal and lateral line condition. N = 4. Error bars represent ± 1 SEM.

Figure 9

Behaviorally determined detection thresholds for a 40-Hz vibratory stimulus situated 6 cm from the animal. The same group of animals was used in each condition. N = 4 for all groups shown. The dotted line represents the previously obtained detection threshold for animals used in Experiment 1. Error bars represent ± 1 SEM.