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The frequency response of primary saccular afferents of toadfish (Opsanus tau) was studied in the time and frequency domains using the reverse correlation (revcor) method. Stimuli were noise bands with flat acceleration spectra delivered as whole-body motion. The recorded acceleration waveform was averaged over epochs preceding and following each spike. This average, termed the revcor, is an estimate of the response of an equivalent linear filter intervening between body motion and spike initiation. The spectrum of the revcor estimates the shape of the equivalent linear filter. Revcor responses were brief, damped oscillations indicative of relatively broadly tuned filters. Filter shapes were generally band-pass and differed in bandwidth, band edge slope, and characteristic frequency (74 Hz to 140 Hz). Filter shapes tend to be independent of stimulus level. Afferents can be placed into two groups with respect to characteristic frequency (74-88 Hz and 140 Hz). Some high-frequency afferents share a secondary peak at the characteristic frequency of low-frequency afferents, suggesting that an afferent may receive differently tuned peripheral inputs. For some afferents having similar filter shapes, revcor responses often differ only in polarity, probably reflecting inputs from hair cells oriented in opposite directions. The origin of frequency selectivity and its diversity among saccular afferents may arise from a combination of hair cell resonance and micromechanical processes. The resulting frequency analysis is the simplest yet observed among vertebrate animals. During courtship, male toadfish produce the 'boatwhistle' call, a periodic vocalization having several harmonics of a 130 Hz fundamental frequency. The saccule encodes the waveform of acoustic particle acceleration between < 50 and about 250 Hz. Thus, the fundamental frequency component of the boatwhistle is well encoded, but the successive higher harmonics are filtered out. The boatwhistle is thus encoded as a time-domain representation of its fundamental frequency or pulse repetition rate.

The displacement sensitivity, frequency response, and directional response properties of primary saccular afferents of toadfish (Opsanus tau) were studied in response to a simulation of acoustic particle motion for which displacement magnitudes and directions were manipulated in azimuth and elevation. Stimuli were 50, 100, and 200 Hz sinusoidal, translatory oscillations of the animal at various axes in the horizontal and midsagittal planes. Thresholds in these planes defined a cell's characteristic axis (the axis having the lowest threshold) in spherical coordinates. Recordings were made from afferents in rostral, middle, and caudal bundles of the saccular nerve. The most sensitive saccular afferents responded with a phase-locked response to displacements as small as 0.1 nm. This sensitivity rivals that of the mammalian cochlea and is probably common to the sacculi and other otolith organs of most fishes. Most afferents showed lower thresholds at 100 Hz than at 50 or 200 Hz. Eighty percent of afferents have three-dimensional directional properties that would be expected if they innervated a group of hair cells having the same directional orientation on the saccular epithelium. Of the afferents that are not perfectly directional, most appear to innervate just two groups of hair cells having different orientations. The directional characteristics of afferents are qualitatively correlated with anatomically defined patterns of hair cell orientation on the saccule. In general, azimuths of best sensitivity tend to lie parallel to the plane of the otolith and sensory epithelium. Elevations of best sensitivity correspond well with hair cell orientation patterns in different regions of the saccular epithelium. Directional hearing in the horizontal plane probably depends upon the processing of interaural differences in overall response magnitude. These response differences arise from the gross orientations of the sacculi and are represented, in part, as time differences among nonspontaneous afferents that show level-dependent phase angles of synchronization. Directional hearing in the vertical plane may be derived from the processing of across-afferent profiles of activity within each saccule. Fishes were probably the first vertebrates to solve problems in sound source localization, and we suggest that their solutions formed a model for those of their terrestrial inheritors.

A stimulus generalization paradigm was used with classical respiratory conditioning to study analytic listening in the goldfish. Animals were first conditioned to suppress respiration upon the presentation of a long-duration complex sound comprised of two sinusoidal components, 166 and 724 Hz. Conditioned animals were then presented with a set of eight novel test tones with frequencies between 95 and 1514 Hz, and including 166 and 724 Hz. Response magnitudes were greatest at the frequencies of the components making up the complex to which the animals were initially conditioned. This is a demonstration that the goldfish had acquired independent information about the frequencies of the individual sinusoidal components making up a complex sound, and thus had listened to the complex analytically. To my knowledge, this is the first demonstration of simultaneous frequency analysis and analytic listening by a nonhuman animal, and suggests that this fundamental aspect of human hearing may be a primitive character shared with the fishes and perhaps with all living vertebrates.

Temperature change and hypoxia produce consistent, reversible effects on the response of single auditory nerve fibers in the goldfish. Cooling and hypoxia produce reductions of a cell's spontaneous activity, sensitivity, most excitatory or best frequency (BF) at a given signal level, and overall responsiveness to acoustic stimulation. Warming above ambient temperatures increases a cell's spontaneous activity, sensitivity, BF, and responsiveness. Adaptation, or the tendency for responsiveness to decline with time during a stimulus, increases during hypoxia and cooling, and decreases during warming. The effects of temperature change and hypoxia on a fiber's BF are similar to the effects of overall sound level. Since BF normally increases with sound level, the BF-shift with temperature change and hypoxia can be understood as a change in sensitivity or the overall effectiveness of a stimulus at a given sound level. The effects on neural response of temperature change and hypoxia are probably due in part to changes in the release and replenishment of neurotransmitter at the synapses between hair cells and auditory nerve fibers.

The responses of single fibers of the auditory nerve of the goldfish (Carassius auratus) were recorded in response to two tones of different duration (20 ms 'signals' and 200 ms 'maskers') presented simultaneously or non-simultaneously. A single tone may produce excitation, adaptation, and suppression in auditory nerve fibers. For fibers with characteristic frequencies (CF) in the 200 to 400 Hz range, frequencies well above CF tend to produce suppression. If the net response to the masker tone is excitation, an added excitatory signal tone tends to increment the response in a way predictable from the rate-level function for the masker. A masker can attenuate the response to a signal as a result of a compressive and saturating response to the masker, and as a result of a low signal-to-masker ratio. If the net response to a masker tone is suppression, it effectively subtracts from signal excitation, causing 'suppressive masking.' In non-spontaneous fibers, suppression, additive excitatory effects, and adaptation can be revealed by responses to the signal in the absence of spike responses to the masker. In general, the ability of one tone (the masker) to reduce the response to a second tone (the signal) is greater in non-spontaneous fibers than in spontaneous fibers. These results also show that estimates of the frequency selectivity of many goldfish auditory nerve fibers will depend on whether the response of the fiber is defined by excitation, suppression, or both. The response of many fibers with CF in the 200-400 Hz region, as defined by excitation, can be masked or suppressed by a broad range of frequencies covering the effective hearing range of the goldfish.

The suppression of background spike activity in the absence of deliberate acoustic stimulation occurs in fibers of the goldfish saccular nerve tuned in the region of 250 Hz. Suppression is most robust in the frequency range between 450 and 1050 Hz, the range of CF for the mid- and high-frequency saccular fibers. Suppression of background activity tends to occur following the suppressor tone offset ('off-suppression'), even though the spike response during the suppressor is below the background rate. This suggests that the suppressor tone is excitatory at the level of the hair cells and their synapses onto saccular afferents. Tones at the low- frequency edge of the suppression region may show net excitation at low intensity levels, and net suppression at higher levels. This suggests that the spike response observed is the result of the relative strengths of excitatory and suppressive effects which operate simultaneously. The magnitude and frequency of best suppression tends to increase with stimulus intensity. A suppressing tone produces transient excitation at onset. In fibers with high levels of spontaneous activity, a spike response 'rebound' often occurs 20 to 50 ms following the suppressing tone offset. These 'on' and 'off' effects are not due to energy 'splatter' in the stimulus domain. Suppression by tones can also be observed in non-spontaneous fibers when the background spike activity is evoked by noise. In these cases, however, off-suppression following a suppressed response and the 'rebound' seldom occurs. Possible sites of suppression are the hair cells and their synapses, the spike-initiation zones of the saccular afferents, and efferent inhibition. The most likely site seems to be the spike-initiation zones of saccular afferents. An important consequence of suppression for hearing is the sharpening of frequency response areas for low frequency fibers, and the partial preservation of frequency analysis in saccular fibers stimulated well above threshold.

The psychophysics and neurophysiology of repetition noise (RN) processing was studied in the goldfish. RN is the sum of a noise waveform with its delayed (by T s) repetition, which may be attenuated (by A dB), and inverted relative to the undelayed signal. Such a signal has a periodic spectrum with peaks separated by 1/T Hz, and a prominence in its autocorrelation function at T s. In usual environments, RN contains information about sound-reflecting surfaces. Delays in the range of 0.5-20 ms create pitch sensations in man. Psychophysical experiments using classical respiratory conditioning investigated the masking effectiveness of RN on tones, the detection of changes in delay (T) at various values of T, A and overall noise level, and the values of A required to bring a 20% delay discrimination to threshold. While the masking data define detection filters quite broadly tuned compared with man, various measures of delay discrimination are comparable to those for man. Unit responses from the auditory nerve are consistent with broadly tuned psychophysical filters, but in all cells studied show prominent inter-spike-interval (ISI) peaks which predict the delay values used to generate the RN. We conclude that the qualitative features of RN are coded in ISIs, and are processed by the CNS in the time domain. Similar mechanisms may be used by other vertebrate species in processing repetition noise.

Psychophysical data on unspecialized mammals commonly used in auditory research were compiled from the literature, and an attempt was made to compare the hearing capacities of these species with man. Binaural hearing and sound localization were not considered. The most complete psychoacoustic data exist for chinchilla, cat, various primates, and the mouse. The existing data include audiograms, frequency and intensity discrimination thresholds, critical masking ratios, critical bandwidths, temporal summation functions at threshold, psychophysical tuning curves, gap detection thresholds, temporal modulation transfer functions, temporal discriminations, and auditory filter shapes. In general, the qualitative forms of most all psychoacoustic functions for these mammals are similar to those for man, and there is little reason to believe that the mechanisms underlying these capacities are different across mammals. Although the discriminative capacities of humans are generally more acute than those of non-humans, the database on the capacities of non-humans is not yet sufficient for systematic comparisons across species to be made with confidence.

The ability of goldfish to detect the presence of amplitude modulations (AM) impressed on 200, 570 and 800 Hz tones was measured under stimulus conditions producing intermittent, short-term adaptation and continuous, long-term adaptation. Sensitivity to AM under intermittent conditions increased as a function of modulation rate, with thresholds of AM detection occurring between 10 and 25% modulation at 10 Hz and around 2% modulation at 100 Hz. AM sensitivity was independent of carrier frequency and did not change under randomly varying intensity changes. Under long-term adaptation, thresholds of AM detection ranged from 1.3% at 100 Hz to 2.1% at 10 Hz, showing increased sensitivity and less dependence on modulation rate. The effects of overall intensity on AM sensitivity were the same for both conditions, with sensitivity being relatively independent of overall signal level at 10 Hz modulation and dependent on level at 100 Hz. The responses of goldfish auditory neurons to modulated and unmodulated signals were measured under stimulus conditions similar to those for behavioral studies. Single saccular neurons responded to modulated signals with both an increase in average rate above that evoked by the unmodulated signal and with phase-locking to the AM envelope. Rate increments and phase-locking responses were observed in neurons showing significant short-term adaptation to the unmodulated signal, whereas neurons showing no increase in rate or synchronization to the AM envelope showed little or no adaptation to the unmodulated signal. The effects of overall intensity, modulation rate and adaptation duration on neural responses were similar to behaviorally measured effects. These results show that adaptation affects AM detection and that phase-locking to the AM envelope is the most likely basis for behavioral detection.

The psychophysics and neurophysiology of sound detection in quiet and under noise masking were studied in goldfish. Psychophysical masking is a linear function of masker level. For long duration signals, signal-to-noise ratios (S/N) at threshold are 15.5, 19, and 22.5 dB for 200, 400 and 800 Hz signals, respectively, and is -5 dB for a noise signal. Threshold declines with signal duration to about 700 ms. The slopes of the masked temporal summation functions are about unity, indicating that energy is constant at threshold. In quiet however, the slopes are generally less than 0.5, indicating that shorter signals are detected at lower energy. Neural correlates of the masked S/Ns and the slopes of temporal summation functions were sought in the response patterns of single saccular neurons. Rate- and synchronization-intensity functions were obtained for tone and noise signals in quiet and in noise. S/Ns at behavioral threshold correspond closely to those required to raise spike rate just above that evoked by the masker alone, but are well above those required to cause clear synchronization. Therefore, sound detection is probably based on spike rate and not synchronization criteria. The equivalence of behavioral and neural thresholds indicates that the filters used in behavioral sound detection are simply the bandwidths of saccular fibers. A model outlined by Zwislocki which predicts the rate of temporal summation from the rate of growth of neural activity with intensity accounts quite well for the observed slopes of temporal summation functions both in quiet and in noise.