Frequency and time domain comparison of low-frequency auditory fiber responses in two anuran amphibians.

A comparative study of the phase-locked response of auditory nerve fibers was performed in two frog species, Eleutherodactylus coqui and Bombina orientalis. From the tuning characteristics and phase response of single auditory nerve fibers to low frequency tones (0.08-1.0 kHz) we attempt to deduce the mechanics of the auditory organ responsible for low-frequency hearing in the frog, the amphibian papilla (a.p.). The phase-locked responses of auditory nerve fibers in B. orientalis were essentially identical to those from cells with similar CFs in E. coqui, despite the presence of a conspicuous caudal extension of the a.p. in E. coqui (an apparently derived morphology), a feature completely absent in B. orientalis. The fine structure of the frequency-dependent phase behavior was examined in both species with a residual phase analysis. The most significant non-linear phase behavior was confined to neurons with CFs less than 0.3 kHz. The intensity dependence of the phase response in E. coqui revealed that the preferred firing phase of an auditory nerve fiber depends upon the relation of test frequency (TF) and CF of the neuron examined. For TFs greater than CF there was a progressive phase lag as stimulus level was increased; the inverse was true for TFs less than CF. Click latencies measured in E. coqui were inversely related to CF and were similar though systematically shorter than the response latencies estimated from the phase-frequency functions. The click response was similar to that documented in other species, showing a significant level dependence and the presence of multiple peaks, with the time between peaks related to the period of the neuron's CF. A 'neurogram' was compiled for a.p. fiber responses in both species in response to several pure tones. Based on the known tonotopy of the a.p. this measure reflects the phase response of the a.p. over the extent of its length. The population phase response in anurans is quite similar to that obtained from mammalian auditory nerve fibers for the same range of test frequencies (0.08-1.0 kHz). The similarity between the responses of auditory fibers in these two anuran species suggests the micromechanics of the a.p. rostral to the tectorial curtain is similar in both species and that it is the likely site for the origin of the CF-dependent time delays.

Neurophysiological evidence for a traveling wave in the amphibian inner ear.

In response to low-frequency sounds (less than 1.0 kilohertz) auditory nerve fibers in the treefrog, Eleutherodactylus coqui, discharge at a preferred phase of the stimulus waveform which is a linear function of the stimulus frequency. Moreover, the slopes of the phase-versus-frequency functions (equivalent to the system time delays) systematically increase as the characteristic frequency of the fibers decreases. These neurophysiological observations, coupled with the known tonotopy of the amphibian papilla suggest that a traveling wave occurs in the inner ear of frogs despite the absence of a basilar membrane. Electrical tuning may contribute to these characteristic frequency-dependent delays.

Detection of amplitude-modulated tones by frogs: implications for temporal processing mechanisms.

The whole nerve action potential (AP) from the auditory nerve and midbrain averaged evoked potential (AEP) were recorded in Hyla chrysoscelis and H. versicolor in response to synthesized amplitude-modulated stimuli with variable modulation frequencies (Fm). The AP from these frogs is similar to the potential described for mammals and showed a bandpass characteristic in its ability to follow sinusoidally amplitude-modulated (AM) sound stimuli. A lesioning study suggests that the midbrain AEP is a localized neural response of neurons near the ventral border of the torus semicircularis. The AEP is a complex waveform consisting of fast and slow components. The fast component encodes the temporal structure of acoustic stimuli and is used to measure temporal sensitivity in these two species. The AEP behaves like a low-pass filter with a cutoff frequency of 250 Hz when tracking AM signals. Threshold for detection requires a modulation depth of 8-12% of the total stimulus amplitude (delta I = 1.5-2.0 dB). Relative to the eighth nerve AP, the AEP displays an enhanced coding of AM signals when Fm less than 100 Hz, and a slightly inferior ability to code Fm above 250 Hz. The AEP reflects only that portion of the neural response that encodes amplitude fluctuations. In comparison to the range of amplitude fluctuations coded by single units in the rat inferior colliculus or by human evoked potential, the frog AEP codes higher rates of Fm. The proposal that these frogs process AM stimuli solely on the basis of amplitude fluctuations, and do not use spectral cues at higher modulation frequencies is considered. The AM sensitivity of the AEP, which encompasses most biologically relevant rates of amplitude fluctuation for the animal, and the limited frequency resolution of the periphery, lend support to this proposal. However, convergent spectral processing at higher auditory centers cannot be excluded by this study. Psychophysical tests will be required to determine whether both of these mechanisms may be operating during temporal information processing in anurans.

Representation of sound pressure and particle motion information in the midbrain of the goldfish.

1. Averaged evoked responses from multiple electrodes in the goldfish midbrain (torus semicircularis) area were recorded in response to acoustic stimulation by loudspeaker and to direct vertical vibration of the head. 2. Relative pressure and displacement sensitivity was such that in the far field, the response to sound pressure would dominate the response to particle motion by 40-90 dB. 3. Swimbladder deflation caused a flat (70-1000 Hz) loss in pressure sensitivity ranging from 20 to over 50 dB, and led to an enhanced response to vibration at low frequencies. 4. The goldfish midbrain is not homogeneous with regard to relative pressure and motion sensitivity.