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Rebound excitation (Off-responses) following non-neural suppression in the cochleas of echolocating bats

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Summary

Auditory nerve evoked potential responses (N1) occur at the termination of tone pips as well as the onset in several species of bats that emit orientation sounds having a constant frequency component of several msec duration.

  1. 2.

    These “off”-responses are present only in a narrow band of frequencies around the emitted constant frequency. The “on”-response is most sensitive at slightly lower or higher frequencies and shows a relative null at the best frequency for the “off” (Fig. 2).

  2. 3.

    The “off”-response is similar in waveform to the “on” response, and follows the termination of a tone pip with a latency (0.9 ±0.1 msec) indistinguishable from that with which the “on”-response follows the onset of the signal (Fig. 1).

  3. 4.

    “Off”-responses are seen at signal durations as short as 0.5msec and are typically maximal with a signal duration of only 2 msec. Summation of “on” and “off” responses at durations shorter than 1.5 msec suggests that separate populations of units are contributing to the two responses.

  4. 5.

    Many single units at higher neural levels respond only to the “off ” of a signal of the frequency that produces an N1 “off ” evoked potential, and only to the onset of a slightly lower frequency that produces a maximal “on” evoked potential (Fig. 3).

  5. 6.

    A frequency that produces “off”-responses can either suppress or enhance the “on”-response to a lower frequency tone pip, depending on the relative intensity of the two sounds (Fig. 4). The suppression probably represents a form of two-tone inhibition comparable to that seen in other mammals. Similar enhancement has not been reported in other mammals, however. The “off”-response appears to represent rebound excitation of cells tuned to slightly lower frequencies than the suppressant tone.

  6. 7.

    The “off”-response is most sensitive to masking by frequencies that elicit maximal “on”-responses, well below those that produce a maximal “off”-response (Fig. 5).

  7. 8.

    It is concluded that the suppression is unlikely to be mediated by chemical neural inhibition. The properties of the “off” response appear compatible with a mechanism whereby vibration of a certain part of the basilar partition causes an electrical or mechanical bias that reduces spontaneous activity in a population of primary fibers innervating an adjacent part of the partition, possibly by reducing tonic hair cell transmitter release, with termination of this suppression resulting in synchonous resumption of spontaneous firing at normal or greater than normal rate.

  8. 9.

    The apparent function of this interaction in the constant frequency emitting bats is a peripheral sharpening of frequency resolution, and a “sensitization” of primary afferent pathways to the lower frequencies of the downward sweep at the end of the emitted pulses.

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It is a pleasure to acknowledge the participation of Dr. S. Hagiwara in many of the experiments on which this paper is based, and to express my gratitude to Drs. Hagiwara, R. Eckert, R. Orkand, and V. Honrubia for helpful criticisms of the manuscript. This research was supported by USPH grant NS 06232 and by the NSF under grant GB 8400 for operation of the Alpha Helix research program.

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Grinnell, A.D. Rebound excitation (Off-responses) following non-neural suppression in the cochleas of echolocating bats. J. Comp. Physiol. 82, 179–194 (1973). https://doi.org/10.1007/BF00696152

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