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Auditory encoding during the last moment of a moth's life

James H. Fullard^1,*, Jeff W. Dawson^1, and David S. Jacobs²

¹ Department of Biology, Erindale College (University of Toronto), 3359 Mississauga Road, Mississauga, Ontario Canada L5L 1C6
² Department of Zoology, University of Cape Town, Cape Town, South Africa
Present address: Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK

View larger version (18K): [in a new window]   Fig. 1. Oscillograms of the auditory response of the arctiid, Hyphantria cunea, to single 20 ms bursts of ultrasound, illustrating how the three receptor cell action potentials were distinguished from each other. (A) A long-time sample reveals the regularity of the non-tympanal B cell as well as its higher amplitude. (B) A shorter time sample shows the variety of waveforms encountered when the two auditory receptors (A1 and A2) respond to an intense sound burst (the B cell is not present in this trace). The different amplitudes of the compound action potential formed by the firing of the A1 and A2 cells is due to the slightly changing phase relationship of the two cells as they fire. The apparent amplitude modulation of the 90 dB burst is due to the insufficient digital sampling used in creating the figure, but was not present in the stimuli used for the auditory trials.

View larger version (28K): [in a new window]   Fig. 2. Auditory sensitivity curves (audiograms) of the moths examined in this study. Each curve is the median of five individuals.

View larger version (27K): [in a new window]   Fig. 3. Intensity response curves of the auditory nerve receptors for the species of moths in our study. (A) In each graph the median (+75% quartiles) A cell periods to pulsed stimuli at each intensity are illustrated, the median A1 threshold is indicated above the first bar. Filled bars, A1 cells; open bars, A2 cells. The total numbers (lines) of A1 (filled circles) and A2 (open circles) action potentials for each stimulus intensity (dB SPL) were normalised and plotted as a fraction of the intensity producing the most spikes. (B) Median B cell periods were measured during the pulsed stimulus exposures that were used to examine A1 and A2 cell responses.

View larger version (28K): [in a new window]   Fig. 4. Representative trace of an auditory response of the moth Hyphantria cunea to the recorded echolocation attack sequence of Eptesicus fuscus. (A) The entire playback sequence with the attack stages of approach and terminal buzz as defined by Kick and Simmons (1984) and Surlykke and Moss (2000). The asterisk over call 20 indicates the call of maximum amplitude that was adjusted to produce a 94 dB (peSPL) intensity, matching that of the original recording. (B—D) The lines beneath the sequence have been enlarged in the subsequent traces to illustrate the moth's auditory response to: (B) the approach stage, (C) the initial and (D) end portions of the terminal buzz stage. Spike instantaneous periods (IPs) were calculated as the time from one A1 or A2 spike to the next. The traces of the echolocation calls appear distorted due to the insufficient digital sampling used to create the illustration, but the signals used for the playback trials were analog and not distorted.

View larger version (31K): [in a new window]   Fig. 5. The instantaneous B cell periods before, during and after exposures to the recorded bat attack sequence. Each colour represents a different individual.

View larger version (32K): [in a new window]   Fig. 6. Auditory receptor responses for the single A1 cell in the two notodontid moths of our study. For each species, the top graph shows all of the instantaneous A1 cell periods for each individual plotted (as separate colours) to the recorded bat attack sequence (marked as vertical lines). The time scale begins at the beginning of the first bat echolocation call. The median A1 periods measured for the pulsed intensity response trials at both threshold and 70 dB stimulus intensities (Fig. 3) are indicated as horizontal lines. For each species the bottom graph shows the median number of A1 cell spikes (APs) to each of the bat echolocation calls up to the point where encoding ceases (determined visually). After this point firing continues but in a non-bursting, continual pattern. The median spike (AP) numbers are also represented as normalised fractions of the maximum counts (thick lines).

View larger version (28K): [in a new window]   Fig. 7. The instantaneous A1 and A2 spike periods and total number of spikes elicited to the recorded bat attack sequence in the most sensitive moth we tested, the noctuid Leucania pseudargyria. Filled bars, A1 cell spikes; open bars, A2 cell spikes. For further details, see Fig. 6.

View larger version (23K): [in a new window]   Fig. 8. The instantaneous A1 and A2 spike periods and total number of spikes elicited to the recorded bat attack sequence in the arctiid moth, Hyphantria cunea. Filled bars, A1 cell spikes; open bars, A2 cell spikes. For further details, see Fig. 6.

View larger version (19K): [in a new window]   Fig. 9. Oscillogram of the auditory (top trace) and tymbal response (bottom trace) in the sound-producing moth, Cycnia tenera. (A) At a pulsed stimulus of 80 dB, only the A1 auditory cell is evoked to the sound; (B) at 90 dB, both A1 and A2 receptors fire. B, B cell. In extracellular recordings the large compound action potentials of the tymbal nerve can be indirectly recorded at the tympanic nerve and are seen as alternating spikes produced by the right (R) and left (L) tymbal motor nerves.

View larger version (27K): [in a new window]   Fig. 10. Instantaneous A1 and A2 cell spike periods for the sound-producing arctiid moth Cycnia tenera, when acoustically stimulated by the bat attack sequence delivered at an intensity that: (A) does not evoke a tymbal response and, (B) does evoke a tymbal response (tymbal motor nerve compound action potentials are indicated in B as inverted triangles). For further details, see Fig. 6.