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Biol. Bull. 203: 195-196. (October 2002)
© 2002 Marine Biological Laboratory

Preliminary Evidence for Interpulse Interval Selectivity of Cells in the Torus Semicircularis of the Oyster Toadfish (Opsanus tau)

Richard R. Fay and Peggy L. Edds-Walton

Marine Biological Laboratory, Woods Hole, Massachusetts 02543 and Loyola University Chicago, Chicago, Illinois 60626

Both the grunt and the boatwhistle sounds of toadfish are a series of rapidly produced sound pulses. These sounds can therefore be described, not only by their spectral components, but also by the pulse repetition rate (pulses/s) or interval between the beginning of consecutive pulses (interpulse interval, IPI). Indeed, some of the information conveyed in these communication sounds may be encoded in the pulse repetition rate or in the IPI (1). As part of our investigation on auditory processing in the toadfish (e.g., 2), we have evaluated the sensitivity of the auditory midbrain (torus semicircularis, TS) to sound pulses produced at several periodic rates. The stimuli for our previous experiments have been various frequencies of sinusoidal particle motion (described in 3). Here, we have used sound pulses to determine whether cells in the TS are selective for IPI or pulse rate.

Fish were anesthetized with 3 aminobenzoic acid (1:1000, Sigma), immobilized with an injection of pancuronium bromide (0.05 mg/kg); and lidocaine was applied to the skin prior to surgery. After its left midbrain region was exposed, the fish was secured to a seawater-filled dish in the stimulus shaker system (3). Glass micropipettes were broken to obtain low impedance electrodes (5–20 megohms) when filled with 4% neurobiotin in 2 M NaCl for determining electrode tip locations. All recordings were made in the left torus semicircularis.

The stimulus pulse was a 150-Hz sinusoid multiplied by the first half-cycle (10 ms duration) of a 50-Hz cosine. This produced a pulse as brief as possible, but still having frequency components low enough to stimulate the toadfish auditory system. Pulse trains were produced at 13 repetition rates between 10 and 83 pulses/s, or IPIs of 12–100 ms. The shortest IPI was dictated by the pulse duration (10 ms), because higher rates would have resulted in pulse coincidence. The pulse trains (500-ms duration) were presented 8 times each, in random order, at several levels (peak-peak displacement in dB with respect to 1 nm) within a cell’s dynamic range. The total number of spikes produced for each set of 8 pulse-train repetitions was measured at each level.

Responses were classified as selective or nonselective. A selective unit was defined as one for which the number of spikes evoked by the most effective IPI was at least 2.5 standard deviation units above the average number of spikes for all pulsed stimuli, and for which the most effective IPI was independent of sound intensity. Of 71 units evaluated, 43 (61%) were selective and the rest non-selective. Of the selective units, 56% responded best at the shortest IPI (12 ms, or 84 pulses/s). The remaining selective units responded best to IPIs between 16 and 50 ms, with a secondary mode at 20 ms.

Figure 1 shows the pulse response functions for three selective units (panels A–C). Panel A shows the data for one unit that responded best to the shortest IPI (12 ms). Panel B shows a unit that is clearly most selective to a 20-ms IPI, and panel C shows a unit responding best to a 40-ms IPI.



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Figure 1. Representative responses to pulses with varying IPIs (or pulse repetition rates). (A) Four stimulus levels for cell Y2 are represented by different symbols. The cell preferred an IPI of 12 ms (84 pulses/s). This was the most common response that was observed. The best frequency for this cell was 84 Hz, and the background activity (in the absence of a stimulus) was 1.8 spikes/s. (B) Cell C1 was nonmonotonic in that fewer spikes were produced at the highest level of stimulation (25 dB) than at the lower level (20 dB). This cell preferred an IPI of 20 ms (50 pulses/s). It had a best frequency of 141 Hz, and background activity of 4.8 spikes/s. (C) A rare cell (Z4) that responded best to a low pulse repetition rate, at three stimulus levels. This cell exhibited a preference for a 40-ms IPI (25 pulses/s). It had a best frequency of 65 Hz and background activity of 1 spike/s.

 
Selectivity of brain units to the pulse rate or IPI of sounds has been demonstrated in other fishes (1) and in vertebrates generally (e.g., 4). Pulse repetition rates for boatwhistle sounds produced by male toadfish (100–200 pulses/s) are higher than those that we could generate in this study. However, our data indicate that most cells in the midbrain that exhibit pulse selectivity respond best to the highest pulse repetition rate (84 pulses/s) used. Thus, these units might respond to pulse rates well above 84 pulses/s. Additional research on pulse selectivity by cells in the toadfish TS is warranted, particularly at higher repetition rates. Because temporally selective units occur widely in vertebrate auditory systems (1,4), it is not yet clear whether this selectivity is a primitive (i.e., widely shared) vertebrate character generally useful in sound source determination, or is a special adaptation for processing communication sounds.

Research funded by an NIH, NIDCD R01 grant to R. Fay (1 R01 DC 03666-4), and by an NIH, NIDCD Program Project Grant (1 P01 DC 00293-11) to the Parmly Hearing Institute.

Literature Cited

  1. Crawford, J. D. 1997. J. Comp. Physiol. A 180: 439–450.[Medline]
  2. Edds-Walton, P., R. Fay, and S. Highstein. 1999. J. Comp. Neurol. 411: 212–238.[ISI][Medline]
  3. Fay, R. R., and P. L. Edds-Walton. 1997. Hear. Res. 111: 1–21.[Medline]
  4. Langner, G. 1992. Hear. Res. 60: 115–142.[ISI][Medline]




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