Mauthner and Reticulospinal Responses to the Onset of Acoustic Pressure and Acceleration Stimuli

Abstract

We determined how the Mauthner cell and other large, fast-conducting reticulospinal neurons of the goldfish responded to acoustic stimuli likely to be important in coordinating body movements underlying escape. The goal was to learn about the neurophysiological responses to these stimuli and the underlying processes of sensorimotor integration. We compared the intracellularly recorded postsynaptic responses (PSPs) of 9 Mauthner cells and a population of 12 other reticulospinal neurons to acoustic pressure and acceleration stimuli. All recorded cells received both pressure and acceleration inputs and responded to stimuli regardless of initial polarity. Thus these cells receive acoustic components necessary to determine source direction. We observed that the Mauthner cell was broadly tuned to acoustic pressure from 100 to 2,000 Hz, with a Q10dB of 0.5–1.1 over the best frequency range, 400–800 Hz. This broad tuning is probably due to input from S1 afferents and is similar to tuning of the behavioral audiogram. Our data suggest that cells have relatively more sustained responses to acceleration than to pressure stimuli, to which they rapidly adapted. For a given cell, PSP latencies and amplitudes varied inversely with stimulus intensity. For the entire population of cells studied, minimum onset latencies (i.e., those at the highest intensities) ranged from 0.7 to 7.6 ms for acoustic pressure and 0.7 to 9.8 ms for acceleration. This distribution in minimum onset latencies is consistent with earlier EMG and kinematic findings and supports our previous hypothesis that escape trajectory angle is controlled, in part, by varying the activation time of neurons in the escape network. While the Mauthner cell latency did not differ to both onset polarities of pressure and acceleration, this was not true of all cells. Also, the Mauthner cell responses to pressure were ∼0.6 ms faster than to acceleration; for the other cells, this difference was 1.1 ms with some cells having differences ≤3 ms. To both pressure and acceleration, the average, minimum Mauthner cell latency was ∼1 ms faster than the average of the 12 other cells. These data are consistent with the hypothesis that the Mauthner cell fires first, followed by other reticulospinal neurons, which more finely regulate escape trajectory. Finally, analysis of our results suggests that while pressure is more important in depolarizing the cell near threshold, high levels of acceleration, perhaps from fluid flow, may be very important in activating the system in a directional manner.