Differential activation of Mauthner and non-Mauthner startle circuits in the zebrafish: Implications for functional substitution

Summary

• 1. The Mauthner (M-) cell triggers a complex startle or escape movement when the zebrafish,Brachydanio rerio, is presented with a sudden vibrational stimulus. Alternative (non-Mauthner) circuits functionally substitute for the M-cell to produce similar behavior patterns when the M-cell is missing or fails to fire. These responses are called non-Mauthner responses. In this paper, we demonstrate that vibrational stimulation of the tail reliably elicits responses initiated by non-Mauthner circuits in animals with intact M-cells. We conclude that such non-Mauthner circuits can functionally substitute for the M-cell in generating the escape response.

• 2. To characterize sensory pathways responsible for activating the Mauthner and non-Mauthner responses in intact animals, we made detailed comparisons of response thresholds and latencies to vibrational stimuli applied to the head and the tail.

• 3. In a comparison of vibrational stimulation applied to the head versus the tail, the M-cell was more sensitive to vibrational stimuli applied to the head. In pairwise comparisons the M-cell had the lowest threshold to the head stimulus in about 62% of the trials and the shortest latency in 79% of the trials (Table 1). For responses initiated by non-Mauthner cells, there was no difference in threshold to head and tail stimuli, but shorter latencies occurred when the head was stimulated than when the tail was stimulated (Table 1).

• 4. In a comparison of Mauthner and non-Mauthner responses, we found that in 77% of the trials, Mauthner responses occurred at lower stimulus intensities than the responses initiated by non-Mauthner circuits when a vibrational stimulus was applied to the head. But, when the tail was stimulated, there was no apparent difference in stimulus intensity required to elicit Mauthner responses and responses initiated by non-Mauthner circuits. The Mauthner responses were always substantially shorter in latency (by an average of 15 or 21 ms) than the responses initiated by non-Mauthner circuits when stimulating either the head or tail.

• 5. We conclude that at least two sensory systems are involved in the activation of these startle systems when stimulating the head and tail of the zebrafish. One system is the otolithic receptors of the ear and another is probably either the posterior lateral line or Rohon-Beard cell system. The findings are discussed in terms of a general model that provides a mechanism for functional substitution of responses initiated by non-Mauthner circuits for Mauthner responses.