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Identification of Mauthner-initiated response patterns in goldfish: Evidence from simultaneous cinematography and electrophysiology

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Summary

  1. 1.

    This paper demonstrates that the Mauthner (M-) cell action potential is correlated with the onset of C-type fast-start responses beginning with a contraction of the contralateral body musculature. We made extracellular recordings from individual M-cells with chronically implanted microelectrodes in six goldfish while the animals were free to swim in an aquarium (19–23 °C). Fast-start responses were elicited by dropping a ball into the aquarium from above the fish. The behavior was filmed at 500 frames/s with a high-speed cine camera (Fig. 31).

  2. 2.

    In 45 responses, the M-cell action potential (M-spike) fired 7.4 ms ±6.7 (±SD) after the ball hit the water. The M-spike was followed after 8.1 ms±1.6 by the first stage of a C-type fast-start response that began with an initial contraction of the body on the side opposite the monitored M-cell (Figs. 5 A and 6). This is consistent with neuroanatomical and physiological evidence that the M-cell excites contra-lateral motor neurons. No M-spike was recorded in 18 trials when the C-start began with an initial contraction on the same side as the monitored M-cell (Fig. 7B1, 7B2). Presumably, such responses were initiated by the unmonitored M-cell on the opposite side of the brain. There was also no M-spike when the fish did not respond to the stimulus (ten trials).

  3. 3.

    M-initiated C-starts fell into two different response categories differentiated by the turns taken during the second stage of the motor pattern. In most cases (83%) the animal continued in the trajectory of its initial turn (Fig. 5 A). In 17% of the responses the second stage turn was in a direction opposite that taken initially, so that the animal darted forward (Fig. 5B).

  4. 4.

    The maximum mean displacement speed of three fish in 21 trials was 18 body lengths/s as measured from the rostrum. This occurred at about 16 ms after the response began (Fig. 9A). The maximum mean angular velocity of the head was 3,500 deg/s. This occurred at 10 ms after the response began (Fig. 9C). These values correspond to the pronounced lateral movement of the head during the initial stage of the response.

  5. 5.

    The M-initiated first stage was Stereotypic in terms of the trajectory taken (Fig. 8) and the mechanical performance of the animal (Fig. 9 B and D). In contrast, the turning performance during the second stage was variable from trial to trial (Figs. 8, 9B and D).

  6. 6.

    M-initiated responses were directed away from the stimulus. The M-cell on the side closest to the ball was the one that usually fired (85% of the trials) so that the initial turn was away from the stimulus. During 87% of the second stage responses, the animal oriented away from the stimulus (Fig. 10).

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Abbreviations

M :

Mauthner

SD :

standard deviation of the mean

ST :

coefficient of stereotypy

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We thank Drs. A.C. Bekoff, C.B. Kimmel and S.J. Zottoli for comments on the manuscript, D.G. Brooks for assistance with illustrations and G. Narfadottir for data analysis. Support was provided by grants from N.S.F. (BNS 78-10687 and BNS 79-05770) and N.I.H. (BRSG RR07013-1980). R.C.E. is grateful to Dr. C.B. Kimmel and R.J. Kimmel for micrographs and to Dr. H. Korn (C.H.U. Pitié-Salpêtrière, Paris, France) for helpful advice on the goldfish M-cell preparation during an I.N.S.E.R.M. fellowship.

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Eaton, R.C., Lavender, W.A. & Wieland, C.M. Identification of Mauthner-initiated response patterns in goldfish: Evidence from simultaneous cinematography and electrophysiology. J. Comp. Physiol. 144, 521–531 (1981). https://doi.org/10.1007/BF01326837

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