The Mauthner cell in a fish with top-performance and yet flexibly-tuned C-starts I. Identification and comparative morphology

Abstract

Archerfish use two powerful C-starts: one to escape threats, the other to secure prey that they have downed with a shot of water. The two C-starts are kinematically equivalent and variable in both phases, and the predictive C-starts - used in hunting - are adjusted in terms of the angle of turning and the final linear speed to where and when their prey will hit the water surface. Presently, nothing is known about the neural circuits that drive the archerfish C-starts. As the starting point for a neuroethological analysis, we first explored the presence and morphology of a pair of Mauthner cells, which are key cells in the teleost fast-start system. We show that archerfish have a typical Mauthner cell in each medullary hemisphere and that these send by far the largest axons down the spinal cord. Stimulation of the spinal cord caused short-latency all-or-none field potentials that could be detected even at the surface of the medulla and that had the Mauthner cell as its only source. The archerfish's Mauthner cell is remarkably similar morphologically to that of equally sized goldfish, except that the archerfish's ventral dendrite is slightly longer and its lateral dendrite thinner. Our data provide the necessary starting point for the dissection of the archerfish fast-start system and of any role potentially played by its Mauthner cell in the two C-start manoeuvres. Moreover, they do not support the recently expressed view that Mauthner cells should be reduced in animals with highly variable fast-start manoeuvres.

Principles Governing Locomotion in Vertebrates: Lessons From Zebrafish

“…The reliability and rapidity of the C-start is accommodated by a dedicated escape circuit in the brainstem and spinal cord which has been studied intensively across numerous fish species, especially in goldfish (for reviews, see Zottoli and Faber, 2000 ; Eaton et al, 2001 ). Furthermore, studies across fish species are revealing that there is considerable flexibility in the escape response depending on the environmental context (Domenici, 2010 ; Machnik et al, 2018a , b ). Recent studies using the zebrafish have continued to illuminate new insights into the neural mechanisms underlying the C-start response and its inherent flexibility.…”

The archerfish predictive C-start

“…Archerfish do have Mauthner neurons (Fig. 6 b) that have a so-called axon cap, which means that they can be found in the hindbrain by an electrical signature, the same way as the goldfish Mauthner cell is found (Machnik et al 2018a , b). The archerfish Mauthner axon has the largest diameter of all axons that run down the archerfish spinal cord (Fig.…”

“…b Intracellular filling of the MN in equally sized goldfish (red) and archerfish (blue) revealed no major differences. See Machnik et al ( 2018a ) for detailed measurements. c Left: The axons of the archerfish MN are by far the largest in the spinal cord, but their diameter is not significantly different from that in goldfish of similar total length (right).…”

“…d The only difference found in a detailed comparative analysis was that in archerfish postsynaptic potentials (PSPs) elicited by acoustic stimuli and light flashes, whose intensities were chosen to elicit PSPs of comparable size in goldfish, were larger for the visual stimuli. Adapted from Hecker et al ( 2020a ), Machnik et al ( 2018a , b ) …”

Learning and cognition in a decision made at reflex speed

“…In the turn decisions of archerfish, specifically, it is known that the kinematics of their turn decisions is completely equivalent to the so-called Cstarts that the fish produce to escape (37). Both the turn decisions (also called predictive C-starts) and the escape C-starts are among the fastest C-start known in fish (37) and so at least the motor circuits are restricted to the well-known powerful hindbrain circuits of a comparably small number of tractable numbers of neurons, organized around the giant Mauthner neuron (59)(60)(61)(62). Its rapidly conducting axon would be suited to initiate the turn but it would clearly have to work together with other hindbrain neurons to account for the precision and adjusted straightening speed of the fish (37).…”