A neurochemical map of the developing amphioxus nervous system

Glutamate and locomotory control in amphioxus larvae

Thurston Lacalli   (2013-03-08 12:55)  University of Victoria

As the investigator responsible for the EM-level reconstructions [1] used as a point of reference by Candiani et al. in this new study, I am gratified at the degree to which their neurochemical map of the amphioxus larval CNS matches our morphological one. An unexpected result, for me at any rate, is that Candiani et al. find only a single pair of glutaminergic neurons in the anterior nerve cord, in contrast with the cholinergic, GABAergic and glycinergic neurons, which occur in greater numbers over multiple segments. The authors conclude that their single glutaminergic pair corresponds to the third pair of Large Paired Neurons (LPN3s) identified by EM. The location supports this, as does the nature of the LPN3s themselves: they are essentially unique, being by far the largest interneurons in the nerve cord in young larvae, with massive axons and extensive synaptic output to the motoneurons responsible for the larval escape response.

This conclusion regarding LPN3 identity has consequences worth noting: the LPN3s have contralateral projections and reciprocal synapses at their first point of mutual contact, a feature also unique to this pair of cells which could, in principle, provide the basis for a pacemaker using cross inhibition to generate the phased output required for undulatory swimming. Based on the neurochemical data, this now seems untenable if glutamate acts in amphioxus, as in vertebrates, as an excitatory neurotransmitter. If so, the LPN3s would then be the only excitatory interneurons intrinsic to the locomotory control system. If the cross innervation between them is also excitatory, sensory input to either cell would activate both, and this in turn would activate motoneurons on both sides of the nerve cord. The core function of the LPN3s would therefore seem to be an overall activation of neurons involved in the escape response. This accords with observations on swimming in another protochordate, the tadpole larva of Ciona, where L-glutamate has been shown to strongly stimulate swimming [2]. It accords also with preliminary results obtained with amphioxus larvae in my own lab in the mid-1990s: L-glutamate, in micromolar concentration, evoked by far the strongest response of any of the neuroactive substances tested, producing extended bouts of vigorous escape-mode swimming that only ceased as the larvae became totally exhausted and close to death. Neither GABA nor glycine had pronounced behavioral effects.

Thus, both what is known of CNS circuitry from EM data, and the admittedly incomplete results we have on behavior, support the supposition that the pair of glutaminergic neurons located at the level of the somite 1/2 junction are LPN3s that act in an excitatory fashion. Where the pacemaker resides is a more complex question, but the involvement of inhibitory interneurons, i.e. those identified by Candiani et al. as containing GABA and glycine, both generally inhibitory in vertebrate CNS, seems likely. Further work on amphioxus larvae combining the neurochemistry and morphology with careful behavioral studies, could be a way to confirm this.

References

1. Lacalli TC, Kelly SJ: Ventral neurons in the anterior nerve cord of amphioxus larvae I. An inventory of cell types and synaptic patterns. J Morph 2003, 257:190-211.

2. Nishino A, Okamura Y, Piscopo S, Brown ER: A glycine receptor is involved in the organization of swimming movements in an invertebrate chordate. BMC Neurosci 2010, 11:6.

Competing interests

None

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