A whole nervous system atlas of glutamate receptors reveals distinct receptor roles in sensorimotor circuits

Abstract

A goal of connectomics is to reveal the links between neural circuits and behavior. Larvae of the primitive chordate Ciona are well-suited to make contributions in this area. The small size of the Ciona larval nervous system ([~]180 neurons) has facilitated the full characterization of a connectome. In addition, the larvae display a range of behaviors that are readily quantified in both normal and manipulated larvae. Moreover, the small number of neurons allows for a neuron-by-neuron characterization of attributes such as neurotransmitter use. We present here a nervous system-wide atlas of glutamate receptor expression. Included in the atlas are both ionotropic receptors (AMPA, NMDA, and Kainate), and metabotropic receptors. The expression of these receptors is presented in the context of known circuits driving behaviors such as phototaxis, mechanosensation, and looming shadow response. The expression of AMPA and NMDA receptors, in particular, helps to resolve the apparently paradoxical coproduction of GABA and glutamate by some photoreceptors. We find that the targets of these photoreceptors, midbrain relay neurons, primarily express NMDA receptors in the absence of AMPA receptors. This is in agreement with previous results indicating that GABA is the primary neurotransmitter from the photoreceptors evoking a behavioral response (swimming) through a disinhibition mechanism. We hypothesize that NMDA receptors have a modulatory effect in the relay neurons. Other findings reported here are more unexpected. For example, the targets of glutamatergic epidermal sensory neurons (ESNs) do not express any of the ionotropic receptors, yet the ESNs themselves express metabotropic receptors. Thus, we speculate that their production of glutamate may be for communication with neighboring ESNs, rather than to their interneuron targets.