The fidelity of neuronal processing depends on the resolution of signaling through the neuronal circuits. Preventing spillover of neurotransmitter therefore becomes a prominent issue, typically addressed by anatomical separation between synapses by cells that express neurotransmitter transporters. The nervous system of C. elegans presents a challenge to this concept, because of the widespread use of Glutamate (Glu) as a neurotransmitter (which cannot be inactivated in the synapse), and the lack of glial barrier between synapses. Instead, we show that the nematode nervous system relies on a robust two-tier system for Glu clearance, composed of proximal and distal Glu Transporters (GluTs). We use behavioral analysis and Ca2+ imaging in intact animals to show that distal GluTs regulate synaptic activity in the ASH-controlled nociceptive circuit. In contrast, inactivation of proximal GluTs seems to cause Glu spillover from the low-salt responsive chemoattractive circuit to the nociceptive circuit. To explain the differential contribution of distal and proximal GluTs to synaptic activity in different circuits, we present a hypothesis that mechanical agitation and washout might contribute to Glu clearance in some synapses in the nerve ring. Examination of nematode Glu clearance therefore widens the discussion on additional potential strategies for Glu clearance in a nervous system that seems to maintain circuit resolution in the face of strong morphological challenges.
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