Neural circuits are extensively remodeled during development; however, the mechanisms underlying this process and the timing of rewiring remain largely unknown. Here we describe a transcriptionally regulated immunoglobulin super family protein, OIG-1, that fine-tunes synaptic plasticity in remodeling GABAergic motor neurons. DD class GABAergic motor neurons reverse polarity in the first larval (L1) stage. In newly born animals, DDs receive cholinergic inputs in the dorsal nerve cord but these are switched to the ventral side by the end of the L1 stage. The relocation of the DD postsynaptic apparatus can be monitored with the acetylcholine receptor (AChR) subunit, ACR-12::GFP. OIG-1 is highly expressed in early DD neurons where it antagonizes the relocation of ACR-12::GFP from the dorsal side. During the L1/L2 transition, OIG-1 is down-regulated by the transcription factor, IRX-1/Iroquois, in DD neurons to coincide with the translocation of postsynaptic ACR-12 to the ventral side. In VD class GABAergic motor neurons, which normally do not remodel, the transcription factor, UNC-55/COUP-TF turns off IRX-1, thus maintaining high levels of OIG-1 to block the removal of dorsally-located ACR-12 receptors. OIG-1 is secreted from GABAergic motor neurons but its anti-plasticity function is cell-autonomous and does not require secretion. Instead, we propose that secretion offers a rapid mechanism for clearing functionally active, intracellular OIG-1 thereby unleashing the postsynaptic remodeling program. Our study provides a novel mechanism by which synaptic remodeling is set in motion, through the temporal and spatial regulation of an Ig domain protein. .
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