Synaptic plasticity induced by differential manipulation of tonic and phasic motoneurons in Drosophila

Structural and functional plasticity induced by neuronal competition is a common feature of developing nervous systems. However, the rules governing how postsynaptic cells differentiate between presynaptic inputs are unclear. In this study we characterized synaptic interactions following manipulations of Ib tonic or Is phasic glutamatergic motoneurons that co-innervate postsynaptic muscles at Drosophila neuromuscular junctions (NMJs). After identifying drivers for each neuronal subtype, we performed ablation or genetic manipulations to alter neuronal activity and examined the effects on synaptic innervation and function. Ablation of either Ib or Is resulted in decreased muscle response, with some functional compensation occurring in the tonic Ib input when Is was missing. In contrast, the phasic Is terminal failed to show functional or structural changes following loss of the co-innervating Ib input. Decreasing the activity of the Ib or Is neuron with tetanus toxin light chain resulted in structural changes in muscle innervation. Decreased Ib activity resulted in reduced active zone (AZ) number and decreased postsynaptic subsynaptic reticulum (SSR) volume, with the emergence of filopodial-like protrusions from synaptic boutons of the Ib input. Decreased Is activity did not induce structural changes at its own synapses, but the co-innervating Ib motoneuron increased the number of synaptic boutons and AZs it formed. These findings indicate tonic and phasic neurons respond independently to changes in activity, with either functional or structural alterations in the tonic motoneuron occurring following ablation or reduced activity of the co-innervating phasic input, respectively. Significance StatementBoth invertebrate and vertebrate nervous systems display synaptic plasticity in response to behavioral experiences, indicating underlying mechanisms emerged early in evolution. How specific neuronal classes innervating the same postsynaptic target display distinct types of plasticity is unclear. Here, we examined if Drosophila tonic Ib and phasic Is motoneurons display competitive or cooperative interactions during innervation of the same muscle, or compensatory changes when the output of one motoneuron is altered. We established a system to differentially manipulate the motoneurons and examined the effects of cell-type specific changes to one of the inputs. Our findings indicate Ib and Is motoneurons respond differently to activity mismatch or loss of the co-innervating input, with the tonic subclass responding robustly compared to phasic motoneurons.