Specificity of identified central synapses in the embryonic cockroach: appropriate connections form before the onset of spontaneous afferent activity

Abstract

The mechanisms by which neurons recognize the appropriate postsynaptic cells remain largely unknown. A useful approach to this problem is to use a system with a few identifiable neurons that form highly specific synaptic connections. We studied the development of synapses between two identified cercal sensory afferents and two giant interneurons (GIs) in the embryonic cockroach Periplaneta americana. By 46% of embryonic development, the axons of the filiform hair sensory neurons have entered the terminal ganglionic neuropil and grow alongside the GI primary dendrites, although they do not form synapses. From 50% of development, the GI dendrites grow outward from the center of the neuropil to contact the presynaptic axons and their branches. The sensory neurons begin to spike at 52% of development, and, from 55% of development, these action potentials evoked excitatory postsynaptic potentials in the GIs. Synaptic contacts were first seen at this time. The pattern of synaptic connections was highly specific from the outset. G12 had strong input from the medial (M) afferent and had almost negligible input from the lateral (L) afferent, whereas G13 had input from both. This specificity was present before bursts of spontaneous activity began in the sensory neurons at 59% of development. G12 filopodia selectively formed synaptic contacts with the M axon rather than the L axon. The few contacts made by G12 with the L axon had a normal morphology but fewer presynaptic densities. Filopodial insertions were not involved in selective synapse formation. In this system, highly specific synaptic recognition appears to be activity independent.