Sensory Neuron Terminals in Paddlefish Electroreceptors: Where Do Spikes Start?

We studied the branching terminals of sensory neuron axons at electroreceptors in the skin of paddlefish. They respond to weak electric fields in nearby water, from prey. FOCUS PROBLEM: Where are spikes initiated? Since a sensory neuron branches repeatedly to receive input from 3-30 ``sensors,'' is there a separate spike initiation zone for each sensor? Or do all the sensors sum to drive spiking at a single zone? APPROACH: (i) 3-Color fluorescent antibody labeling and light microscopy revealed the locations of specific cell components known to be involved in action potential generation, including voltage-gated sodium channels, and neurofilament-H inside sensory axons, and myelin around axons. (ii)Fluorescent lipophilic tracers DiI and DiO revealed the membrane of sensory axon branches. RESULTS: (i) Antibody labeling showed that as a sensory axon branched repeatedly, each sub-branch remained myelinated until 100 microns from the sensors, where each sub-branch had a classic ``hemi-node'' organization, with a final cluster of sodium channels (the last node), beyond which unmyelinated neurites, not showing voltage-gated sodium channels, branched profusely to innervate a pair of adjacent sensors. (ii) Lipophilic tracers confirmed this organization. We used 2-color tracing to ask if the 3-6 sensory axons in an electroreceptor co-innervate all of its sensors. CONCLUSION: A sensory axon can have multiple spike initiation zones, e.g. up to 15 (one for each pair of sensors) in paddlefish electroreceptors.