Spontaneous spiking in photoreceptors of Periplaneta americana

Insect photoreceptors are non-spiking neurons that encode visual information with graded voltage responses produced by stochastic activation of the phototransduction cascade in the microvilli. However, light-evoked, voltage-gated sodium channel (Na_V) dependent axonal spikes have been reported in several species, where they are thought to support downstream signal transmission. Here we report a new mode of electrical activity in rhabdomeric photoreceptors: spontaneous trains of small, fast spikes appearing in darkness immediately after piercing the membrane. These spike trains differed from both quantum bumps and conventional axonal spikes. They occurred without light stimulation, persisted for tens of seconds to minutes, exhibited several millivolt amplitudes, and had kinetics and waveforms resembling Na_V-dependent regenerative action potentials. Several lines of evidence indicated that spikes are generated in distal parts of the axon. First, spiking was suppressed by off-axis illumination that produced minimal somatic hyperpolarization, consistent with the effects of lateral interactions on axon terminals in the neuropil. Second, observation of spike superposition indicated that they can arise from multiple electrotonically separated loci and summate at the soma, suggesting distal, spatially separated spike-generating sites. Third, while spiking was sensitive to experimentally imposed changes in somatic membrane potential, spike frequency and duration often changed spontaneously and independently of it. Spiking spontaneously and irreversibly terminated through a gradual decline in spike frequency and often amplitude, consistent with a progressive reduction in Na_V channel availability. Our results suggest that spontaneous spike trains reflect a transient shift in axonal excitability, possibly triggered by electrical perturbations associated with membrane penetration.