Sparse but specific temporal coding by spikes in an insect sensory-motor ocellar pathway

We investigate coding in a locust brain neuron, DNI, which transforms graded synaptic input from ocellar L-neurons into axonal spikes that travel to excite particular thoracic flight neurons. Ocellar neurons are naturally stimulated by fluctuations in light collected from a wide field of view, for example when the visual horizon moves up and down. We used two types of stimuli: fluctuating light from a light-emitting diode (LED), and a visual horizon displayed on an electrostatic monitor. In response to randomly fluctuating light stimuli delivered from the LED, individual spikes in DNI occur sparsely but are timed to sub-millisecond precision, carrying substantial information: 4.5-7 bits per spike in our experiments. In response to these light stimuli, the graded potential signal in DNI carries considerably less information than in presynaptic L-neurons. DNI is excited in phase with either sinusoidal light from an LED or a visual horizon oscillating up and down at 20 Hz, and changes in mean light level or mean horizon level alter the timing of excitation for each cycle. DNI is a multimodal interneuron, but its ability to time spikes precisely in response to ocellar stimulation is not degraded by additional excitation. We suggest that DNI is part of an optical proprioceptor system, responding to the optical signal induced in the ocelli by nodding movements of the locust head during each wing-beat.