Spatiotemporal profile of synaptic activation produced by the electrical and visual stimulation of retinal inputs to the optic tectum: a current source density analysis in the pigeon (Columba livia)

The optic tectum of the pigeon is a highly organized, multilayered structur e that receives a massive polystratified afference of at least five differe nt populations of retinal ganglion cells and gives rise to various anatomic ally segregated efferent systems. The synaptic organization of retino-tecta l circuitry is, at present, mostly unknown. To investigate the spatiotempor al profile of synaptic activation produced by differential (electrical and visual) stimulation of the retinal inputs, we performed a high-spatial-reso lution current source density analysis in the optic tectum of the anaesthet ized pigeon. Electrical stimuli consisted of brief pulses of different dura tions applied to the optic nerve head, while visual stimuli consisted of li ght flashes of different intensities. Electrical stimulation generated sink s confined to retinorecipient layers. The temporal structure, spatial locat ion and thresholds of these sinks indicated that they are all due to primar y tectal synapses of retinal fibers with different conduction velocities. S inks evoked by the fastest retinal axons were more superficially located th an sinks produced by slower retinal fibers. Visual stimulation, on the othe r hand, resulted in a more complex pattern of current sinks, with various s inks located in the retinorecipient layers and also well below. Visual stim ulation induced action potentials at superficial as well as deep tectal lev els. We conclude that electrical stimulation activates most of the populati ons of ganglion cells as well as their primary tectal synapses, but is unab le to elicit a significant activation of secondary tectal synapses. Visual stimulation, on the contrary, activates just some of the incoming retinal p opulations, but in a way that produces noticeable secondary activation of i ntratectal circuits. Laminar segregation of retinally evoked tectal activit y, as reported here, has also been found in other vertebrates. Similarities and differences with previous studies are discussed.