Distributed processing by visual interneurons of crayfish brain. I. Response characteristics and synaptic interactions.

1. The visual responses and synaptic interactions of a small population of crayfish interneurons are described. 2. The discharge of optic nerve sustaining fibers (tonic on-cells) appears in the brain prior to the onset of the light-evoked discharge of any of the higher order, descending visual interneurons. Direct depolarization of impaled sustaining fibers elicits impulse responses in a large number of descending interneurons. These results indicate that the sustaining fibers provide the visual input to higher order interneurons. 3. Four classes of descending interneurons can be distinguished. All arise in the brain and have axons in the circumesophageal connectives. The response forms vary from tonic to phasic. Two classes of tonic cells are distinguished by response latency and two classes of phasic neurons are distinguished by the rate of response adaptation. The phasic neurons exhibit the most rapid habituation, the largest receptive fields, and the most potent nonvisual inputs. 4. Synaptic interactions are studied by cross-correlation of impulse trains and direct observation of synaptic potentials. About 84% of the cells examined reveal evidence of functional connections to other descending visual interneurons. 5. Cross-correlograms derived from impulses of parallel interneurons exhibit a mean time lage to peak of 6.6 +/- 2.8 ms (SD). The measured delay from EPSP onset to spike onset is 6.0 +/- 4.0 ms. Thus a substantial proportion of the correlogram's time lag to peak is associated with postsynaptic integration time. 6. Direct depolarization of impaled tonic on-cells elicits impulse activity at a fixed delay in other descending interneurons. 7. Synaptic potentials in descending visual interneurons are correlated 1:1 with axon spikes of other descending interneurons. 8. A third of the 80 interactions examined were reciprocal and many cells were implicated in multiple interactions. 9. The results suggest that the descending visual interneurons are organized in a complex network, which can cordinate the discharge of various subpopulations of the ensemble. It is proposed that the coordination of impulses in parallel interneurons may be a mechanism for coding and information transfer in the crayfish nervous system.