On and off channels of the frog optic tectum revealed by current source density analysis

Abstract

The spatiotemporal patterns of excitatory synaptic activity in response to diffuse light ON and OFF stimuli were examined by means of current source density (CSD) analysis. The qualitative and quantitative analyses obtained from 24 depth profiles for each stimulus revealed obviously different distributions of synaptic activity in the laminar structure. Two or three dominant current sinks I, II, and III were evoked in response to diffuse light ON stimulation. Sink I was observed at the bottom of the retinorecipient layer. Both sinks II and III, showing an identical spatial pattern, were observed just above sink I. On the other hand, diffuse light OFF stimulation elicited up to six current sinks IV, V, VI, VII, VIII, and IX. Sink IV was observed at the bottom of the retinorecipient layer. Sink V was observed in the most superficial layer. Both sinks VI and VIII were located between the two preceding sinks. Finally, sinks VII and IX occurred below the retinorecipient layer. Five electrically evoked current sinks A, B, C, D, and E, characterized in our previous study, were also recognized in the present quantitative analysis. A statistical analysis revealed that, in visually evoked responses, statistical differences in the spatial distribution were not present between sinks I and IV, and sinks II and VIII (P < 0.05). The analysis also showed that, in electrically evoked responses, only a pair of sinks C and E exhibit virtually identical spatial distribution (P < 0.05). Based on well-known properties of the retinal ganglion cells, possible neuronal mechanisms underlying each of current sinks in the ON and OFF channels and their functional meanings were considered. Sink I reflects the excitatory monosynaptic activity derived from R3 retinal ganglion cells. Sink IV reflects the excitatory monosynaptic activity derived from both R3 and R4 cells. Sinks V, VI, VII, and IX may be composed of successive polysynaptic excitatory potentials derived from convergence of inputs from both R3 and R4 cells. We concluded that the early four sinks play in particular an important role in eliciting avoidance behavior. On the other hand, sinks II, III, and VIII reflect excitatory synaptic activities derived from ON-OFF retinal fibers of another type having slow conduction velocity. These late current sinks were suggested to mediate prey catching and its facilitation.