Time-dependent Activation of Feed-forward Inhibition in a Looming-sensitive Neuron

The lobula giant movement detector (LGMD) is an identified neuron in the locust visual system that responds preferentially to objects approaching on a collision course with the animal. For such looming stimuli, the LGMD firing rate gradually increases, peaks, and decays toward the end of approach. The LGMD receives both excitatory and feed-forward inhibitory inputs on distinct branches of its dendritic tree, but little is known about the contribution of feed-forward inhibition to its response properties. We used picrotoxin, a chloride channel blocker, to selectively block feed-forward inhibition to the LGMD. We then computed differences in firing rate and membrane potential between control and picrotoxin conditions to study the activation of feed-forward inhibition. For looming stimuli, a significant activation of inhibition was observed early, as objects exceeded on average approximately 23 degrees in angular extent at the retina. Inhibition then increased in parallel with excitation over the remainder of approach trials. Experiments in which the final angular size of the approaching objects was systematically varied revealed that the relative activation of excitation and inhibition remains well balanced over most of the course of looming trials. Feed-forward inhibition actively contributed to the termination of the response to approaching objects and was particularly effective for large or slowly moving objects. Suddenly appearing and receding objects activated excitation and feed-forward inhibition nearly simultaneously, in contrast to looming stimuli. Under these conditions, the activation of excitation and feed-forward inhibition was weaker than for approaching objects, suggesting that both are preferentially tuned to approaching objects. These results support a phenomenological model of multiplication within the LGMD and provide new constraints for biophysical models of its responses to looming and receding stimuli.