Neural network based on the input organization of an identified neuron signaling impending collision

1. We describe a four-layered neural network (Fig. 1), based on the input organization of a collision signaling neuron in the visual system of the locust, the lobula giant movement detector (LGMD). The 250 photoreceptors ("P" units) in layer 1 are excited by any change in illumination, generated when an image edge passes over them. Layers 2 and 3 incorporate both excitatory and inhibitory interactions, and layer 4 consists of a single output element, equivalent to the locust LGMD. 2. The output element of the neural network, the "LGMD", responds directionally when challenged with approaching versus receding objects, preferring approaching objects (Figs. 2-4). The time course and shape of the "LGMD" response matches that of the LGMD (Fig. 4). Directionality is maintained with objects of various sizes and approach velocities. The network is tuned to direct approach (Fig. 5). The "LGMD" shows no directional selectivity for translatory motion at a constant velocity across the "eye", but its response increases with edge velocity (Figs. 6 and 9). 3. The critical image cues for a selective response to object approach by the "LGMD" are edges that change in extent or in velocity as they move (Fig. 7). Lateral inhibition is crucial to the selectivity of the "LGMD" and the selective response is abolished or else much reduced if lateral inhibition is taken out of the network (Fig. 7). We conclude that lateral inhibition in the neuronal network for the locust LGMD also underlies the experimentally observed critical image cues for its directional response. 4. Lateral inhibition shapes the velocity tuning of the network for objects moving in the X and Y directions without approaching the eye (see Fig. 1). As an edge moves over the eye at a constant velocity, a race occurs between the excitation that is caused by edge movement and which passes down the network and the inhibition that passes laterally. Excitation must win this race for units in layer 3 to reach threshold (Fig. 8). The faster the edge moves over the eye the more units in layer 3 reach threshold and pass excitation on to the "LGMD" (Fig. 9). 5. Lateral inhibition shapes the tuning of the network for objects moving in the Z direction, toward or away from the eye (see Fig. 1). As an object approaches the eye there is a buildup of excitation in the "LGMD" throughout the movement whereas the response to object recession is often brief, particularly for high velocities. During object motion, a critical race occurs between excitation passing down the network and inhibition directed laterally, excitation must win this race for the rapid buildup in excitation in the "LGMD" as seen in the final stages of object approach (Figs. 10-12). The buildup is eliminated if, during object approach, excitation cannot win this race (as happens when the spread of inhibition laterally takes < 1 ms Fig. 13, D and E). Taking all lateral inhibition away increases the "LGMD" response to object approach, but overall directional selectivity is reduced as there is also a lot of residual network excitation following object recession (Fig. 13B). 6. Directional selectivity for rapidly approaching objects is further enhanced at the level of the "LGMD" by the timing of a feed-forward, inhibitory loop onto the "LGMD", activated when a large number of receptor units are excited in a short time. The inhibitory loop is activated at the end of object approach, truncating the excitatory "LGMD" response after approach has ceased, but at the initiation of object recession (*Fig. 2, 3, and 13). Eliminating the feed-forward, inhibitory loop prolongs the "LGMD" response to both receding and approaching objects (Fig. 13F).