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 ...

1. The "descending contralateral movement detector" (DCMD) neuron in the locust has been challenged with a variety of moving stimuli, including scenes from a film (Star Wars), moving disks, and images generated by computer. The neuron responds well to any rapid movement. For a dark object moving along a straight path at a uniform velocity, the DCMD gives the strongest response when the object travels directly toward the eye, and the weakest when the object travels away from the eye. Instead of expressing selectivity for movements of small rather than large objects, the DCMD responds preferentially to approaching objects. 2. The neuron shows a clear selectivity for approach over recession for a variety of sizes and velocities of movement both of real objects and in simulated movements. When a disk that subtends > or = 5 degrees at the eye approaches the eye, there are two peaks in spike rate: one immediately after the start of movement; and a second that builds up during the approach. When a disk recedes from the eye, there is a single peak in response as the movement starts. There is a good correlation between spike rate and angular acceleration of the edges of the image over the eye. 3. When an object approaches from a distance sufficient for it to subtend less than one interommatidial angle at the start of its approach, there is a single peak in response. The DCMD tracks the approach, and, if the object moves at 1 m/s or faster, the spike rate increases throughout the duration of object movement. The size of the response depends on the speed of approach. 4. It is unlikely that the DCMD encodes the time to collision accurately, because the response depends on the size as well as the velocity of an approaching object. 5. Wide-field movements suppress the response to an approaching object. The suppression varies with the temporal frequency of the background pattern. 6. Over a wide range of contrasts of object against background, the DCMD gives a stronger response to approaching than to receding objects. For low contrasts, the selectivity is greater for objects that are darker than the background than for objects that are lighter.

We challenged tethered, flying locusts with visual stimuli looming from the side towards one eye in a way that mimics the approach of a predatory bird. Locusts respond to the lateral approach of a looming object with steering movements and a stereotyped, rapid behaviour in which the wingbeat pattern ceases and the wings are swept into a gliding posture. This gliding behaviour may cause the locust to dive. The gliding posture is maintained for 200 ms or more after which flight is resumed with an increased wingbeat frequency or else the wings are folded. A glide begins with a strong burst of activity in the mesothoracic second tergosternal motor neuron (no. 84) on both sides of the locust. Recordings of descending contralateral movement detector (DCMD) activity in a flying locust show that it responds to small (80-mm diameter) looming stimuli during tethered flight, with a prolonged burst of spikes that tracks stimulus approach and reaches peak instantaneous frequencies as, or after, stimulus motion ceases. There is a close match between the visual stimuli that elicit a gliding behaviour and those that are effective at exciting the DCMD neuron. Wing elevation into the gliding posture occurs during a maintained burst of high frequency DCMD spikes.

Role of an identified looming-sensitive neuron in triggering a flying locust's escape. J Neurophysiol 95: 3391-3400, 2006. First published February 1, 2006 doi:10.1152/jn.00024.2006. Flying locusts perform a characteristic gliding dive in response to predatorsized stimuli looming from one side. These visual looming stimuli trigger trains of spikes in the descending contralateral movement detector (DCMD) neuron that increase in frequency as the stimulus gets nearer. Here we provide evidence that high-frequency (Ͼ150 Hz) DCMD spikes are involved in triggering the glide: the DCMD is the only excitatory input to a key gliding motor neuron during a loom; DCMD-mediated EPSPs only summate significantly in this motor neuron when they occur at Ͼ150 Hz; when a looming stimulus ceases approach prematurely, high-frequency DCMD spikes are removed from its response and the occurrence of gliding is reduced; and an axon important for glide triggering descends in the nerve cord contralateral to the eye detecting a looming stimulus, as the DCMD does. DCMD recordings from tethered flying locusts showed that glides follow high-frequency spikes in a DCMD, but analyses could not identify a feature of the DCMD response alone that was reliably associated with glides in all trials. This was because, for a glide to be triggered, the high-frequency spikes must be timed appropriately within the wingbeat cycle to coincide with wing elevation. We interpret this as flight-gating of the DCMD response resulting from rhythmic modulation of the flight motor neuron's membrane potential during flight. This means that the locust's escape behavior can vary in response to the same looming stimulus, meaning that a predator cannot exploit predictability in the locust's collision avoidance behavior.

No abstract