The Perception of the Visual Flow Field by Flying Locusts: A Behavioural and Neuronal Analysis

Abstract

1. Tethered locusts (Locusta mlgratoria) were stimulated with an artificial flow field (FF) device, which produced the visual effect of forward motion (‘progressive flow field’) or backward motion (‘regressive flow field’). Progressive FFs (contrast frequencies, CF, of 2–10 Hz and angular period of pattern, λ, of 33° or 42°) can initiate and maintain flight, even without frontal wind. Regressive FFs inhibit flight. The locusts adjust their wingbeat frequency (and thus probably their flight speed) in response to a gradually changing FF contrast frequency; they fly faster when the FF motion is faster and vice versa. Sudden decelerations of FF motion, however, are transiently counteracted by increases in wingbeat frequency. 2. Rotational movements of the entire flow field device, simulating yaw and/or roll deviations during progressive flight, elicit compensatory steering responses of the head and abdomen. Corrective steering behaviour and simultaneously presented FF stimuli do not influence each other. 3. A descending interneurone (FFDN1) is described which reports the progressive visual FF. It receives input from both compound eyes, prefers FFs on the ventral retina, and responds over the range of contrast frequencies of 1–20 Hz. Its response is tonic and adapts only weakly to maintained FF stimuli. It follows changing FF velocities but tends to counteract sudden decelerations. In addition, FFDN1 is excited by frontal and contralateral wind and inhibited by ipsilateral wind. It is also excited by the flight motor and sometimes by light-off at the ocelli. The neurone is generally insensitive to simulated roll and yaw deviations. Electrical stimulation of the cell can result in lifting of the abdomen, inhibition of dorsal neck muscle activity, and occasional flight muscle spikes. FFDN1 is probably a sister cell of the previously described DNM neurone, but the two could be one neurone with very variable responses. 4. At least one further descending interneurone responding selectively to progressive flow fields, but with a different morphology, is present in the central nervous system. Additionally, two different thoracic interneurones have been found with properties suggesting that they are postsynaptic to FFDNs and presynaptic to the flight circuitry. 5. The possible role of the visual flow field in the regulation of flight activity of locusts and other insects is discussed. Note: Present address: Department of Biology 0322, University of California at San Diego, La Jolla, CA 92093–0322, USA.