Properties of predictive gain modulation in a dragonfly visual neuron

Abstract

Dragonflies pursue and capture tiny prey and conspecifics with extremely high success rates. These moving targets represent a small visual signal on the retina and successful chases require accurate detection and amplification by downstream neuronal circuits. This amplification has been observed in a population of neurons called small target motion detectors (STMDs), through a mechanism we term predictive gain modulation. As targets drift through the neuron’s receptive field, spike frequency builds slowly over time. This increased likelihood of spiking or gain is modulated across the receptive field, enhancing sensitivity just ahead of the target’s path, with suppression of activity in the remaining surround. Whilst some properties of this mechanism have been described, it is not yet known which stimulus parameters modulate the amount of response gain. Previous work suggested that the strength of gain enhancement was predominantly determined by the duration of the target’s prior path. Here, we show that predictive gain modulation is more than a slow build-up of responses over time. Rather, the strength of gain is dependent on the velocity of a prior stimulus combined with the current stimulus attributes (e.g. angular size). We also describe response variability as a major challenge of target-detecting neurons and propose that the role of predictive gain modulation is to drive neurons towards response saturation, thus minimising neuronal variability despite noisy visual input signals.