Properties of predictive gain modulation in a dragonfly visual neuron

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 termed predictive gain modulation. As targets drift through the receptive field responses build slowly over time. This gain is modulated across the receptive field, enhancing sensitivity just ahead of the target’s path, with suppression of activity elsewhere in the surround. Whilst some properties of this mechanism have been described, it is not yet known which stimulus parameters are required to generate this gain modulation. 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 the predictive gain modulation is more than a sluggish build-up of gain over time. Rather, gain is dependent on both past and present parameters of the stimulus. We also describe response variability as a major challenge of target detecting neurons and propose that the predictive gain modulation’s role is to drive neurons into response saturation, thus minimising neuronal variability despite noisy visual input signals.

[1]  Bart R. H. Geurten,et al.  Neural mechanisms underlying target detection in a dragonfly centrifugal neuron , 2007, Journal of Experimental Biology.

[2]  Robert A. Harris,et al.  Contrast Gain Reduction in Fly Motion Adaptation , 2000, Neuron.

[3]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster , 2004, Cell and Tissue Research.

[4]  Scott N. J. Watamaniuk,et al.  Seeing motion behind occluders , 1995, Nature.

[5]  Patrick A. Shoemaker,et al.  Facilitation of dragonfly target-detecting neurons by slow moving features on continuous paths , 2012, Front. Neural Circuits.

[6]  David C. O'Carroll,et al.  Contrast sensitivity and the detection of moving patterns and features , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  David O'Carroll,et al.  Feature-detecting neurons in dragonflies , 1993, Nature.

[8]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[9]  David C O'Carroll,et al.  A predictive focus of gain modulation encodes target trajectories in insect vision , 2017, eLife.

[10]  G. Barnes,et al.  Human ocular pursuit during the transient disappearance of a visual target. , 2003, Journal of neurophysiology.

[11]  Steven Grainger,et al.  Properties of neuronal facilitation that improve target tracking in natural pursuit simulations , 2015, Journal of The Royal Society Interface.

[12]  G. Boynton,et al.  Global effects of feature-based attention in human visual cortex , 2002, Nature Neuroscience.

[13]  S A Combes,et al.  Capture success and efficiency of dragonflies pursuing different types of prey. , 2013, Integrative and comparative biology.

[14]  S. McKee,et al.  Detecting a trajectory embedded in random-direction motion noise , 1995, Vision Research.

[15]  M. Egelhaaf,et al.  Variability in spike trains during constant and dynamic stimulation. , 1999, Science.

[16]  Anthony Leonardo,et al.  Heuristic Rules Underlying Dragonfly Prey Selection and Interception , 2017, Current Biology.

[17]  Eero P. Simoncelli,et al.  Partitioning neuronal variability , 2014, Nature Neuroscience.

[18]  David C. O'Carroll,et al.  Spatial facilitation by a high-performance dragonfly target-detecting neuron , 2011, Biology Letters.