Invisible noise obscures visible signal in insect motion detection

Ghaith Tarawneh,Ronny Rosner,Bruce G Cumming,Vivek Nityananda,William Herbert,Jenny C A Read,Steven Errington,Ignacio Serrano-Pedraza

doi:10.1038/s41598-017-03732-7

Abstract

The motion energy model is the standard account of motion detection in animals from beetles to humans. Despite this common basis, we show here that a difference in the early stages of visual processing between mammals and insects leads this model to make radically different behavioural predictions. In insects, early filtering is spatially lowpass, which makes the surprising prediction that motion detection can be impaired by “invisible” noise, i.e. noise at a spatial frequency that elicits no response when presented on its own as a signal. We confirm this prediction using the optomotor response of praying mantis Sphodromantis lineola. This does not occur in mammals, where spatially bandpass early filtering means that linear systems techniques, such as deriving channel sensitivity from masking functions, remain approximately valid. Counter-intuitive effects such as masking by invisible noise may occur in neural circuits wherever a nonlinearity is followed by a difference operation.

Highlights

Linear system analysis, first introduced in visual neuroscience decades ago[1, 2], has been highly influential and continues to be successfully applied in several domains including contrast, disparity and motion perception[3,4,5,6]
We here reveal a profound difference in how noise affects motion perception in insects versus humans, we show that this need not conflict with existing evidence that both species use a similar mechanism to compute visual motion
The attraction of the quadrature assumption is that it makes leftward and rightward responses to a simple moving grating constant, despite the temporal modulation of the stimulus. This is consistent with the behaviour of directionally-selective complex cells in primary visual cortex[9, 34], which are assumed to be the physiological substrate of directionally-selective motion detection channels in humans[35], the phase-independence of complex cells is probably achieved by summing many inputs at a range of phases, rather than just two inputs in quadrature[36]

Summary

Introduction

First introduced in visual neuroscience decades ago[1, 2], has been highly influential and continues to be successfully applied in several domains including contrast, disparity and motion perception[3,4,5,6]. The prominent models in the domain of motion perception, for example, include well-known nonlinearities but are still assumed to not respond to noise outside their frequency sensitivity band[30]. We show that this assumption is not generally true for the standard models of motion perception The nonlinearity of these models means that a moving signal at a highly visible frequency can be “masked” (made less detectable) by noise at frequencies outside the detector’s sensitivity band (i.e. invisible noise). This effect has been neglected because it does not occur when the filtering prior to motion detection is spatially bandpass, as it is in mammals. We here reveal a profound difference in how noise affects motion perception in insects versus humans, we show that this need not conflict with existing evidence that both species use a similar mechanism to compute visual motion

Methods

Results

Conclusion