Neural computations combine low- and high-order motion cues similarly, in dragonfly and monkey

Abstract

Visual motion analysis is fundamental to survival across the animal kingdom. In insects, our understanding of the underlying computations has centered on the Hassenstein-Reichardt motion detector, which computes two-point cross-correlation via multiplication; in mammalian cortex, it is postulated that a similar signal is computed by comparing matched squaring operations. Both of these operations are difficult to implement biophysically in a precise fashion; moreover, they fail to detect the more complex multipoint local motion cues present in the visual environment. Here, via single-unit recordings in two visual specialists, dragonfly "(Odonata)" and macaque, and via model simulations, we show that neuronal computations are not simply approximations to idealized behaviors forced by biological constraints, but rather, are signatures of a common computational strategy to capture multiple local motion cues. The similarity of motion computations at the neuronal level in the brains of two extremely dissimilar animals, with evolutionary divergence of over 700 Myr 1 , suggests convergence on a common computational scheme for detecting visual motion.

Predictive encoding of motion begins in the primate retina

“…Sensitivity to these correlations arise early in the visual stream in fruit flies-at the level of tangential cells in the lobula plate, if not earlier (Leonhardt et al, 2016). In humans and nonhuman primates, this sensitivity was thought to arise first in the primary visual cortex (Nitzany et al, 2017;Clark et al, 2014). Our findings indicate, however, that sensitivity to higher-order spatiotemporal correlations arises much earlier than previously thoughtit is present in the synaptic outputs of diffuse bipolar cells at the second synapse of the visual stream.…”

“…The asymmetrical distribution of bright and dark intensities in nature produce correlations between three or more points in space and time during visual motion (Field, 1987;Dong and Atick, 1995;Fitzgerald et al, 2011;Hu and Victor, 2010;Ratliff et al, 2010). Indeed, humans and other animals utilize these higher-order correlations in estimating motion (Nitzany et al, 2017;Clark et al, 2014). Sensitivity to these correlations arise early in the visual stream in fruit flies-at the level of tangential cells in the lobula plate, if not earlier (Leonhardt et al, 2016).…”

Optomotor Swimming in Larval Zebrafish Is Driven by Global Whole-Field Visual Motion and Local Light-Dark Transitions

“…These studies show that luminance on and off responses are processed very differently in the zebrafish brain, consistent with our results shown in Figure 6, where the clusters 1 and 5 show very little overlap. In the context of the OMR, experiments in flies, dragonflies, and primates (Clark et al, 2014;Leonhardt et al, 2016;Nitzany et al, 2017) have shown asymmetries in the processing of light and dark in the on and off pathways using two-and three-point correlation glider stimuli (Hu and Victor, 2010). Furthermore, the differential contribution of the on-off symmetric whole-field motion in the periphery and the local off edge is reminiscent of the figureground distinctions that have been probed in flies (Aptekar et al, 2015;Barnhart et al, 2018;Fox et al, 2014), although the systematic analysis of local and global motion percepts or object motion superimposed on a moving background has not been investigated in larval zebrafish.…”

Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes

“…Nevertheless, it remains unclear how similar or different the details of such strategies will be across the animal kingdom. Indeed, although both primates and insects respond to third-order glider stimuli, their patterns of response differ (Clark et al, 2014; Hu and Victor, 2010; Nitzany et al, 2017). ON-OFF asymmetric visual processing also varies in other ways, and there is evidence that contrast adaptation in ON and OFF pathways is different between primate and salamander retinas (Chander and Chichilnisky, 2001).…”