Abstract

Coordinated sensory and motor system activity leads to efficient localization behaviours; but what neural dynamics enable object tracking and what are the underlying coding principles? Here we show that optimized distance estimation from motion-sensitive neurons underlies object tracking performance in weakly electric fish. First, a relationship is presented for determining the distance that maximizes the Fisher information of a neuron's response to object motion. When applied to our data, the theory correctly predicts the distance chosen by an electric fish engaged in a tracking behaviour, which is associated with a bifurcation between tonic and burst modes of spiking. Although object distance, size and velocity alter the neural response, the location of the Fisher information maximum remains invariant, demonstrating that the circuitry must actively adapt to maintain ‘focus' during relative motion.

Highlights

  • Coordinated sensory and motor system activity leads to efficient localization behaviours; but what neural dynamics enable object tracking and what are the underlying coding principles? Here we show that optimized distance estimation from motion-sensitive neurons underlies object tracking performance in weakly electric fish

  • We show that ON and OFF cell spiking is not a Poisson process under spontaneous or stimulus-driven conditions and move on to more accurately investigate the idea that optimal estimation in sensory neural networks enables observed tracking behaviours

  • ON cells are selective for increases in stimulus intensity over time and OFF cells are selective for decreases in stimulus intensity, due to the sign inversion

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Summary

Introduction

Coordinated sensory and motor system activity leads to efficient localization behaviours; but what neural dynamics enable object tracking and what are the underlying coding principles? Here we show that optimized distance estimation from motion-sensitive neurons underlies object tracking performance in weakly electric fish. To assess whether precise tracking performance relies on optimized stimulus estimation, we apply Fisher Information[6] (IF) to sequences of action potentials (spikes) recorded from the motion-sensitive responses of electrosensory ON and OFF contrast-coding neurons. In other words, stimulusinduced changes in firing rate are more readily estimated against lower levels of spiking activity This estimation principle appears to be reflected in natural behaviour: during echolocation, bats cast their echo-beams off-axis from a target so that the maximum spatial slope, not the peak intensity, of the beam is reflected back to the animal[5]. A fine balance exists between sensing an object at a distance that evokes a relatively low firing rate in sensory neurons but where relative changes in object distance over time cause large changes in the neural response. We show that ON and OFF cell spiking is not a Poisson process under spontaneous or stimulus-driven conditions and move on to more accurately investigate the idea that optimal estimation in sensory neural networks enables observed tracking behaviours

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