Abstract
Neural circuits for behavior transform sensory inputs into motor outputs in patterns with strategic value. Determining how neurons along a sensorimotor circuit contribute to this transformation is central to understanding behavior. To do this, a quantitative framework to describe behavioral dynamics is needed. In this study, we built a high-throughput optogenetic system for Drosophila larva to quantify the sensorimotor transformations underlying navigational behavior. We express CsChrimson, a red-shifted variant of channelrhodopsin, in specific chemosensory neurons and expose large numbers of freely moving animals to random optogenetic activation patterns. We quantify their behavioral responses and use reverse-correlation analysis to uncover the linear and static nonlinear components of navigation dynamics as functions of optogenetic activation patterns of specific sensory neurons. We find that linear-nonlinear models accurately predict navigational decision-making for different optogenetic activation waveforms. We use our method to establish the valence and dynamics of navigation driven by optogenetic activation of different combinations of bitter-sensing gustatory neurons. Our method captures the dynamics of optogenetically induced behavior in compact, quantitative transformations that can be used to characterize circuits for sensorimotor processing and their contribution to navigational decision making.
Highlights
To successfully navigate their environments, animals transform sensory inputs into motor outputs in patterns that strategically orient themselves towards improving conditions
A fundamental step towards understanding how animal navigation is encoded in neural circuits is the development of a quantitative framework that accurately describes behavioral dynamics
To take this step with the Drosophila larva, we combined optogenetics with high-resolution behavioral analysis and reverse-correlation techniques to build LN models that provide an accurate estimate of the decision-making processes that guide navigation during optogenetically induced chemotaxis
Summary
To successfully navigate their environments, animals transform sensory inputs into motor outputs in patterns that strategically orient themselves towards improving conditions. The small size and simple nervous system of the Drosophila larva, combined with its powerful genetic toolbox and recent advances in optical neurophysiology and anatomical reconstruction of circuit structure and connectivity, opens the possibility of understanding the neural encoding of animal navigation from sensory inputs to motor outputs without gaps (Saalfeld et al, 2012). A quantitative framework to describe navigation decision-making is needed. Such a framework can be used to dissect the function of the neurons and circuits in charge of processing sensory information. Attractive and repulsive responses can be estimated by the tendency of the larva to aggregate near or avoid an environmental
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