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.
DOI:
http://dx.doi.org/10.7554/eLife.06225.001
Living organisms can sense their surroundings and respond in appropriate ways. For example, animals will often move towards the smell of food or away from potential threats, such as predators. However, it is not fully understood how an animal's nervous system is setup to allow sensory information to control how the animal navigates its environment.
Optogenetics is a technique that allows neuroscientists to control the activities of individual nerve cells in freely moving animals, simply by shining light on to them. Here, Hernandez-Nunez et al. have used optogenetics in fruit fly larvae to activate nerve cells that normally respond to smells and tastes, while the larvae's movements were tracked. Fruit fly larvae were chosen because they have a simple, but well-studied, nervous system. These larvae also move in two distinct ways: ‘runs’, in which a larva moves forward; and ‘turns’, during which a larva sweeps its head back and forth until it selects the direction of a new run.
The data from these experiments were quantified using a specific type of statistical analysis called ‘reverse correlation’ and used to build mathematical models that predict navigational behavior. This analysis of the experiments allowed Hernandez-Nunez et al. to reveal how specific sensory nerve cells can contribute to pathways that control an animal's navigation—and an independent study by Gepner, Mihovilovic Skanata et al. revealed similar results.
The approach of using optogenetics in combination with quantitative analysis, as used in these two independent studies, is now opening the door to a more complete understanding of the connections between the activity of sensory nerve cells and perception and behavior.
DOI:
http://dx.doi.org/10.7554/eLife.06225.002