The avoidance of light by fly larvae is a classic paradigm for sensorimotor behavior. Here, we use behavioral assays and video microscopy to quantify the sensorimotor structure of phototaxis using the Drosophila larva. Larval locomotion is composed of sequences of runs (periods of forward movement) that are interrupted by abrupt turns, during which the larva pauses and sweeps its head back and forth, probing local light information to determine the direction of the successive run. All phototactic responses are mediated by the same set of sensorimotor transformations that require temporal processing of sensory inputs. Through functional imaging and genetic inactivation of specific neurons downstream of the sensory periphery, we have begun to map these sensorimotor circuits into the larval central brain. We find that specific sensorimotor pathways that govern distinct light-evoked responses begin to segregate at the first relay after the photosensory neurons.N avigating organisms must extract spatial information about their surroundings to orient and move toward preferred environments. Phototaxis of fly larvae has long been a paradigm for understanding the mechanisms of animal orientation behavior (1). The study of phototaxis in the Drosophila larva provides an opportunity to investigate the circuits for orientation behavior from sensory input to motor output in a small nervous system. First, however, the sensorimotor structure of responses to illumination must be defined by studying larval behavior in controlled environments.The tropism theory of Jacques Loeb states that bilateral body plans allow animals to extract spatial information through the sensation of external forces acting asymmetrically on symmetric body halves. The navigation of fly larvae away from incident light rays was interpreted as a direct demonstration of tropism. However, temporal comparisons performed by moving animals, also known as klinotaxis, also can encode spatial information (2). Like most fly larvae, Drosophila larvae are negatively phototactic during most of their development (3-9). To navigate away from light, the Drosophila larva uses two sets of photosensors, the Rhodopsin-expressing Bolwig's organs (BO) that mediate phototaxis at low light levels and the non-Rhodopsin-expressing class IV multidendritic (md) neurons that respond to intense light levels comparable to direct sunlight (10). Here, we sought to resolve the sensorimotor structure of larval phototaxis to understand how these photosensitive structures extract and use information about ambient light conditions to control motor behavior.We developed a tracking assay and illumination system that allowed us to quantify the movements of individual animals in defined spatiotemporal illumination patterns at both low and high light intensities. We uncovered a set of sensorimotor relationships that allow the larva to navigate away from light based on temporal processing of sensory inputs. Even the capacity to navigate away from directed illumination is mediated by temporal process...

Complex animal behaviors are built from dynamical relationships between sensory inputs, neuronal activity, and motor outputs in patterns with strategic value. Connecting these patterns illuminates how nervous systems compute behavior. Here, we study Drosophila larva navigation up temperature gradients toward preferred temperatures (positive thermotaxis). By tracking the movements of animals responding to fixed spatial temperature gradients or random temperature fluctuations, we calculate the sensitivity and dynamics of the conversion of thermosensory inputs into motor responses. We discover three thermosensory neurons in each dorsal organ ganglion (DOG) that are required for positive thermotaxis. Random optogenetic stimulation of the DOG thermosensory neurons evokes behavioral patterns that mimic the response to temperature variations. In vivo calcium and voltage imaging reveals that the DOG thermosensory neurons exhibit activity patterns with sensitivity and dynamics matched to the behavioral response. Temporal processing of temperature variations carried out by the DOG thermosensory neurons emerges in distinct motor responses during thermotaxis. N avigation toward environmental conditions that improve survival and fitness is of near-universal importance in motile biological organisms. Quantitative analysis of such animal behaviors to defined sensory inputs is a powerful approach to elucidate how behavior is encoded in underlying neurons and circuits. The advantage of studying navigation in small, optically transparent, genetically modifiable animals like Caenorhabditis elegans (1) or Drosophila larvae (2) is the opportunity to dissect sensory, neuronal, and behavioral dynamics in live animals by using optical neurophysiology and optogenetics throughout the nervous system.The Drosophila melanogaster larva navigates gradients of many sensory cues, including light, temperature, odors, and tastes, but with fewer neurons in its sensory periphery and brain than the adult. Moreover, the simpler body plan and crawling movements of the larva facilitate the precise quantification of behavioral dynamics. Poikilotherms like C. elegans or Drosophila use sensitive thermosensory mechanisms to navigate moderate temperature ranges, thereby enabling them to use their environments to regulate their own body temperatures (3, 4). Here, we study sensory and behavioral dynamics during positive thermotaxis (i.e., cool avoidance) by the Drosophila larva. Tracking the movements of Drosophila exploring temperature, olfactory, or gaseous gradients has shown that their navigation is generated by a sequence of two alternating motor programs: runs involving peristaltic forward movement that are interrupted by turns involving probing side-to-side head sweeps until the initiation of a new run (5-8). Larvae negotiating temperature gradients stochastically transition between runs and turns by strategies that cause runs pointed in favorable directions to be more frequent and longer than runs pointed in unfavorable directions. These transitions b...