Sensorimotor structure of Drosophila larva phototaxis

Abstract

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...

CRYPTOCHROME mediates behavioral executive choice in response to UV light

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A Group of Segmental Premotor Interneurons Regulates the Speed of Axial Locomotion in Drosophila Larvae

“…The behavior is generated by a coordinated wave of motor activity from posterior to anterior segments [22][23][24][25][26][27][28][29][30][31]. In normal conditions at room temperature (w25 C), the speed of forward peristalsis is remarkably stereotypic (w1 s/cycle), suggesting that it is rigorously regulated.…”

The impact of odor–reward memory on chemotaxis in larval Drosophila

“…Nonetheless, these animals display diverse capabilities of orientation including chemo-, photo-, and thermotaxis (Luo et al 2010;Gomez-Marin et al 2011;Louis 2012, 2014;Kane et al 2013;Klein et al 2015) as well as associative learning and memory (for review, see Diegelmann et al 2013;Schleyer et al 2013). Here, we specifically investigate how an odor-reward memory influences innate chemotaxis.…”