Distinct Visual Pathways MediateDrosophilaLarval Light Avoidance and Circadian Clock Entrainment

Abstract

Visual organs perceive environmental stimuli required for rapid initiation of behaviors and can also entrain the circadian clock. The larval eye of Drosophila is capable of both functions. Each eye contains only 12 photoreceptors (PRs), which can be subdivided into two subtypes. Four PRs express blue-sensitive rhodopsin5 (rh5) and eight express green-sensitive rhodopsin6 (rh6). We found that either PR-subtype is sufficient to entrain the molecular clock by light, while only the Rh5-PR subtype is essential for light avoidance. Acetylcholine (ACh) released from PRs confers both functions. Both subtypes of larval PRs innervate the main circadian pacemaker neurons of the larva, the PDF-expressing lateral neurons (LNs), providing sensory input to control circadian rhythms. However, we show that PDF-expressing LNs are dispensable for light avoidance, and a distinct set of three clock neurons is required. Thus we have identified distinct sensory and central circuitry regulating light avoidance behavior and clock entrainment. Our findings provide insights into the coding of sensory information for distinct behavioral functions and the underlying molecular and neuronal circuitry.

Sensorimotor structure of Drosophila larva phototaxis

“…6C and Movie S6). We hypothesize that the opaque cephalopharyngeal skeleton restricts the accessibility of incident light onto the BO, effectively forming a pigment cup eye (17,24), as has been proposed in Calliphora larvae (25). When an animal is crawling with a 180°heading or a 0°heading relative to the incidence of light, it experiences a relative minimum or maximum of apparent luminosity, respectively (Fig.…”

“…The BO is comprised of 12 PRs; eight express Rh6, and four express Rh5. We and others have found that the Rh6 cells are dispensable for phototaxis (17). All PRs extend their axons to the larval optic neuropil (LON).…”

“…2C). We presented larvae with a temporal analog of the checkerboard, a temporal squarewave light stimulus (8,16) (17). The temporal square-wave setup also revealed a distinct photosensory behavior: pausing in response to an abrupt decrease in light intensity (cessation of forward movement without initiation of head-sweeps) ( Fig.…”

“…The LNs along with two dorsal neurons (DN1 and DN2) constitute the clock neurons that are involved in Rh6-dependent circadian rhythms (Fig. 8A) (17). The LNs have been implicated in phototaxis in a spatial gradient assay (17,27); however the relative contribution of each of these downstream neuronal types to specific phototactic responses has not yet been dissected.…”

“…8A) (17). The LNs have been implicated in phototaxis in a spatial gradient assay (17,27); however the relative contribution of each of these downstream neuronal types to specific phototactic responses has not yet been dissected. The LN population consists of four pigment-dispersing factor (PDF)-positive cells and one PDF-negative cell, the fifth LN.…”