Adult and larval photoreceptors use different mechanisms to specify the same Rhodopsin fates

Sprecher, Simon G.; Pichaud, Franck; Desplan, Claude

doi:10.1101/gad.1565407

Cited by 62 publications

(104 citation statements)

References 59 publications

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“…The squares were 3.6 cm wide, and the intensity was 70 W/m 2 for bright squares and 1.4 W/m 2 for dark squares, conditions that evoke robust light avoidance (21,22). Each larva began the assay in a light square, and for each boundary crossing during 10 min of observation, we recorded whether the larva crossed into dark or light squares.…”

Section: Methodsmentioning

confidence: 99%

“…For thermal fluctuation experiments, groups of ∼20 larvae were placed evenly on a 300-μm-thick agar surface and imaged at 14 Hz on a 5-megapixel CCD camera (Basler). Larvae were illuminated with four custom-built LED bars arranged in a square around the gel; the illumination wavelength was 624 nm, outside the range visible to larval photosensors (22). For the Channelrhodopsin CsChrimson optogenetic activation experiments, larvae were instead illuminated with infrared LED bars (875 nm), with images recorded at 4 Hz; the red light used to induce neuronal activity was 624 nm with an intensity of 1.9 W/m 2 .…”

Section: Methodsmentioning

confidence: 99%

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Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Klein

Afonso

Vonner

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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152

206

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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...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Klein

Afonso

Vonner

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

152

206

View full text Add to dashboard Cite

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“…2a) 1 . The eyelet of these animals is not affected and three or four cells express Rh6 normally (Fig.…”

mentioning

confidence: 99%

“…transcription factor, Orthodenticle (Otd), expressed in all larval photoreceptors, acts only in the Rh5 subtype to promote Rh5 expression and to repress Rh6 (refs 1,11 ).…”

mentioning

confidence: 99%

Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons

Sprecher

Desplan

2008

Nature

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106

124

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Specificity of sensory neurons requires restricted expression of one sensory receptor gene and the exclusion of all others within a given cell. In the Drosophila retina, functional identity of photoreceptors depends on light-sensitive Rhodopsins (Rhs). The much simpler larval eye (Bolwig organ) is composed of about 12 photoreceptors, eight of which are green-sensitive (Rh6) and four blue-sensitive (Rh5) 1 . The larval eye becomes the adult extraretinal 'eyelet' composed of four greensensitive (Rh6) photoreceptors 2,3 . Here we show that, during metamorphosis, all Rh6 photoreceptors die, whereas the Rh5 photoreceptors switch fate by turning off Rh5 and then turning on Rh6 expression. This switch occurs without apparent changes in the programme of transcription factors that specify larval photoreceptor subtypes. We also show that the transcription factor Senseless (Sens) mediates the very different cellular behaviours of Rh5 and Rh6 photoreceptors. Sens is restricted to Rh5 photoreceptors and must be excluded from Rh6 photoreceptors to allow them to die at metamorphosis. Finally, we show that Ecdysone receptor (EcR) functions autonomously both for the death of larval Rh6 photoreceptors and for the sensory switch of Rh5 photoreceptors to express Rh6. This fate switch of functioning, terminally differentiated neurons provides a novel, unexpected example of hard-wired sensory plasticity.The adult Drosophila eyelet comprises approximately four photoreceptors located between the retina and the optic ganglia 2 . It directly contacts the pacemaker neurons of the adult fly, the lateral neurons 4 . In conjunction with the compound eye and the clock-neuron intrinsic bluesensitive receptor cryptochrome 3 it helps shift the phase of the molecular clock in response to light. All eyelet photoreceptors express green-sensitive Rh6, and are derived from photoreceptors of the larval eye 2,5,6 that mediate light avoidance and entrainment of the molecular clock by innervating the larval lateral neurons 7-9 .Larval photoreceptors develop in a two-step process during embryogenesis 1,10 . Primary precursors are specified first and develop as the four Rh5-subtype photoreceptors. They signal through Epidermal growth factor receptor (EGFR) to the surrounding tissue to develop as secondary precursors, which develop into the eight Rh6-subtype photoreceptors 1 . Two transcription factors specify larval photoreceptor subtypes 1 . Spalt (Sal) is exclusively expressed in Rh5 photoreceptors, where it is required for Rh5 expression. Seven-up (Svp) is restricted to Rh6 photoreceptors, where it represses sal and promotes Rh6 expression. A third

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“…In the BO, there are only two photoreceptor sub-types (Figs. 6d and 8) (Sprecher et al 2007). Three to four photoreceptors express a blue-sensitive opsin and differentiate first.…”

Section: Evolutionary History Of the Drosophila Larval Eyesmentioning

confidence: 99%

Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling

Buschbeck

Friedrich

2008

Evo Edu Outreach

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The visual organs of insects are known for their impressive evolutionary conservation. Compound eyes built from ommatidia with four cone cells are now accepted to date back to the last common ancestor of insects and crustaceans. In species as different as fruit flies and tadpole shrimps, the stepwise cellular patterning steps of the early compound eye exhibit detailed similarities implying 500 million years of developmental conservation. Strikingly, there is also a cryptic diversity of insect visual organs, which gives proof to evolution's versatility in molding even the most tenacious structures into something new. We explore this fascinating aspect in regard to the structure and function of a variety of different insect eyes. This includes work on the unique compound-single-chamber combination eye of twistedwinged insects and the bizarre evolutionary trajectories of specialized larval eyes in endopterygote insects.

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Adult and larval photoreceptors use different mechanisms to specify the same Rhodopsin fates

Cited by 62 publications

References 59 publications

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Sensory determinants of behavioral dynamics in Drosophila thermotaxis

Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons

Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling

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