Photic input pathways that mediate the <i>Drosophila</i> larval response to light and circadian rhythmicity are developmentally related but functionally distinct

Hassan, Jana A.; Iyengar, Balaji; Scantlebury, Nadia; Moncalvo, Veronica Rodriguez; Campos, Ana Regina Nascimento

doi:10.1002/cne.20383

Cited by 31 publications

(49 citation statements)

References 54 publications

(62 reference statements)

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“…Because of the limits of the projector's dynamic range, we could not increase the steepness of the gradient without significantly reducing the size of the experimental arena, so we turned to temporal gradients using triangle waveforms to mimic the stimulus received by larvae moving in straight lines on illumination patterns with a steeper linear spatial gradient. In our previous studies of spatial and temporal gradients of temperature (3)(4)(5)(6)(7)(8)(9)14), odor, and carbon dioxide (10, 11), we found that temporal triangle waves evoked the same behavioral responses as linear spatial gradients.…”

Section: Significancementioning

confidence: 64%

“…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)(4)(5)(6)(7)(8)(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).…”

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confidence: 99%

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Sensorimotor structure of Drosophila larva phototaxis

Kane

Gershow

Afonso

et al. 2013

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

119

216

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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...

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Section: Significancementioning

confidence: 64%

mentioning

confidence: 99%

Sensorimotor structure of Drosophila larva phototaxis

Kane

Gershow

Afonso

et al. 2013

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

119

216

View full text Add to dashboard Cite

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“…The central nervous system was dissected from early foraging third instar larvae staged as above and treated as described previously (Hassan et al, 2005). The primary antibody used was rabbit antiphospho-Histone H3 (1:1000 dilution; catalogue no.…”

Section: Immunohistochemistry and Imagingmentioning

confidence: 99%

Insulin signalling in mushroom body neurons regulates feeding behaviour inDrosophilalarvae

Zhao

Campos

2012

Journal of Experimental Biology

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SUMMARYWhereas the pivotal role of insulin signalling in cell division, growth and differentiation is well documented, its role in the regulation of neuronal function and behaviour has recently become the focus of intense investigation. The simple organization of the Drosophila larval brain and the availability of genetic tools to impair the function of insulin receptor signalling in a spatially specific manner makes Drosophila an attractive model to investigate the role of the insulin pathway in specific behaviours. Here, we show that impairment of insulin signalling in the mushroom body neurons, a structure involved in associative learning, impairs feeding behaviour in the Drosophila larva.

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“…However, the fifth LN might be involved in RH5-dependent acute larval responses to light, which do not require the PDF ϩ LNs (Hassan et al, 2005;Keene et al, 2011). The entrainment of the fifth LN in the absence of both CRY and the PDF ϩ LNs suggests a direct connection to the visual system, in agreement with its arborization in the larval optic neuropil.…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, both photoreceptor types are equally able to suppress TIM levels in the LNs after a 2 h light exposure at the beginning of the night (Keene et al, 2011). In contrast, RH5 fibers alone specifically mediate acute larval responses to light (Hassan et al, 2005;Keene et al, 2011), while RH6 fibers alone are specifically required for the development of a serotonergic arborization that also contacts the LNs (Rodriguez Moncalvo and Campos, 2005). That RH6 activation strongly disrupts molecular oscillations in the LNs even in RR was, however, not anticipated.…”

Section: Discussionmentioning

confidence: 99%

Identifying Specific Light Inputs for Each Subgroup of Brain Clock Neurons inDrosophilaLarvae

Klarsfeld¹,

Picot²,

Vias³

et al. 2011

J. Neurosci.

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In Drosophila, opsin visual photopigments as well as blue-light-sensitive cryptochrome (CRY) contribute to the synchronization of circadian clocks. We focused on the relatively simple larval brain, with nine clock neurons per hemisphere: five lateral neurons (LNs), four of which express the pigment-dispersing factor (PDF) neuropeptide, and two pairs of dorsal neurons (DN1s and DN2s). CRY is present only in the PDF-expressing LNs and the DN1s. The larval visual organ expresses only two rhodopsins (RH5 and RH6) and projects onto the LNs. We recently showed that PDF signaling is required for light to synchronize the CRY Ϫ larval DN2s. We now show that, in the absence of functional CRY, synchronization of the DN1s also requires PDF, suggesting that these neurons have no direct connection with the visual system. In contrast, the fifth (PDF Ϫ ) LN does not require the PDF-expressing cells to receive visual system inputs. All clock neurons are light-entrained by light-dark cycles in the rh5 2 ;cry b , rh6 1 cry b , and rh5 2 ;rh6 1 double mutants, whereas the triple mutant is circadianly blind. Thus, any one of the three photosensitive molecules is sufficient, and there is no other light input for the larval clock. Finally, we show that constant activation of the visual system can suppress molecular oscillations in the four PDF-expressing LNs, whereas, in the adult, this effect of constant light requires CRY. A surprising diversity and specificity of light input combinations thus exists even for this simple clock network.

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Photic input pathways that mediate the Drosophila larval response to light and circadian rhythmicity are developmentally related but functionally distinct

Cited by 31 publications

References 54 publications

Sensorimotor structure of Drosophila larva phototaxis

Sensorimotor structure of Drosophila larva phototaxis

Insulin signalling in mushroom body neurons regulates feeding behaviour inDrosophilalarvae

Identifying Specific Light Inputs for Each Subgroup of Brain Clock Neurons inDrosophilaLarvae

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