Circadian rhythms in olfactory responses of Drosophila melanogaster

Olfactory responses of Drosophila undergo pronounced changes after eclosion. The flies develop attraction to odors to which they are exposed and aversion to other odors. Behavioral adaptation is correlated with changes in the firing pattern of olfactory receptor neurons (ORNs). In this article, we present an information-theoretic analysis of the firing pattern of ORNs. Flies reared in a synthetic odorless medium were transferred after eclosion to three different media: (i) a synthetic medium relatively devoid of odor cues, (ii) synthetic medium infused with a single odorant, and (iii) complex cornmeal medium rich in odors. Recordings were made from an identified sensillum (type II), and the Jensen-Shannon divergence (D JS ) was used to assess quantitatively the differences between ensemble spike responses to different odors. Analysis shows that prolonged exposure to ethyl acetate and several related esters increases sensitivity to these esters but does not improve the ability of the fly to distinguish between them. Flies exposed to cornmeal display varied sensitivity to these odorants and at the same time develop greater capacity to distinguish between odors. Deprivation of odor experience on an odorless synthetic medium leads to a loss of both sensitivity and acuity. Rich olfactory experience thus helps to shape the ORNs response and enhances its discriminative power. The experiments presented here demonstrate an experience-dependent adaptation at the level of the receptor neuron.imaginal conditioning | sensory adaptation | odor imprinting | JensenShannon divergence | chemo receptor tuning O lfaction in the fruit fly, Drosophila melanogaster, is crucial for a variety of behaviors, including associative learning (1, 2), courtship (3), foraging (4), and flight (5, 6). Odorants are detected by approximately 1,300 olfactory receptor neurons (ORNs), which are housed in sensilla on the third antennal segment and individually express one of approximately 50 functional odor receptors in adults (7-9). All ORNs expressing the same olfactory receptor project to one of approximately 50 glomeruli in the antennal lobe, where they synapse with a set of projection neurons (PNs) (10, 11). The activity of ORNs, either excitation or inhibition, provides behaviorally relevant information about odorants such as their identity, concentration, and source. The information transduced by an ORN is processed in the antennal lobe (12, 13) and sent via PNs to the mushroom bodies, which are believed to be centers for olfactory learning and memory (14, 15).Experience-dependent modifiability (i.e., plasticity) of olfactory representation at the level of the central nervous system is well known (2,16,17). Relatively little attention has been paid to long-term changes in sensory neuron activity resulting from odor experiences. It was previously shown that exposure of newly born imago to a particular set of odorants alters their responses to these odors (18,19). The flies develop an attraction to the chemicals to which they are exposed and an av...

Section: Discussionsupporting

confidence: 62%

Post-eclosion odor experience modifies olfactory receptor neuron coding in Drosophila

Iyengar

Chakraborty

Goswami

et al. 2010

“…In addition, the oscillators are clearly independent of the central circadian oscillator(s) in the brain (15,16). Previous reports revealed that the peripheral oscillator shares the same genes with the central clock in the brain (12,17). However, there is a remarkable difference that, in the peripheral oscillator, CRY functions as a core component besides a photoreceptor.…”

mentioning

confidence: 81%

Peripheral circadian clock for the cuticle deposition rhythm in Drosophila melanogaster

Ito

Goto

Shiga

et al. 2008

Insect endocuticle thickens after adult emergence by daily alternating deposition of two chitin layers with different orientation. Although the cuticle deposition rhythm is known to be controlled by a circadian clock in many insects, the site of the driving clock, the photoreceptor for entrainment, and the oscillatory mechanism remain elusive. Here, we show that the cuticle deposition rhythm is regulated by a peripheral oscillator in the epidermis in Drosophila melanogaster. Free-running and entrainment experiments in vitro reveal that the oscillator for the cuticle deposition rhythm is independent of the central clock in the brain driving the locomotor rhythms. The cuticle deposition rhythm is absent in null and dominant-negative mutants of clock genes (i.e., period, timeless, cycle, and Clock), indicating that this oscillator is composed of the same clock genes as the central clock. Entrainment experiments with monochromatic light-dark cycles and cry b flies reveal that a blue light-absorbing photoreceptor, cryptochrome (CRY), acts as a photoreceptor pigment for the entrainment of the cuticle deposition rhythm. Unlike other peripheral rhythms in D. melanogaster, the cuticle deposition rhythm persisted in cry b and cry OUT mutant flies, indicating that CRY does not play a core role in the rhythm generation in the epidermal oscillator.circadian rhythm ͉ clock genes ͉ cryptochrome ͉ entrainment ͉ epidermal cell C ircadian clocks control daily rhythms at the molecular, physiological, and behavioral levels. Like most organisms, the central circadian oscillator controlling the locomotor activity rhythm in Drosophila is proposed to consist of molecular feedback loops. The feedback loops comprise several core clock genes, such as period (per), timeless (tim), Clock (Clk), and cycle (cyc) (1). These genes encode PER, TIM, CLK, and CYC proteins, respectively, and loss-of-function or dominant-negative mutations in these genes result in loss of normal circadian rhythmicity (2-5). CLK and CYC form a heterodimer to activate transcription of per and tim (2, 4, 6). PER and TIM form another heterodimer, are transferred into the nucleus, and then inactivate the transcriptional activity of the CLK/CYC heterodimer (6). The feedback loops are entrained and reset by the lightinduced degradation of TIM mediated by a photoreceptor pigment, cryptochrome (CRY) (7-10).In addition to the central oscillator, peripheral oscillators exist in many tissues, including the compound eyes, antennae, wings, legs, and Malpighian tubules in adults and the ring gland in pupae (11)(12)(13)(14). These oscillators are self-sustained and directly light-entrainable even in vitro (11-13). In addition, the oscillators are clearly independent of the central circadian oscillator(s) in the brain (15, 16). Previous reports revealed that the peripheral oscillator shares the same genes with the central clock in the brain (12, 17). However, there is a remarkable difference that, in the peripheral oscillator, CRY functions as a core component besides a photorecepto...

“…The mating-activity rhythm of D. melanogaster females is under the restricted control of circadian clock genes, and the lateral neurons might be essential to generate the rhythm. Flies, especially males, use olfactory cues for mating (28 -30), and the circadian rhythm of the olfactory response is robust in Drosophila (31). Olfactory responses of the wild-type were elevated in the middle of the night in LD cycles (31), but mating activities were decreased during the early part of the night (Fig.…”

Section: Resultsmentioning

confidence: 99%

Circadian rhythms of female mating activity governed by clock genes in Drosophila

Sakai

Ishida

2001

234

204

The physiological and behavioral activities of many animals are restricted to specific times of the day. The daily fluctuation in the mating activity of some insects is controlled by an endogenous clock, but the genetic mechanism that controls it remains unknown. Here we demonstrate that wild-type Drosophila melanogaster display a robust circadian rhythm in the mating activity, and that these rhythms are abolished in period-or timeless-null mutant flies (per 01 and tim 01 ). Circadian rhythms were lost when rhythm mutant females were paired with wild-type males, demonstrating that female mating activity is governed by clock genes. Furthermore, we detected an antiphasic relationship in the circadian rhythms of mating activity between D. melanogaster and its sibling species Drosophila simulans. Female-and species-specific circadian rhythms in the mating activity of Drosophila seem to cause reproductive isolation.M ost organisms show circadian 24-h rhythmicity in their behavior and physiology. Various behavioral phenomena in insects are controlled by an endogenous clock (1). A core oscillator mechanism of circadian rhythm and feedback loops, involving several clock genes including period (per) and timeless (tim), control locomotor activity and eclosion of the fruit fly, Drosophila melanogaster (2-6). Mutants of D. melanogaster with defective feedback loops (7-10) provide the means of studying the relationship between behavioral rhythms and circadian clock genes.Mating by animals is the most important and fundamental process to select the best partner and to produce progeny. Insects in particular show daily rhythms in mating activity (11)(12)(13)(14)(15)(16)(17), and these are controlled in some by an endogenous clock (14,15). Mating activity of the fruit fly Drosophila mercatorum shows the daily rhythms of the mating activity under 12-h͞12-h light͞dark (LD) cycles (16), and several Drosophila species show the daily rhythms of male courtship under LD cycles (17). However, the genetic mechanism(s) that modulates mating rhythm in these insects remains unknown.The present study shows that wild-type D. melanogaster display a robust circadian rhythm in mating activity that is governed by clock genes and that females are responsible for generating the mating rhythms. Furthermore, we found that the mating activities of disconnected (disco) mutants, which have a severe defect in the optic lobe and are missing lateral neurons, are arrhythmic. We also identified an antiphasic relationship in the circadian rhythms of the mating activity between D. melanogaster and its sibling species, Drosophila simulans. Materials and MethodsFly Strains. D. melanogaster wild-type strains (Canton-S and OGS-4, Ogasawara, Japan), rhythm mutants [period 01 (per 01 ), timeless 01 (tim 01 ), and disconnected 3 forked (disco 3 f )], transgenic flies (hsp-per s13) carrying heat shock (HS)-inducible per coding sequences (18), forked ( f ) mutant, and D. simulans wild-type strains (Og, Ogasawara, Japan; and Ots, Otsuki, Japan) were grown on glucose͞yea...