Distinct memory traces for two visual features in the Drosophila brain

Liu, Gang; Seiler, Holger; Ai, Wen; Zars, Troy; Ito, Kei; Wolf, Ronni; Heisenberg, Martin; Liu, Li

doi:10.1038/nature04381

Cited by 390 publications

(433 citation statements)

References 33 publications

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“…Output from the MB α′β′ neurons and EB neurons have been implicated in olfactory memory consolidation and visual pattern memory (23,(49)(50)(51)(52)(53). Because activity of dopamine neurons and MB α′β′ neurons are required for both oviposition preference for ethanol and ethanol-reward memory in the fly (23), our results raise the possibility that competing dopamine responses may also modulate memory for ethanol reward.…”

Section: Discussionmentioning

confidence: 69%

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Azanchi

Kaun

Heberlein

2013

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

100

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The neural circuits that mediate behavioral choice evaluate and integrate information from the environment with internal demands and then initiate a behavioral response. Even circuits that support simple decisions remain poorly understood. In Drosophila melanogaster, oviposition on a substrate containing ethanol enhances fitness; however, little is known about the neural mechanisms mediating this important choice behavior. Here, we characterize the neural modulation of this simple choice and show that distinct subsets of dopaminergic neurons compete to either enhance or inhibit egg-laying preference for ethanol-containing food. Moreover, activity in α′β′ neurons of the mushroom body and a subset of ellipsoid body ring neurons (R2) is required for this choice. We propose a model where competing dopaminergic systems modulate oviposition preference to adjust to changes in natural oviposition substrates.I n nature, rotting fruit is the social hub for the fruit fly Drosophila melanogaster. Flies use fermenting fruit as a food source (1) and a site for oviposition (2). The choice of a suitable oviposition substrate is an ecologically important decision with a direct impact on species fitness. However, other than having a clear preference for fermenting fruit, how females choose oviposition sites in nature is largely unknown.One of the main metabolites of fermentation is ethanol, which is present in ripe fleshy fruits (3). Although ethanol concentrations in the fruit are rather low [≤5% (vol/vol)] (4), plumes containing ethanol vapor can act as long-distance signals to attract flies to rotting fruit (3, 5). When given the choice, female flies prefer to lay their eggs on media containing low concentrations of ethanol (up to 5%) (6), which leads to enhanced fitness of the developing larva and the adult fly.D. melanogaster's resistance to ethanol toxicity may have evolved to allow inhabitation of ethanol-containing environments (7). For example, adult flies allowed to mate on ethanolcontaining media improve mating success and fecundity (8). Although rearing larvae on food containing relatively high ethanol concentrations delays development and decreases survival (9-11), larvae reared on low concentrations of ethanol develop into heavier adults (7,12). This weight increase may be a result of D. melanogaster larvae metabolizing ethanol and using it as a food source (12). Ingestion of ethanol during the larval stage has additional benefits, such as protection from natural parasites such as endoparasitoid wasps (13).Studies on the neural circuits underlying the oviposition program and choice of oviposition substrates have been initiated only recently in D. melanogaster (14, 15). Ethanol is a particularly intriguing stimulus for oviposition preference, because it has, depending on concentration, both beneficial and detrimental effects on developing larvae. In flies, the function of dopaminergic neurons has been implicated in responses to both rewarding and aversive stimuli (16-19), making it a candidate neuromodulator to signa...

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Section: Discussionmentioning

confidence: 69%

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Azanchi

Kaun

Heberlein

2013

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

100

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“…Whereas sensory neuron function was essential for the rhythmic crawling, larvae immobilized by exposure to 37°C still exhibited movements of the mouth hook (SI Movie 3), indicating that some other type of movement remains. To corroborate these results, we used Gal80 ts /UAS-inwardly rectifying K ϩ channel (Kir) as an alternative means to silence all sensory neurons conditionally at third larval instar by acutely overexpressing Kir so that the neurons would be much less excitable (19). We found that larvae carrying both SN-Gal4 and Gal80 ts /UAS-Kir became immobilized after exposure to restrictive temperature for 30 min (data not shown).…”

Section: Drosophila Larval Sensory Neurons Are Necessary For Locomotionmentioning

confidence: 75%

Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae

Song

Onishi

Jan

2007

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

167

178

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From breathing to walking, rhythmic movements encompass physiological processes important across the entire animal kingdom. It is thought by many that the generation of rhythmic behavior is operated by a central pattern generator (CPG) and does not require peripheral sensory input. Sensory feedback is, however, required to modify or coordinate the motor activity in response to the circumstances of actual movement. In contrast to this notion, we report here that sensory input is necessary for the generation of Drosophila larval locomotion, a form of rhythmic behavior. Blockage of all peripheral sensory inputs resulted in cessation of larval crawling. By conditionally silencing various subsets of larval peripheral sensory neurons, we identified the multiple dendritic (MD) neurons as the neurons essential for the generation of rhythmic peristaltic locomotion. By recording the locomotive motor activities, we further demonstrate that removal of MD neuron input disrupted rhythmic motor firing pattern in a way that prolonged the stereotyped segmental motor firing duration and prevented the propagation of posterior to anterior segmental motor firing. These findings reveal that MD sensory neuron input is a necessary component in the neural circuitry that generates larval locomotion.rhythmic behavior ͉ sensory feedback ͉ locomotion generation ͉ motor pattern ͉ central pattern generator R hythmic behaviors comprise a cyclic, repetitive set of movements, such as locomotion, respiration, and mastication (1, 2). The prevailing model for the neural basis underlying rhythmic behavior is that all rhythmic movements are generated by specialized circuits within the CNS called central pattern generators (CPGs), which can operate without sensory inputs (3-5). Nevertheless, a functional motor program also requires sensory inputs reporting peripheral feedback due to the actual movements to produce the correct behavior (6, 7). This model draws support from reports of sensory feedback affecting the timing and magnitude of motor activity generated by CPGs and from studies based on surgical removal of afferent input (1, 4, 6, 7). Whereas there are electrophysiological demonstrations of the influence of sensory feedback on the output of CPGs, how interactions between sensory neurons in the peripheral and neurons in the CNS contribute to rhythmic behavior in an intact organism is not known. It is therefore important to ask whether sensory inputs are essential for rhythmic behavior and how sensory inputs contribute to rhythmic behavior.Drosophila is ideal for investigations of neural circuits underlying rhythmic behavior due to its amenability to genetic manipulation. Larval crawling, used for travel across various types of terrain, is accomplished by repeated peristaltic wave-like strides (8) and involves molecules mediating neuronal signaling (9-12). Whereas one study suggests that embryonic assembly of CPG for larval locomotion does not require sensory inputs, the same study reports that interference with the sensory function during embry...

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“…The strong expression of dNR2 in ellipsoid body interested us, as another closely-related substructure of the central complex, the fanshaped body, appears to subserve a short-term memory trace for visual learning 25 and may be involved with LTM formation after courtship conditioning 26 . We identified several GAL4 drivers with preferential expression in these dNR2-positive ellipsoid body neurons ( Fig.…”

Section: Resultsmentioning

confidence: 96%

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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In humans and many other animals, memory consolidation occurs through multiple temporal phases and usually involves more than one neuroanatomical brain system. Genetic dissection of Pavlovian olfactory learning in Drosophila melanogaster has revealed multiple memory phases, but the predominant view holds that all memory phases occur in mushroom body neurons. Here, we demonstrate an acute requirement for NMDA receptors (NMDARs) outside of the mushroom body during long-term memory (LTM) consolidation. Targeted dsRNA-mediated silencing of Nmdar1 and Nmdar2 (also known as dNR1 or dNR2, respectively) in cholinergic R4m-subtype large-field neurons of the ellipsoid body specifically disrupted LTM consolidation, but not retrieval. Similar silencing of functional NMDARs in the mushroom body disrupted an earlier memory phase, leaving LTM intact. Our results clearly establish an anatomical site outside of the mushroom body involved with LTM consolidation, thus revealing both a distributed brain system subserving olfactory memory formation and the existence of a system-level memory consolidation in Drosophila.Pavlovian olfactory learning in Drosophila creates an elemental associative memory in a simple, accessible insect brain. This form of behavioral plasticity requires the normal function of NMDARs 1 , as is the case in other invertebrate and vertebrate species 2,3 . Memory formation in flies thereafter proceeds through several temporal phases and involves multiple biochemical cascades, which is again similar to findings from other animal models 4-6 . In particular, spaced training produces stronger, longer-lasting memory than massed training, which is a common property of memory formation 7,8 . Contrary to the fact that memory storage involves multiple anatomical regions in other animal models 9 , olfactory memory has been proposed to be stored predominantly in the mushroom body neurons 5,10 .The mushroom body is a prominent neuropillar structure in the insect central brain. Intrinsic mushroom body cells send neurites ventrally into the calyx, a region of dendritic arborization that is innervated by efferents from several different regions, including projection neurons from the antennal lobes 11 . Mushroom body axons project rostrally as a densely packed and stalk-like structure called the pedunculus to the anterior face of the brain, where they split and give rise to the dorsally projecting a and a¢ lobes and the medially projecting b, b¢ and g lobes 12 . Output neurons from the mushroom body project to many parts of the central brain. Another prominent neuropil is the central complex, which consists of four substructures, the ellipsoid body, the fan-shaped body, the nodulii and the protocerebral bridge. The central complex lies in the central brain between the pedunculi of the mushroom body and is bounded laterally by the two antennoglomerular tracts, dorsally by the pars intercerebralis, ventrally by the esophagus and the great commissure and frontally by the median bundle and the b-lobes of the mushroom bodies fronta...

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Distinct memory traces for two visual features in the Drosophila brain

Cited by 390 publications

References 33 publications

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

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