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1.  Aversive Learning and Appetitive Motivation Toggle Feed-Forward Inhibition in the Drosophila Mushroom Body 
Neuron  2016;90(5):1086-1099.
In Drosophila, negatively reinforcing dopaminergic neurons also provide the inhibitory control of satiety over appetitive memory expression. Here we show that aversive learning causes a persistent depression of the conditioned odor drive to two downstream feed-forward inhibitory GABAergic interneurons of the mushroom body, called MVP2, or mushroom body output neuron (MBON)-γ1pedc>α/β. However, MVP2 neuron output is only essential for expression of short-term aversive memory. Stimulating MVP2 neurons preferentially inhibits the odor-evoked activity of avoidance-directing MBONs and odor-driven avoidance behavior, whereas their inhibition enhances odor avoidance. In contrast, odor-evoked activity of MVP2 neurons is elevated in hungry flies, and their feed-forward inhibition is required for expression of appetitive memory at all times. Moreover, imposing MVP2 activity promotes inappropriate appetitive memory expression in food-satiated flies. Aversive learning and appetitive motivation therefore toggle alternate modes of a common feed-forward inhibitory MVP2 pathway to promote conditioned odor avoidance or approach.
•Aversive learning reduces odor-specific feed-forward inhibition in mushroom body•Feed-forward inhibition selectively inhibits avoidance-directing neural pathways•Appetitive motivation increases feed-forward inhibition in the mushroom body•Imposing feed-forward inhibition favors appetitive memory expression
Fruit fly memory and its state-dependent behavioral expression involve modulation of mushroom body output synapses. Perisse et al. demonstrate aversive learning and appetitive motivation toggle alternate modes of feed-forward inhibition in mushroom body, favoring either conditioned avoidance or approach behavior.
PMCID: PMC4893166  PMID: 27210550
2.  Memory-Relevant Mushroom Body Output Synapses Are Cholinergic 
Neuron  2016;89(6):1237-1247.
Memories are stored in the fan-out fan-in neural architectures of the mammalian cerebellum and hippocampus and the insect mushroom bodies. However, whereas key plasticity occurs at glutamatergic synapses in mammals, the neurochemistry of the memory-storing mushroom body Kenyon cell output synapses is unknown. Here we demonstrate a role for acetylcholine (ACh) in Drosophila. Kenyon cells express the ACh-processing proteins ChAT and VAChT, and reducing their expression impairs learned olfactory-driven behavior. Local ACh application, or direct Kenyon cell activation, evokes activity in mushroom body output neurons (MBONs). MBON activation depends on VAChT expression in Kenyon cells and is blocked by ACh receptor antagonism. Furthermore, reducing nicotinic ACh receptor subunit expression in MBONs compromises odor-evoked activation and redirects odor-driven behavior. Lastly, peptidergic corelease enhances ACh-evoked responses in MBONs, suggesting an interaction between the fast- and slow-acting transmitters. Therefore, olfactory memories in Drosophila are likely stored as plasticity of cholinergic synapses.
•Mushroom body Kenyon cell function requires ChAT and VAChT expression•Kenyon cell-released acetylcholine drives mushroom body output neurons•Blocking nicotinic receptors impairs mushroom body output neuron activation•Acetylcholine interacts with coreleased neuropeptide
Fruit fly memory involves plasticity of mushroom body synapses. Barnstedt et al. identified acetylcholine as the mushroom body neurotransmitter. Mushroom body output neuron activation requires nicotinic acetylcholine receptors. Impaired receptor function reduces physiological responses and alters odor-driven behavior.
PMCID: PMC4819445  PMID: 26948892
3.  Remembering Components of Food in Drosophila 
Remembering features of past feeding experience can refine foraging and food choice. Insects can learn to associate sensory cues with components of food, such as sugars, amino acids, water, salt, alcohol, toxins and pathogens. In the fruit fly Drosophila some food components activate unique subsets of dopaminergic neurons (DANs) that innervate distinct functional zones on the mushroom bodies (MBs). This architecture suggests that the overall dopaminergic neuron population could provide a potential cellular substrate through which the fly might learn to value a variety of food components. In addition, such an arrangement predicts that individual component memories reside in unique locations. DANs are also critical for food memory consolidation and deprivation-state dependent motivational control of the expression of food-relevant memories. Here, we review our current knowledge of how nutrient-specific memories are formed, consolidated and specifically retrieved in insects, with a particular emphasis on Drosophila.
PMCID: PMC4759284  PMID: 26924969
insects; Drosophila; dopamine; neural circuits; food; memories; internal states
4.  Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila 
•Dopamine neurons coding opposite value are segregated in the fly brain.•Dopamine neurons representing reward type innervate discrete mushroom body areas.•Mushroom body output neurons are specific to dopaminergic reinforcement zones.•Olfactory learning skews different collections of mushroom body output junctions.•Mushroom bodies are fan-out fan-in circuits like the cerebellum and hippocampus.
Learning permits animals to attach meaning and context to sensory stimuli. How this information is coded in neural networks in the brain, and appropriately retrieved and utilized to guide behavior, is poorly understood. In the fruit fly olfactory memories of particular value are represented within sparse populations of odor-activated Kenyon cells (KCs) in the mushroom body ensemble. During learning reinforcing dopaminergic neurons skew the mushroom body network by driving zonally restricted plasticity at synaptic junctions between the KCs and subsets of the overall small collection of mushroom body output neurons. Reactivation of this skewed KC-output neuron network retrieves memory of odor valence and guides appropriate approach or avoidance behavior.
PMCID: PMC4835525  PMID: 26496148
5.  Understanding the brain by controlling neural activity 
Causal methods to interrogate brain function have been employed since the advent of modern neuroscience in the nineteenth century. Initially, randomly placed electrodes and stimulation of parts of the living brain were used to localize specific functions to these areas. Recent technical developments have rejuvenated this approach by providing more precise tools to dissect the neural circuits underlying behaviour, perception and cognition. Carefully controlled behavioural experiments have been combined with electrical devices, targeted genetically encoded tools and neurochemical approaches to manipulate information processing in the brain. The ability to control brain activity in these ways not only deepens our understanding of brain function but also provides new avenues for clinical intervention, particularly in conditions where brain processing has gone awry.
PMCID: PMC4528814  PMID: 26240417
brain stimulation; behaviour; perception; optogenetics; neurophysiology; neural circuits
6.  Light, heat, action: neural control of fruit fly behaviour 
The fruit fly Drosophila melanogaster has emerged as a popular model to investigate fundamental principles of neural circuit operation. The sophisticated genetics and small brain permit a cellular resolution understanding of innate and learned behavioural processes. Relatively recent genetic and technical advances provide the means to specifically and reproducibly manipulate the function of many fly neurons with temporal resolution. The same cellular precision can also be exploited to express genetically encoded reporters of neural activity and cell-signalling pathways. Combining these approaches in living behaving animals has great potential to generate a holistic view of behavioural control that transcends the usual molecular, cellular and systems boundaries. In this review, we discuss these approaches with particular emphasis on the pioneering studies and those involving learning and memory.
PMCID: PMC4528823  PMID: 26240426
Drosophila; behaviour; cellular resolution; optogenetics; thermogenetics; reporters
7.  Neural correlates of water reward in thirsty Drosophila 
Nature neuroscience  2014;17(11):1536-1542.
Drinking water is innately rewarding to thirsty animals. In addition, the consumed value can be assigned to behavioral actions and predictive sensory cues by associative learning. Here we show that thirst converts water avoidance into water-seeking in naïve Drosophila. Thirst also permits flies to learn olfactory cues paired with water reward. Water learning requires water taste and <40 water-responsive dopaminergic neurons that innervate a restricted zone of the mushroom body γ lobe. These water learning neurons are different from those that are critical to convey the reinforcing effects of sugar. Naïve water-seeking behavior in thirsty flies does not require water taste but relies on another subset of water-responsive dopaminergic neurons that target the mushroom body β′ lobe. Furthermore, these naïve water-approach neurons are not required for learned water-seeking. Our results therefore demonstrate that naïve and learned water-seeking, and water learning, utilize separable neural circuitry in the brain of thirsty flies.
PMCID: PMC4213141  PMID: 25262493
8.  Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila 
Neuron  2015;86(2):417-427.
During olfactory learning in fruit flies, dopaminergic neurons assign value to odor representations in the mushroom body Kenyon cells. Here we identify a class of downstream glutamatergic mushroom body output neurons (MBONs) called M4/6, or MBON-β2β′2a, MBON-β′2mp, and MBON-γ5β′2a, whose dendritic fields overlap with dopaminergic neuron projections in the tips of the β, β′, and γ lobes. This anatomy and their odor tuning suggests that M4/6 neurons pool odor-driven Kenyon cell synaptic outputs. Like that of mushroom body neurons, M4/6 output is required for expression of appetitive and aversive memory performance. Moreover, appetitive and aversive olfactory conditioning bidirectionally alters the relative odor-drive of M4β′ neurons (MBON-β′2mp). Direct block of M4/6 neurons in naive flies mimics appetitive conditioning, being sufficient to convert odor-driven avoidance into approach, while optogenetically activating these neurons induces avoidance behavior. We therefore propose that drive to the M4/6 neurons reflects odor-directed behavioral choice.
•Glutamatergic mushroom body output neurons are required for memory expression•Training bidirectionally alters relative odor drive to output neurons•Blocking glutamatergic mushroom body output neurons mimics appetitive conditioning•Optogenetic activation drives avoidance behavior
Fruit fly olfactory memory involves mushroom body plasticity. Owald et al. identified glutamatergic mushroom body output neurons that are critical for memory expression. Conditioning bidirectionally alters odor drive to these outputs. Blocking them mimics appetitive conditioning, whereas activation induces avoidance behavior.
PMCID: PMC4416108  PMID: 25864636
9.  Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila 
Current Biology  2015;25(6):751-758.
Dopaminergic neurons provide reward learning signals in mammals and insects [1–4]. Recent work in Drosophila has demonstrated that water-reinforcing dopaminergic neurons are different to those for nutritious sugars [5]. Here, we tested whether the sweet taste and nutrient properties of sugar reinforcement further subdivide the fly reward system. We found that dopaminergic neurons expressing the OAMB octopamine receptor [6] specifically convey the short-term reinforcing effects of sweet taste [4]. These dopaminergic neurons project to the β′2 and γ4 regions of the mushroom body lobes. In contrast, nutrient-dependent long-term memory requires different dopaminergic neurons that project to the γ5b regions, and it can be artificially reinforced by those projecting to the β lobe and adjacent α1 region. Surprisingly, whereas artificial implantation and expression of short-term memory occur in satiated flies, formation and expression of artificial long-term memory require flies to be hungry. These studies suggest that short-term and long-term sugar memories have different physiological constraints. They also demonstrate further functional heterogeneity within the rewarding dopaminergic neuron population.
•Sweet taste and nutrient value recruit different reinforcing dopaminergic neurons•Sweetness and nutrient value separately reinforce short- and long-term memories•Reinforcement of short-term memory is not dependent on the state of hunger•Acquisition and retrieval of long-term memory are hunger state dependent
A small number of dopaminergic neurons in the fly brain are crucial for appetitive memory reinforcement. Huetteroth et al. further subdivide these rewarding neurons into those required for sweet taste reinforcement of short-term memory, nutrient-dependent long-term memory, and others that can artificially reinforce food-independent long-term memory.
PMCID: PMC4372253  PMID: 25728694
10.  Drosophila Learn Opposing Components of a Compound Food Stimulus 
Current Biology  2014;24(15):1723-1730.
Dopaminergic neurons provide value signals in mammals and insects [1–3]. During Drosophila olfactory learning, distinct subsets of dopaminergic neurons appear to assign either positive or negative value to odor representations in mushroom body neurons [4–9]. However, it is not known how flies evaluate substances that have mixed valence. Here we show that flies form short-lived aversive olfactory memories when trained with odors and sugars that are contaminated with the common insect repellent DEET. This DEET-aversive learning required the MB-MP1 dopaminergic neurons that are also required for shock learning [7]. Moreover, differential conditioning with DEET versus shock suggests that formation of these distinct aversive olfactory memories relies on a common negatively reinforcing dopaminergic mechanism. Surprisingly, as time passed after training, the behavior of DEET-sugar-trained flies reversed from conditioned odor avoidance into odor approach. In addition, flies that were compromised for reward learning exhibited a more robust and longer-lived aversive-DEET memory. These data demonstrate that flies independently process the DEET and sugar components to form parallel aversive and appetitive olfactory memories, with distinct kinetics, that compete to guide learned behavior.
•Flies trained with unpalatable sugar learn the sweet-, nutrient, and bad-taste qualities•Distinct dopamine neurons reinforce the positive and negative memories in parallel•Early conditioned aversion switches to longer-lasting nutrient-memory-guided attraction•Flies remember individual qualities of a complex food source
Das et al. show that flies trained with unpalatable sugar learn both the nutritional and bad-taste qualities. Opposing memories are reinforced in parallel by distinct dopaminergic neurons. Conditioned behavior is initially aversive but soon switches to approach led by the longer-lasting nutrient-reinforced appetitive memory.
PMCID: PMC4131107  PMID: 25042590
11.  Reinforcement signaling in Drosophila; dopamine does it all after all 
Current opinion in neurobiology  2013;23(3):10.1016/j.conb.2013.01.005.
Reinforcement systems are believed to drive synaptic plasticity within neural circuits that store memories. Recent evidence from the fruit fly suggests that anatomically distinct dopaminergic neurons ultimately provide the key instructive signals for both appetitive and aversive learning. This dual role for dopamine overturns the previous model that octopamine signaled reward and dopamine punishment. More importantly, this anatomically segregated double role for dopamine in reward and aversion mirrors that emerging in mammals. Therefore, an antagonistic organization of distinct reinforcing dopaminegic neurons is a conserved feature of brains. It now seems crucial to understand how the dopaminergic neurons are controlled and what the released dopamine does to the underlying circuits to convey opposite valence.
PMCID: PMC3887340  PMID: 23391527
12.  Transposition driven genomic heterogeneity in the Drosophila brain* 
Science (New York, N.Y.)  2013;340(6128):10.1126/science.1231965.
Recent studies in mammals have documented neural expression and mobility of retrotransposons and suggested that neural genomes are diverse mosaics. Here we report transposition in memory-relevant neurons in the Drosophila brain. Cell-type specific gene expression profiling revealed transposon expression is more abundant in mushroom body (MB) αβ neurons than in neighboring MB neurons. The PIWI-RNA (piRNA) proteins Aubergine and Argonaute 3, known to suppress transposons in the fly germline, are expressed in the brain and appear less abundant in αβ MB neurons. Loss of piRNA proteins correlates with elevated transposon expression in brain. Lastly, paired-end deep sequencing identified over 200 de novo transposon insertions in αβ neurons, including events into memory-relevant loci. Our observations indicate that genomic heterogeneity is a conserved feature of the brain.
PMCID: PMC3887341  PMID: 23559253
13.  Shocking Revelations and Saccharin Sweetness in the Study of Drosophila Olfactory Memory 
Current Biology  2013;23(17):R752-R763.
It is now almost forty years since the first description of learning in the fruit fly Drosophila melanogaster. Various incarnations of the classic mutagenesis approach envisaged in the early days have provided around one hundred learning defective mutant fly strains. Recent technological advances permit temporal control of neural function in the behaving fly. These approaches have radically changed experiments in the field and have provided a neural circuit perspective of memory formation, consolidation and retrieval. Combining neural perturbations with more classical mutant intervention allows investigators to interrogate the molecular and cellular processes of memory within the defined neural circuits. Here, we summarize some of the progress made in the last ten years that indicates a remarkable conservation of the neural mechanisms of memory formation between flies and mammals. We emphasize that considering an ethologically-relevant viewpoint might provide additional experimental power in studies of Drosophila memory.
PMCID: PMC3770896  PMID: 24028959
14.  Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila 
Neuron  2013;79(5):945-956.
In Drosophila, anatomically discrete dopamine neurons that innervate distinct zones of the mushroom body (MB) assign opposing valence to odors during olfactory learning. Subsets of MB neurons have temporally unique roles in memory processing, but valence-related organization has not been demonstrated. We functionally subdivided the αβ neurons, revealing a value-specific role for the ∼160 αβ core (αβc) neurons. Blocking neurotransmission from αβ surface (αβs) neurons revealed a requirement during retrieval of aversive and appetitive memory, whereas blocking αβc only impaired appetitive memory. The αβc were also required to express memory in a differential aversive paradigm demonstrating a role in relative valuation and approach behavior. Strikingly, both reinforcing dopamine neurons and efferent pathways differentially innervate αβc and αβs in the MB lobes. We propose that conditioned approach requires pooling synaptic outputs from across the αβ ensemble but only from the αβs for conditioned aversion.
•Differential representation of memory valence in Drosophila mushroom body neurons•αβ core neurons are specifically required for conditioned approach behavior•Relative aversive learning requires rewarding dopaminergic reinforcement•Distinct circuits drive learned aversion and approach
Perisse et al. demonstrate that discrete mushroom body neuron populations drive learned approach and avoidance behaviors in the fruit fly. Aversive and appetitive memories for the same odor are therefore represented in different neural ensembles.
PMCID: PMC3765960  PMID: 24012007
15.  Layered reward signaling through octopamine and dopamine in Drosophila 
Nature  2012;492(7429):433-437.
Dopamine (DA) is synonymous with reward and motivation in mammals1,2. However, only recently has dopamine been linked to motivated behavior and rewarding reinforcement in fruit flies3,4. Instead octopamine (OA) has historically been considered the signal for reward in insects5–7. Here we show using temporal control of neural function in Drosophila that only short-term appetitive memory is reinforced by OA. Moreover, OA-dependent memory formation requires signaling through DA neurons. Part of the OA signal requires the α-adrenergic like OAMB receptor in an identified subset of mushroom body (MB)-targeted DA neurons. OA triggers an increase in intracellular calcium in these DA neurons and their direct activation can substitute for sugar to form appetitive memory, even in flies lacking OA. Analysis of the β-adrenergic like Octβ2R receptor reveals that OA-dependent reinforcement also requires an interaction with DA neurons that control appetitive motivation. These data suggest that sweet taste engages a distributed OA signal that reinforces memory through discrete subsets of MB-targeted DA neurons. In addition, they reconcile prior findings with OA and DA and suggest that reinforcement systems in flies are more similar to mammals than previously envisaged.
PMCID: PMC3528794  PMID: 23103875
16.  Layered reward signaling through octopamine and dopamine in Drosophila 
Nature  2012;492(7429):433-437.
Dopamine (DA) is synonymous with reward and motivation in mammals1,2. However, only recently has dopamine been linked to motivated behavior and rewarding reinforcement in fruit flies3,4. Instead octopamine (OA) has historically been considered the signal for reward in insects5-7. Here we show using temporal control of neural function in Drosophila that only short-term appetitive memory is reinforced by OA. Moreover, OA-dependent memory formation requires signaling through DA neurons. Part of the OA signal requires the α-adrenergic like OAMB receptor in an identified subset of mushroom body (MB)-targeted DA neurons. OA triggers an increase in intracellular calcium in these DA neurons and their direct activation can substitute for sugar to form appetitive memory, even in flies lacking OA. Analysis of the β-adrenergic like Octβ2R receptor reveals that OA-dependent reinforcement also requires an interaction with DA neurons that control appetitive motivation. These data suggest that sweet taste engages a distributed OA signal that reinforces memory through discrete subsets of MB-targeted DA neurons. In addition, they reconcile prior findings with OA and DA and suggest that reinforcement systems in flies are more similar to mammals than previously envisaged.
PMCID: PMC3528794  PMID: 23103875
17.  Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling 
Nature Neuroscience  2010;14(2):190-199.
Adrenergic signaling has important roles in synaptic plasticity and metaplasticity. However, the underlying mechanisms of these functions remain poorly understood. We investigated the role of octopamine, the invertebrate counterpart of adrenaline and noradrenaline, in synaptic and behavioral plasticity in Drosophila. We found that an increase in locomotor speed induced by food deprivation was accompanied by an activity- and octopamine-dependent extension of octopaminergic arbors and that the formation and maintenance of these arbors required electrical activity. Growth of octopaminergic arbors was controlled by a cAMP- and CREB-dependent positive-feedback mechanism that required Octpβ2R octopamine autoreceptors. Notably, this autoregulation was necessary for the locomotor response. In addition, octopamine neurons regulated the expansion of excitatory glutamatergic neuromuscular arbors through Octpβ2Rs on glutamatergic motor neurons. Our results provide a mechanism for global regulation of excitatory synapses, presumably to maintain synaptic and behavioral plasticity in a dynamic range.
PMCID: PMC3391700  PMID: 21186359
18.  A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body 
Current biology : CB  2011;21(10):855-861.
Labile memory is thought to be held in the brain as persistent neural network activity [1–4]. However, it is not known how biologically relevant memory circuits are organized and operate. Labile and persistent appetitive memory in Drosophila requires output after training from the α′β′ subset of mushroom body (MB) neurons and from a pair of modulatory Dorsal Paired Medial (DPM) neurons [5–9]. DPM neurons innervate the entire MB lobe region and appear to be pre- and post-synaptic to the MB [7, 8], consistent with a recurrent network model. Here we identify a role after training for synaptic output from the GABAergic Anterior Paired Lateral (APL) neurons [10, 11]. Blocking synaptic output from APL neurons after training disrupts labile memory but does not affect long-term memory. APL neurons contact DPM neurons most densely in the α′β′ lobes although their processes are intertwined and contact throughout all the lobes. Furthermore, APL contacts MB neurons in the α′ lobe but makes little direct contact with those in the distal α lobe. We propose that APL neurons provide widespread inhibition to stabilize and maintain synaptic specificity of a labile memory trace in a recurrent DPM and MB α′β′ neuron circuit.
PMCID: PMC3111962  PMID: 21530258
19.  Remembering nutrient quality of sugar in Drosophila 
Current biology : CB  2011;21(9):746-750.
Taste is an early stage in food and drink selection for most animals [1, 2]. Detecting sweetness indicates the presence of sugar and possible caloric content. However, sweet taste can be an unreliable predictor of nutrient value because some sugars cannot be metabolized. In addition, discrete sugars are detected by the same sensory neurons in the mammalian [3] and insect gustatory systems [4, 5], making it difficult for animals to readily distinguish the identity of different sugars using taste alone [6–8]. Here we used an appetitive memory assay in Drosophila [9–11] to investigate the contribution of palatability and relative nutritional value of sugars to memory formation. We show that palatability and nutrient value both contribute to reinforcement of appetitive memory. Non-nutritious sugars formed less robust memory that could be augmented by supplementing with a tasteless but nutritious substance. Nutrient information is conveyed to the brain within minutes of training when it can be used to guide expression of a sugar-preference memory. Therefore flies can rapidly learn to discriminate between sugars using a post-ingestive reward evaluation system and they preferentially remember nutritious sugars.
PMCID: PMC3094154  PMID: 21514159
20.  Hungry Flies Tune to Vinegar 
Cell  2011;145(1):17-18.
Many molecular signals that represent hunger and satiety in the body have been identified, but relatively little is known about how these factors alter the nervous system to change behavior. Root et al. (2011) report that hunger modulates the sensitivity of specific olfactory sensory neurons in Drosophila and facilitates odor search behavior.
PMCID: PMC3085245  PMID: 21458663
21.  Dopamine reveals neural circuit mechanisms of fly memory 
Trends in neurosciences  2010;33(10):457-464.
A goal of memory research is to understand how changing the weight of specific synapses in neural circuits in the brain leads to an appropriate learned behavioral response. Finding the relevant synapses should allow investigators to probe the underlying physiological and molecular operations that encode memories and permit their retrieval. In this review, I discuss recent work in Drosophila that implicates subsets of dopaminergic neurons in aversive reinforcement and appetitive motivation. The zonal architecture of these dopaminergic neurons may reveal the functional organization of aversive and appetitive memory in the mushroom bodies. Combinations of fly dopaminergic neurons might code negative and positive value consistent with a motivational systems role proposed in mammals.
PMCID: PMC2947577  PMID: 20701984
22.  Clock and cycle limit starvation-induced sleep loss in Drosophila 
Current biology : CB  2010;20(13):1209-1215.
Neural systems controlling the vital functions of sleep and feeding in mammals are tightly inter-connected: sleep deprivation promotes feeding, while starvation suppresses sleep. Here we show that starvation in Drosophila potently suppresses sleep suggesting that these two homeostatically regulated behaviors are also integrated in flies. The sleep suppressing effect of starvation is independent of the mushroom bodies, a previously identified sleep locus in the fly brain, and therefore is regulated by distinct neural circuitry. The circadian clock genes Clock (Clk) and cycle (cyc) are critical for proper sleep suppression during starvation. However, the sleep suppression is independent of light cues and of circadian rhythms because starved period mutants sleep like wild type flies. By selectively targeting subpopulations of Clk-expressing neurons we localize the observed sleep phenotype to the dorsally located circadian neurons. These findings show that Clk and cyc act during starvation to modulate the conflict of whether flies sleep or search for food.
PMCID: PMC2929698  PMID: 20541409
23.  A neural circuit mechanism integrating motivational state with memory expression in Drosophila 
Cell  2009;139(2):416-427.
Motivational states are important determinants of behavior. In fruit flies appetitive memory expression is constrained by satiety and promoted by hunger. Here we identify a neural mechanism that integrates the motivational state of hunger and memory. We show that stimulation of neurons that express Neuropeptide F (dNPF), an ortholog of mammalian NPY, mimicks food-deprivation and promotes memory performance in satiated flies. Robust appetitive memory performance requires the dNPF receptor in six dopaminergic neurons that innervate a distinct region of the mushroom bodies. Blocking these dopaminergic neurons releases memory performance in satiated flies whereas stimulation suppresses memory performance in hungry flies. Therefore dNPF and dopamine provide a motivational switch in the mushroom body that controls the output of appetitive memory.
PMCID: PMC2780032  PMID: 19837040
24.  Sleep: What Goes Up Must Come Down 
Current biology : CB  2009;19(12):R480-R482.
The function of sleep is hotly contested. Two recent studies suggest that fly sleep may be required to rescale synapses in the brain.
PMCID: PMC2810515  PMID: 19549492
25.  There are many ways to train a fly 
Fly  2009;3(1):3.
PMCID: PMC2814444  PMID: 19164943
Drosophila; learning; memory; behavior; plasticity

Results 1-25 (29)