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Central and Peripheral Regulation of Appetite and Food Intake in Drosophila
Published in Ruth B.S. Harris, Appetite and Food Intake, 2017
Recent studies have also revealed the roles of two conserved monoamine systems in the central processing of rewarding cues. It has been shown that OA signaling mediates the transient reinforcing properties of the sweet taste of sugar, whereas DA signaling in the fly CNS conveys information regarding rewarding stimuli in a fashion very similar to the reward pathways used by mammals. DA signaling enhances the sensitivity of gustatory receptor neurons (GRNs) to sugar in hungry flies (Inagaki et al. 2012; Marella et al. 2012). It also modulates responses to sucrose (Kim et al. 2007; Krashes et al. 2009; Selcho et al. 2009) and satiety state-dependent appetitive memory formation (Krashes et al. 2009) in the mushroom bodies (MBs), a higher-order brain center important for odor processing and learning (de Belle and Heisenberg 1994; Hitier et al. 1998; Schwaerzel et al. 2003; Margulies et al. 2005; Krashes et al. 2007), via overlapping DA and NPF/NPFR1 signaling mechanisms. The lower appetitive memory performance observed in satiated flies is due to tonic inhibition of subsets of DA neurons in the MB, while stimulation of neurons expressing NPF promotes appetitive memory by suppressing this inhibition and enabling the expression of food-associated conditioned responses. OA-dependent mechanisms also enhance short-term sugar-dependent memory encoding via activation of the OAMB receptor on a subset of DA neurons in the MB (Burke et al. 2012). It therefore appears that subsets of DA neurons in the MB represent short- and long-term reinforcing effects of nutritious sugar in learning and act downstream of OA signals. DA appears to provide a tonic inhibitory signal, which can be modulated by selective NPF/NPFR1 gating mechanisms to promote execution of either appetitive or aversive behavior (Krashes et al. 2009) and also by OA/OAMB gated signaling, which provides gustatory signals regarding food quality (Burke et al. 2012). With this model in mind, DA neurons in the MB can be thought of as a central behavioral subprogram selection circuit, in which subprogram selection is gated by both nutrient detection and satiety state.
Cellular and circuit mechanisms of olfactory associative learning in Drosophila
Published in Journal of Neurogenetics, 2020
Tamara Boto, Aaron Stahl, Seth M. Tomchik
The MBs receive olfactory input from the antennal lobe via the PNs (Su et al., 2009). They are composed of approximately 2500 pseudounipolar KCs (Figure 1(B)). Their somata are located in the posterior dorsal region of the brain. The KC dendrites form a calyx structure in each hemisphere, and their axons fasciculate together, projecting to the anterior face of the brain. Once they reach the anterior face, they divide into vertical (α, α′) and horizontal (β, β′ and γ) lobes, forming a distinctive lobular anatomical structure (Figure 1(B); Table 1) (Crittenden, Skoulakis, Han, Kalderon, & Davis, 1998; Guven-Ozkan & Davis, 2014). The MBs function as a critical site of plasticity during learning, integrating information about olfactory stimuli with US signals conveyed by modulatory interneurons (Burke et al., 2012; Claridge-Chang et al., 2009; Gervasi, Tchenio, & Preat, 2010; Schroll et al., 2006; Tomchik & Davis, 2009; Ueno et al., 2017). Flies with abnormal MB morphology show memory defects, as do flies in which the MBs are chemically ablated (de Belle & Heisenberg, 1994). The MBs are specialized for higher-order processes. Insects without mushroom bodies are generally healthy, and can move and perceive multiple sensory modalities (Wolf et al., 1998). Other forms of memory, such as place conditioning, are unaffected by loss of mushroom bodies (Zars et al., 2000b). Many proteins required for olfactory learning and memory exhibit preferential expression in the MBs (e.g. Dnc, Rut, DC0) (Nighorn, Healy, & Davis, 1991; Skoulakis et al., 1993).
Towards a functional connectome in Drosophila
Published in Journal of Neurogenetics, 2020
Context- and state-dependent neural processing is mediated on the level of neuron to neuron connections. A major limit to connectomes assembled by serial-section electron microscopy is that it lacks details on the nature of synaptic connections. Electrical synapses, which provide excitatory, non-directed and fast connections between neurons, are not reported in any Drosophila EM dataset. Chemical synapses provide directed information flow from pre- to postsynapse. In the Drosophila connectomes, chemical synapses are visually characterized by synaptic densities and vesicles filled with neurotransmitters. The Drosophila nervous system spans the full range of neurotransmitter molecules found in most animals including GABA, glutamate, and acetylcholine, monoamines, and neuropeptides. Without knowing the identity of released neurotransmitters, we cannot infer the sign and strength of synaptic modulation. Analysis of EM datasets allows discriminating small core vesicles containing neurotransmitters and dense core vesicles usually containing monoamines and neuropeptides (Michael, Cai, Xiong, Ouyang, & Chow, 2006), but otherwise provides no information about the neurotransmitter identity. Also, a single neuron can release several types of neurotransmitters or neuropeptides (Croset, Treiber, & Waddell, 2018; Nässel, 2018). Recently, input neurons to the learning and memory center in the fly, the mushroom bodies, have been shown to produce nitric oxide together with dopamine to establish short-term memory (Aso et al., 2019).
Sleep restores place learning to the adenylyl cyclase mutant rutabaga
Published in Journal of Neurogenetics, 2020
Stephane Dissel, Ellen Morgan, Vincent Duong, Dorothy Chan, Bruno van Swinderen, Paul Shaw, Troy Zars
As mentioned, enhancing sleep, either pharmacologically by administering the GABA-A agonist gaboxadol (Gab) or genetically by either activating the fan shaped body or by expressing Drosophila fatty acid binding protein (dfabp) restored memory to the calcium-calmodulin-dependent adenylyl cyclase mutant rutabaga (rut2080) and the phosphodiesterase mutant dunce (dnc1; Dissel et al.,2015). Memory was improved in rut2080and dnc1mutants assessed using APS and courtship conditioning. Notably, the mushroom bodies play prominent roles for memories formed using the APS and courtship conditioning (McBride et al., 1999; Seugnet, Suzuki, Vine, Gottschalk, & Shaw, 2008). Interestingly, a recent report found that enhanced sleep can rescue visual attention defects in dnc1 mutants but not in rut2080 mutants (Kirszenblat et al.,2018). These data suggest the possibility that sleep may not be able to fully modulate circuits outside the mushroom bodies to restore deficits in plasticity. The classic memory mutants, rut2080 and dnc1 show behavioral impairments when assessed using place learning and social enrichment, two assays that do not require the mushroom body (Donlea, Ramanan, & Shaw, 2009; Putz & Heisenberg, 2002;). Thus, we evaluated whether Gab-induced sleep could restore performance to rut2080 and dnc1 mutants when assessed using social enrichment and place learning.