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SummaryNeuromodulation permits flexibility of synapses, neural circuits and ultimately behavior. One neuromodulator, dopamine, has been studied extensively in its role as reward signal during learning and memory across animal species. Newer evidence suggests that dopaminergic neurons (DANs) can modulate sensory perception acutely, thereby allowing an animal to adapt its behavior and decision-making to its internal and behavioral state. In addition, some data indicate that DANs are heterogeneous and convey different types of information as a population. We have investigated DAN population activity and how it could encode relevant information about sensory stimuli and state by taking advantage of the confined anatomy of DANs innervating the mushroom body (MB) of the fly Drosophila melanogaster. Using in vivo calcium imaging and a custom 3D image registration method, we find that the activity of the population of MB DANs is predictive of the innate valence of an odor as well as the metabolic and mating state of the animal. Furthermore, DAN population activity is strongly correlated with walking or running, consistent with a role of dopamine in conveying behavioral state to the MB. Together our data and analysis suggest that distinct DAN population activities encode innate odor valence, movement and physiological state in a MB-compartment specific manner. We propose that dopamine shapes innate odor perception through combinatorial population coding of sensory valence, physiological and behavioral context.

Summary Animals continuously evaluate sensory information to decide on their next action. Different sensory cues, however, often demand opposing behavioral responses. How does the brain process conflicting sensory information during decision making? Here, we show that flies use neural substrates attributed to odor learning and memory, including the mushroom body (MB), for immediate sensory integration and modulation of innate behavior. Drosophila melanogaster must integrate contradictory sensory information during feeding on fermenting fruit that releases both food odor and the innately aversive odor CO 2 . Here, using this framework, we examine the neural basis for this integration. We have identified a local circuit consisting of specific glutamatergic output and PAM dopaminergic input neurons with overlapping innervation in the MB-β′2 lobe region, which integrates food odor and suppresses innate avoidance. Activation of food odor-responsive dopaminergic neurons reduces innate avoidance mediated by CO 2 -responsive MB output neurons. We hypothesize that the MB, in addition to its long recognized role in learning and memory, serves as the insect's brain center for immediate sensory integration during instantaneous decision making.

Summary Internal state as well as environmental conditions influence choice behavior. The neural circuits underpinning state-dependent behavior remain largely unknown. Carbon dioxide (CO 2 ) is an important olfactory cue for many insects, including mosquitoes, flies, moths, and honeybees [1]. Concentrations of CO 2 higher than 0.02% above atmospheric level trigger a strong innate avoidance in the fly Drosophila melanogaster [2, 3]. Here, we show that the mushroom body (MB), a brain center essential for olfactory associative memories [4–6] but thought to be dispensable for innate odor processing [7], is essential for CO 2 avoidance behavior only in the context of starvation or in the context of a food-related odor. Consistent with this, CO 2 stimulation elicits Ca 2+ influx into the MB intrinsic cells (Kenyon cells: KCs) in vivo. We identify an atypical projection neuron (bilateral ventral projection neuron, biVPN) that connects CO 2 sensory input bilaterally to the MB calyx. Blocking synaptic output of the biVPN completely abolishes CO 2 avoidance in food-deprived flies, but not in fed flies. These findings show that two alternative neural pathways control innate choice behavior, and they are dependent on the animal's internal state. In addition, they suggest that, during innate choice behavior, the MB serves as an integration site for internal state and olfactory input.

Summary Olfaction in the fruit fly Drosophila melanogaster is increasingly understood, from ligand-receptor-neuron combinations [1–4] to their axonal projection patterns into the antennal lobe [5, 6]. Drosophila thus offers an excellent opportunity to study the evolutionary and ecological dynamics of olfactory systems. We compared the structure and function of the generalist D. melanogaster with that of specialist D. sechellia , which oviposits exclusively on morinda fruit [7]. Our analyses show that whereas the fruit's headspace was dominated by acids, antennae responded most strongly to hexanoates. D. sechellia exhibited an extraordinarily strong response to methyl hexanoate (MeHex). Behaviorally, D. sechellia was much more attracted to these morinda fruit volatiles than was D. melanogaster . The high sensitivity to MeHex was paralleled by a 2.5×–3× overrepresentation of MeHex neurons on the antenna and a concordant 2.9× increase in volume of the corresponding glomerulus as compared to D. melanogaster . In addition, the MeHex neuron exhibited an extreme sensitivity down to femtograms of its ligand. In contrast, no peripherally mediated shift was found paralleling D. sechellia 's increased attraction to acids. These findings are a demonstration of evolution acting at several levels in the olfactory circuitry in mediating a fruit fly's unique preference for fruit toxic to its sibling species [8–10].