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While research into the biology of animal behaviour has primarily focused on the central nervous system, cues from peripheral tissues and the environment have been implicated in brain development and function 1 . There is emerging evidence that bidirectional communication between the gut and the brain affects behaviours including anxiety, cognition, nociception and social interaction 1 – 9 . Coordinated locomotor behaviour is critical for the survival and propagation of animals, and is regulated by internal and external sensory inputs 10 , 11 . However, little is known about how the gut microbiome influences host locomotion, or the molecular and cellular mechanisms involved. Here we report that germ-free status or antibiotic treatment results in hyperactive locomotor behaviour in the fruit fly Drosophila melanogaster . Increased walking speed and daily activity in the absence of a gut microbiome are rescued by mono-colonization with specific bacteria, including the fly commensal Lactobacillus brevis . The bacterial enzyme xylose isomerase from L. brevis recapitulates the locomotor effects of microbial colonization by modulating sugar metabolism in flies. Notably, thermogenetic activation of octopaminergic neurons or exogenous administration of octopamine, the invertebrate counterpart of noradrenaline, abrogates the effects of xylose isomerase on Drosophila locomotion. These findings reveal a previously unappreciated role for the gut microbiome in modulating locomotion, and identify octopaminergic neurons as mediators of peripheral microbial cues that regulate motor behaviour in animals. Female Drosophila that lack a microbiota are hyperactive, and xylose isomerase from Lactobacillus brevis is sufficient to reverse this effect.

Starved animals often exhibit elevated locomotion, which has been speculated to partly resemble foraging behavior and facilitate food acquisition and energy intake. Despite its importance, the neural mechanism underlying this behavior remains unknown in any species. In this study we confirmed and extended previous findings that starvation induced locomotor activity in adult fruit flies Drosophila melanogaster . We also showed that starvation-induced hyperactivity was directed toward the localization and acquisition of food sources, because it could be suppressed upon the detection of food cues via both central nutrient-sensing and peripheral sweet-sensing mechanisms, via induction of food ingestion. We further found that octopamine, the insect counterpart of vertebrate norepinephrine, as well as the neurons expressing octopamine, were both necessary and sufficient for starvation-induced hyperactivity. Octopamine was not required for starvation-induced changes in feeding behaviors, suggesting independent regulations of energy intake behaviors upon starvation. Taken together, our results establish a quantitative behavioral paradigm to investigate the regulation of energy homeostasis by the CNS and identify a conserved neural substrate that links organismal metabolic state to a specific behavioral output. Significance The central nervous system monitors reduction in metabolic state and promotes feeding and foraging in response. While feeding behavior has been extensively studied, the regulation of foraging behavior remains largely unknown. In this study, we show that starvation-induced hyperactivity in adult fruit flies resembled foraging activity. We also found that octopamine, the insect counterpart of vertebrate norepinephrine, was crucial for starvation-induced foraging. We further showed that octopamine was not required for starvation-induced changes in feeding, suggesting independent regulations of energy intake behaviors upon starvation. Taken together, our results establish a quantitative foraging assay and a highly conserved neural substrate that regulates foraging, offering an entry point to further dissect the neural circuitry of this important behavior.

Dopamine is synonymous with reward in mammals but associated with aversive reinforcement in insects, where reward seems to be signalled by octopamine; here it is shown that flies have discrete populations of dopamine neurons representing positive or negative values that are coordinately regulated by octopamine. Shared neuronal reward signals The neurotransmitter dopamine has been synonymous with reward in mammals, but is associated with aversive reinforcement in insects. In insects, it was thought, reward was signalled by octopamine. Now Scott Waddell and colleagues show that flies have discrete 'negative' and 'positive' populations of dopamine neurons, which are coordinately regulated by octopamine. This work reconciles previous findings with octopamine and dopamine, and suggests that reinforcement systems in flies are more like those in mammals than previously thought. Dopamine is synonymous with reward and motivation in mammals 1 , 2 . However, only recently has dopamine been linked to motivated behaviour and rewarding reinforcement in fruitflies 3 , 4 . Instead, octopamine has historically been considered to be the signal for reward in insects 5 , 6 , 7 . Here we show, using temporal control of neural function in Drosophila , that only short-term appetitive memory is reinforced by octopamine. Moreover, octopamine-dependent memory formation requires signalling through dopamine neurons. Part of the octopamine signal requires the α-adrenergic-like OAMB receptor in an identified subset of mushroom-body-targeted dopamine neurons. Octopamine triggers an increase in intracellular calcium in these dopamine neurons, and their direct activation can substitute for sugar to form appetitive memory, even in flies lacking octopamine. Analysis of the β-adrenergic-like OCTβ2R receptor reveals that octopamine-dependent reinforcement also requires an interaction with dopamine neurons that control appetitive motivation. These data indicate that sweet taste engages a distributed octopamine signal that reinforces memory through discrete subsets of mushroom-body-targeted dopamine neurons. In addition, they reconcile previous findings with octopamine and dopamine and suggest that reinforcement systems in flies are more similar to mammals than previously thought.

An approaching predator and self-motion toward an object can generate similar looming patterns on the retina, but these situations demand different rapid responses. How central circuits flexibly process visual cues to activate appropriate, fast motor pathways remains unclear. Here we identify two descending neuron (DN) types that control landing and contribute to visuomotor flexibility in Drosophila. For each, silencing impairs visually evoked landing, activation drives landing, and spike rate determines leg extension amplitude. Critically, visual responses of both DNs are severely attenuated during non-flight periods, effectively decoupling visual stimuli from the landing motor pathway when landing is inappropriate. The flight-dependence mechanism differs between DN types. Octopamine exposure mimics flight effects in one, whereas the other probably receives neuronal feedback from flight motor circuits. Thus, this sensorimotor flexibility arises from distinct mechanisms for gating action-specific descending pathways, such that sensory and motor networks are coupled or decoupled according to the behavioral state.Ache et al. show that neurons controlling landing in flies are permissively gated by flight, indicating that brain sensory networks are flexibly coupled to or decoupled from motor networks in the nerve cord to promote contextually appropriate actions.

Octopamine regulates various physiological phenomena including memory, sleep, grooming and aggression in insects. In Drosophila, four types of octopamine receptors have been identified: Oamb, Oct/TyrR, OctβR and Octα2R. Among these receptors, Octα2R was recently discovered and pharmacologically characterized. However, the effects of the receptor on biological functions are still unknown. Here, we showed that Octα2R regulated several behaviors related to octopamine signaling. Octα2R hypomorphic mutant flies showed a significant decrease in locomotor activity. We found that Octα2R expressed in the pars intercerebralis, which is a brain region projected by octopaminergic neurons, is involved in control of the locomotor activity. Besides, Octα2R hypomorphic mutants increased time and frequency of grooming and inhibited starvation‐induced hyperactivity. These results indicated that Octα2R expressed in the central nervous system is responsible for the involvement in physiological functions. Octα2R signaling regulated activation of locomotor activity, inhibition of grooming and starvation‐induced hyperactivity.

The general association between longevity and energy metabolism has been well-documented for some time, yet the specific metabolic processes that regulate longevity remain largely unexplored. In contrast to the common active swimming daphnids (e.g., Daphnia sinensis ), Simocephalus vetulus is notable for being sedentary and having a lower metabolic rate, yet it has a longer lifespan than D. sinensis . In this study, metabolomic analysis and drug validation experiments are employed to demonstrate that the lower pyruvate dehydrogenase (PDH) activity reduces the locomotor performance of S. vetulus and to identify PDH activity as a regulator of the lifespan of daphnids . Inhibition of PDH activity in daphnids by CPI-613 attenuates its ATP supply and locomotor performance but significantly induces longevity. The study also determines that the invertebrate neurotransmitter octopamine and temperature have a significant impact on PDH activity and modulate daphnids lifespan. And when the effects of temperature and octopamine on PDH activity are counteracted by inhibitors or agonists, the impact on lifespan becomes ineffective. These results support an important role for PDH in lifespan regulation and locomotor performance in daphnids and provide insights into the metabolic regulation of lifespan. Metabolism is known to be linked to lifespan in some species, though it remains unclear how this effect is mediated. Here they show that reduced pyruvate dehydrogenase (PDH) activity lowers locomotion but extends lifespan in daphnids and show that inhibition of PDH can increase lifespan in these species.

Octopamine (OA) is structurally and functionally similar to adrenaline/noradrenaline in vertebrates, and OA modulates diverse physiological and behavioral processes in invertebrates. OA exerts its actions by binding to specific octopamine receptors (OARs). Functional and pharmacological characterization of OARs have been investigated in several insects. However, the literature on OARs is scarce for parasitoids. Here we cloned three β-adrenergic-like OARs (CcOctβRs) from Cotesia chilonis. CcOctβRs share high similarity with their own orthologous receptors. The transcript levels of CcOctβRs were varied in different tissues. When heterologously expressed in CHO-K1 cells, CcOctβRs induced cAMP production, and were dose-dependently activated by OA, TA and putative octopaminergic agonists. Their activities were inhibited by potential antagonists and were most efficiently blocked by epinastine. Our study offers important information about the molecular and pharmacological properties of β-adrenergic-like OARs from C. chilonis that will provide the basis to reveal the contribution of individual receptors to the physiological processes and behaviors in parasitoids.

Trace amines such as p- tyramine, p- octopamine and p- synephrine are found in low concentrations in animals and plants. Consumption of pre-workout supplements containing these plant-derived amines has been associated with cardiovascular side effects. The aim of this study was to determine the mechanisms of action of these trace amines on porcine isolated coronary and mesenteric arteries. Noradrenaline caused contraction of mesenteric arteries and relaxation of coronary arteries. In both tissues, all three trace amines induced contractions with similar potencies and responses were unaffected by the β-adrenoceptor antagonist propranolol (1 µM), the nitric oxide synthase inhibitor L-NNA (100 µM), or the TAAR-1 antagonist, EPPTB (100 nM). However, the contractile responses of mesenteric arteries, but not coronary arteries, were significantly reduced by depletion of endogenous noradrenaline. Mesenteric responses to all three amines were abolished in the presence of prazosin (1 µM) whereas residual contractile responses remained in the coronary artery which were inhibited by a high concentration (100 µM) of EPPTB. The results suggest complex responses of the coronary artery to the trace amines, with activity at α 1 -adrenoceptors and potentially TAARs other than TAAR-1. In contrast the actions of the amines on the mesenteric artery appeared to involve indirect sympathomimetic actions and direct actions on α 1 -adrenoceptors.

Pollinators exhibit a range of innate and learned behaviors that mediate interactions with flowers, but the olfactory bases of these responses in a naturalistic context remain poorly understood. The hawkmoth Manduca sexta is an important pollinator for many night-blooming flowers but can learn—through olfactory conditioning—to visit other nectar resources. Analysis of the flowers that are innately attractive to moths shows that the scents all have converged on a similar chemical profile that, in turn, is uniquely represented in the moth's antennal (olfactory) lobe. Flexibility in visitation to nonattractive flowers, however, is mediated by octopamine-associated modulation of antennal-lobe neurons during learning. Furthermore, this flexibility does not extinguish the innate preferences. Such processing of stimuli through two olfactory channels, one involving an innate bias and the other a learned association, allows the moths to exist within a dynamic floral environment while maintaining specialized associations.

To compare the behavioral roles of biogenic amines in the males of primitive and advanced eusocial bees, we determined the levels of dopamine- and octopamine-related substances in the brain, and the behavioral effects of these monoamines by drug injection in the primitive eusocial bumble bee, Bombus ignitus . The levels of dopamine and its precursors in the brain peaked at the late pupal stage, but the dopamine peak extended to adult emergence. The tyramine and octopamine levels increased from the mid-pupal to adult stages. The locomotor and flight activities, and light preference increased with age. Injection of octopamine and its receptor antagonist had significant effects on the locomotor and flight activities, whereas dopamine injection did not, indicating that these activities can be regulated by the octopaminergic system. We also determined the dynamics of dopamine-related substances in honey bee ( Apis mellifera ) drones. The changes in the dopamine level in the brains of honey bee drones exhibited two peaks from the pupal to adult stages, whereas the bumble bee males had only one peak. These are consistent with the behavioral functions of dopamine in honey bee drones and ineffectiveness of dopamine injection at the adult stage in bumble bee males.