Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling

Department of Neurobiology, University of Massachusetts Medical School, Worcester, Massachusetts, USA.
Nature Neuroscience (Impact Factor: 16.1). 02/2011; 14(2):190-9. DOI: 10.1038/nn.2716
Source: PubMed


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 Octβ2R octopamine autoreceptors. Notably, this autoregulation was necessary for the locomotor response. In addition, octopamine neurons regulated the expansion of excitatory glutamatergic neuromuscular arbors through Octβ2Rs 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.

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    • "These two hormones are analogous to noradrenaline and the hypothalamic gonadotropinreleasing hormone neuropeptide in vertebrates, respectively . They have multiple effects and act quickly to mobilize energy stores and increase search activity for food in response to acute energetic stress (Lee & Park, 2004; Koon et al., 2011). Octopamine acts as a neurohormone and biogenic amine in the brain (Farooqui, 2007), and appears to play a larger role than AKH in modulating foraging behaviour, which requires associative learning and intense muscle activity to successfully sustain increased food searching activity. "
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    • "In insects, their roles are fulfilled by their invertebrate counterparts, octopamine and tyramine (Roeder 2005). The biogenic amine octopamine in insects, and other invertebrates, carries out many of the physiological roles such as aggression (Zhou et al. 2008), locomotion (Koon et al. 2011; Wu et al. 2012), olfactory learning and memory (Farooqui et al. 2003; Schwaerzel et al. 2003; Unoki et al. 2005; Mizunami et al. 2009), ovulation (Monastirioti et al. 1996; Monastirioti 2003), and innate immunity (Adamo 2010; Huang et al. 2012). "
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    • "Intriguingly, it was recently discovered that these insulin-producing cells also produce the Drosophila homolog of cholecystokinin (CCK), known as Drosulfakinin (Dsk) (Söderberg et al. 2012), and in rodents levels of the satiation hormone CCK are correlated with aggression (Zwanzger et al. 2012). Furthermore, it has been reported that in Drosophila both octopamine and Dsk are involved in regulating muscle contractions necessary for the control of locomotory behavior (Koon et al. 2011; Chen and Ganetzky 2012; Chen et al. 2012), although it is not known if they interact. From these previous studies, we hypothesized that octopamine signaling could be modulating aggressiveness by regulating the expression of Dsk. "
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