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

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.

[1]  Stephan Frings,et al.  A family of octapamine receptors that specifically induce cyclic AMP production or Ca2+ release in Drosophila melanogaster , 2005 .

[2]  G. Davis,et al.  Homeostatic Control of Presynaptic Release Is Triggered by Postsynaptic Membrane Depolarization , 2001, Neuron.

[3]  V. Budnik,et al.  WNTs tune up the neuromuscular junction , 2009, Nature Reviews Neuroscience.

[4]  Ronald L. Davis,et al.  The Role of cAMP Response Element-Binding Protein in Drosophila Long-Term Memory , 2004, The Journal of Neuroscience.

[5]  I. Levitan,et al.  Identification of a Neural Circuit that Underlies the Effects of Octopamine on Sleep:Wake Behavior , 2010, Neuron.

[6]  Roberto Malinow,et al.  Emotion Enhances Learning via Norepinephrine Regulation of AMPA-Receptor Trafficking , 2007, Cell.

[7]  J. Steinert,et al.  Experience-Dependent Formation and Recruitment of Large Vesicles from Reserve Pool , 2006, Neuron.

[8]  Masakatsu Watanabe,et al.  Fast manipulation of cellular cAMP level by light in vivo , 2007, Nature Methods.

[9]  C. Breen,et al.  Octopamine—a neurohormone with presynaptic activity-dependent effects at crayfish neuromuscular junctions , 1983, Nature.

[10]  Chuan Zhou,et al.  A subset of octopaminergic neurons are important for Drosophila aggression , 2008, Nature Neuroscience.

[11]  Y. Kidokoro,et al.  Octopamine inhibits synaptic transmission at the larval neuromuscular junction in Drosophila melanogaster , 1999, Brain Research.

[12]  H. Atwood,et al.  Drosophila larval neuromuscular junction's responses to reduction of cAMP in the nervous system. , 1999, Journal of neurobiology.

[13]  K. Han,et al.  A Novel Octopamine Receptor with Preferential Expression inDrosophila Mushroom Bodies , 1998, The Journal of Neuroscience.

[14]  M. Hammer,et al.  Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. , 1998, Learning & memory.

[15]  Tobias M. Rasse,et al.  Glutamate receptor dynamics organizing synapse formation in vivo , 2005, Nature Neuroscience.

[16]  C. Rieder,et al.  Greatwall kinase , 2004, The Journal of cell biology.

[17]  Steven A. Connor,et al.  Viagra for your synapses: Enhancement of hippocampal long-term potentiation by activation of beta-adrenergic receptors. , 2010, Cellular signalling.

[18]  A. Komatsu,et al.  A trace amine, tyramine, functions as a neuromodulator in Drosophila melanogaster , 2002, Neuroscience Letters.

[19]  Y. Zhong,et al.  Morphological plasticity of motor axons in Drosophila mutants with altered excitability , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  A. Komatsu,et al.  Identification of Common Excitatory Motoneurons in Drosophila melanogaster Larvae , 2007, Zoological science.

[21]  M. Monastirioti,et al.  Octopamine immunoreactivity in the fruit fly Drosophila melanogaster , 1995, The Journal of comparative neurology.

[22]  T. Roeder Tyramine and octopamine: ruling behavior and metabolism. , 2005, Annual review of entomology.

[23]  Y. Kimura,et al.  Starvation Induces cAMP Response Element-Binding Protein-Dependent Gene Expression through Octopamine–Gq Signaling in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[24]  S. Thomas,et al.  A Distinct Role for Norepinephrine in Memory Retrieval , 2004, Cell.

[25]  Stephan J. Sigrist,et al.  Bruchpilot Promotes Active Zone Assembly, Ca2+ Channel Clustering, and Vesicle Release , 2006, Science.

[26]  Stephan J Sigrist,et al.  Experience-Dependent Strengthening of Drosophila Neuromuscular Junctions , 2003, The Journal of Neuroscience.

[27]  J. Bains,et al.  Metaplasticity of Hypothalamic Synapses following In Vivo Challenge , 2009, Neuron.

[28]  Richard D Fetter,et al.  Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. II. Fasciclin II Controls Presynaptic Structural Plasticity , 1996, Neuron.

[29]  Richard D Fetter,et al.  Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. I. Fasciclin II Controls Synaptic Stabilization and Growth , 1996, Neuron.

[30]  Leonard K. Kaczmarek,et al.  Targeted Attenuation of Electrical Activity in Drosophila Using a Genetically Modified K+ Channel , 2001, Neuron.

[31]  M. Bate,et al.  The Origin, Location, and Projections of the Embryonic Abdominal Motorneurons of Drosophila , 1997, The Journal of Neuroscience.

[32]  D. Yamamoto,et al.  A tyramine receptor gene mutation causes a defective olfactory behavior in Drosophila melanogaster. , 2000, Gene.

[33]  G. Nagel,et al.  Light-Induced Activation of Distinct Modulatory Neurons Triggers Appetitive or Aversive Learning in Drosophila Larvae , 2006, Current Biology.

[34]  Stephan J. Sigrist,et al.  Rapid Activity-Dependent Modifications in Synaptic Structure and Function Require Bidirectional Wnt Signaling , 2008, Neuron.

[35]  Benjamin H White,et al.  Dissection of synaptic excitability phenotypes by using a dominant-negative Shaker K+ channel subunit. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Heisenberg,et al.  Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila , 2003, The Journal of Neuroscience.

[37]  D. Owald,et al.  Maturation of active zone assembly by Drosophila Bruchpilot , 2009, The Journal of cell biology.

[38]  Evans,et al.  The characterization of presynaptic octopamine receptors modulating octopamine release from an identified neurone in the locust , 1984, The Journal of experimental biology.

[39]  James W Truman,et al.  Disruption of a Behavioral Sequence by Targeted Death of Peptidergic Neurons in Drosophila , 1997, Neuron.

[40]  A. Grace,et al.  Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission , 2003, Nature Neuroscience.

[41]  S. Frings,et al.  A family of octopamine [corrected] receptors that specifically induce cyclic AMP production or Ca2+ release in Drosophila melanogaster. , 2005, Journal of neurochemistry.

[42]  M. Monastirioti,et al.  Characterization of Drosophila Tyramine β-HydroxylaseGene and Isolation of Mutant Flies Lacking Octopamine , 1996, The Journal of Neuroscience.

[43]  T. Kitamoto Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[44]  P. Evans,et al.  Changes in haemolymph octopamine levels associated with food deprivation in the locust, Schistocerca gregaria , 1984 .

[45]  David R Soll,et al.  Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. , 2004, Journal of neurobiology.

[46]  Bing Zhang,et al.  Retrograde signaling that regulates synaptic development and function at the Drosophila neuromuscular junction. , 2006, International review of neurobiology.

[47]  Y. Zhong,et al.  Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  J. Hirsh,et al.  Trace amines differentially regulate adult locomotor activity, cocaine sensitivity, and female fertility in Drosophila melanogaster , 2007, Developmental neurobiology.

[49]  M. Constantine-Paton,et al.  The role of neural activity in synaptic development and its implications for adult brain function. , 1999, Advances in neurology.

[50]  A. Barco,et al.  CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models , 2010, Trends in Neurosciences.

[51]  Ronald L. Davis,et al.  Spatiotemporal Gene Expression Targeting with the TARGET and Gene-Switch Systems in Drosophila , 2004, Science's STKE.

[52]  Ronald L. Davis,et al.  Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. , 2003, Developmental biology.