Beyond the connectome: How neuromodulators shape neural circuits

Powerful ultrastructural tools are providing new insights into neuronal circuits, revealing a wealth of anatomically‐defined synaptic connections. These wiring diagrams are incomplete, however, because functional connectivity is actively shaped by neuromodulators that modify neuronal dynamics, excitability, and synaptic function. Studies of defined neural circuits in crustaceans, C. elegans, Drosophila, and the vertebrate retina have revealed the ability of modulators and sensory context to reconfigure information processing by changing the composition and activity of functional circuits. Each ultrastructural connectivity map encodes multiple circuits, some of which are active and some of which are latent at any given time.

[1]  H. Horvitz,et al.  Serotonin and octopamine in the nematode Caenorhabditis elegans. , 1982, Science.

[2]  B. Mulloney,et al.  Sensory alteration of motor patterns in the stomatogastric nervous system of the spiny lobster Panulirus interruptus. , 1982, The Journal of experimental biology.

[3]  M. E. Lewis,et al.  Endogenous opioids: biology and function. , 1984, Annual review of neuroscience.

[4]  E. Marder,et al.  A mechanism for production of phase shifts in a pattern generator. , 1984, Journal of neurophysiology.

[5]  S. Brenner,et al.  The neural circuit for touch sensitivity in Caenorhabditis elegans , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Ralph E. Davis,et al.  Neural control of behaviour in Ascaris , 1985, Trends in Neurosciences.

[7]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  M. Moulins,et al.  Switching of a neuron from one network to another by sensory-induced changes in membrane properties. , 1989, Science.

[9]  R. Harris-Warrick,et al.  Modulation of neural networks for behavior. , 1991, Annual review of neuroscience.

[10]  E. Marder,et al.  Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. , 1991, Journal of neurophysiology.

[11]  E. Marder,et al.  Switching neurons are integral members of multiple oscillatory networks , 1994, Current Biology.

[12]  S. Massey,et al.  Differential properties of two gap junctional pathways made by AII amacrine cells , 1995, Nature.

[13]  Monica Driscoll,et al.  Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor , 1995, Nature.

[14]  J. Kaplan,et al.  Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor , 1995, Nature.

[15]  R. Weiler,et al.  The modulation of intercellular coupling in the retina. , 1998, Seminars in cell & developmental biology.

[16]  A. V. Maricq,et al.  Neuronal Control of Locomotion in C. elegans Is Modified by a Dominant Mutation in the GLR-1 Ionotropic Glutamate Receptor , 1999, Neuron.

[17]  Yasuhiro Funabashi,et al.  Geometrical structure of the neuronal network of Caenorhabditis elegans , 2001 .

[18]  R. Yuste,et al.  Topology of gap junction networks in C. elegans. , 2001, Journal of theoretical biology.

[19]  S. Shen-Orr,et al.  Networks Network Motifs : Simple Building Blocks of Complex , 2002 .

[20]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[21]  Mario de Bono,et al.  Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans , 2002, Nature.

[22]  Cori Bargmann,et al.  Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli , 2002, Nature.

[23]  U. Alon,et al.  Search for computational modules in the C. elegans brain , 2004, BMC Biology.

[24]  S. Mills,et al.  Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina , 2004, Visual Neuroscience.

[25]  Michael R Koelle,et al.  Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans , 2004, Nature Neuroscience.

[26]  A. Hart,et al.  Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Cone,et al.  The central melanocortin system and the integration of short- and long-term regulators of energy homeostasis. , 2004, Recent progress in hormone research.

[28]  H. Fields.  State-dependent opioid control of pain , 2004, Nature Reviews Neuroscience.

[29]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[30]  M. de Bono,et al.  Neuronal substrates of complex behaviors in C. elegans. , 2005, Annual review of neuroscience.

[31]  Cori Bargmann,et al.  A circuit for navigation in Caenorhabditis elegans , 2005 .

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

[33]  Mario de Bono,et al.  Experience-Dependent Modulation of C. elegans Behavior by Ambient Oxygen , 2005, Current Biology.

[34]  Bruce R. Johnson,et al.  Dopamine modulation of phasing of activity in a rhythmic motor network: contribution of synaptic and intrinsic modulatory actions. , 2005, Journal of neurophysiology.

[35]  Cornelia I Bargmann,et al.  A Distributed Chemosensory Circuit for Oxygen Preference in C. elegans , 2006, PLoS biology.

[36]  Mario de Bono,et al.  Behavioral Motifs and Neural Pathways Coordinating O2 Responses and Aggregation in C. elegans , 2006, Current Biology.

[37]  M. Koelle,et al.  Biogenic amine neurotransmitters in C. , 2007 .

[38]  P. Komuniecki,et al.  Tyramine and Octopamine Independently Inhibit Serotonin-Stimulated Aversive Behaviors in Caenorhabditis elegans through Two Novel Amine Receptors , 2007, The Journal of Neuroscience.

[39]  E. Marder,et al.  Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. , 2007, Annual review of physiology.

[40]  M. Koelle,et al.  Biogenic amine neurotransmitters in C. elegans. , 2007, WormBook : the online review of C. elegans biology.

[41]  Saskia E. J. de Vries,et al.  Retinal Ganglion Cells Can Rapidly Change Polarity from Off to On , 2007, PLoS Biology.

[42]  Cori Bargmann,et al.  Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans , 2008, Proceedings of the National Academy of Sciences.

[43]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[44]  Robert Steven,et al.  Three Distinct Amine Receptors Operating at Different Levels within the Locomotory Circuit Are Each Essential for the Serotonergic Modulation of Chemosensation in Caenorhabditis elegans , 2009, The Journal of Neuroscience.

[45]  Evan Z. Macosko,et al.  A huband-spoke circuit drives pheromone attraction and social behaviour in C . elegans , 2009 .

[46]  W. Kristan,et al.  Behavioral choice by presynaptic inhibition of tactile sensory terminals , 2009, Nature Neuroscience.

[47]  Jeremy D. Schmahmann,et al.  A Proposal for a Coordinated Effort for the Determination of Brainwide Neuroanatomical Connectivity in Model Organisms at a Mesoscopic Scale , 2009, PLoS Comput. Biol..

[48]  Evan Z. Macosko,et al.  A Hub-and-Spoke Circuit Drives Pheromone Attraction and Social Behavior in C. elegans , 2009, Nature.

[49]  Louis K. Scheffer,et al.  Semi-automated reconstruction of neural circuits using electron microscopy , 2010, Current Opinion in Neurobiology.

[50]  R. Oostenveld,et al.  Stress-Related Noradrenergic Activity Prompts Large-Scale Neural Network Reconfiguration , 2011, Science.

[51]  S. Sternson,et al.  Hunger States Switch a Flip-Flop Memory Circuit via a Synaptic AMPK-Dependent Positive Feedback Loop , 2011, Cell.

[52]  R. Komuniecki,et al.  Monoamines activate neuropeptide signaling cascades to modulate nociception in C. elegans: a useful model for the modulation of chronic pain? , 2012, Invertebrate Neuroscience.

[53]  D. Mastronarde,et al.  Exploring the retinal connectome , 2011, Molecular vision.

[54]  Zhaoyang Feng,et al.  The Neural Circuits and Synaptic Mechanisms Underlying Motor Initiation in C. elegans , 2011, Cell.

[55]  Ian A. Meinertzhagen,et al.  Wiring Economy and Volume Exclusion Determine Neuronal Placement in the Drosophila Brain , 2011, Current Biology.

[56]  Lav R. Varshney,et al.  Structural Properties of the Caenorhabditis elegans Neuronal Network , 2009, PLoS Comput. Biol..

[57]  Jing W. Wang,et al.  Presynaptic Facilitation by Neuropeptide Signaling Mediates Odor-Driven Food Search , 2011, Cell.

[58]  Steffen Prohaska,et al.  Large-Scale Automated Histology in the Pursuit of Connectomes , 2011, The Journal of Neuroscience.

[59]  Louis K. Scheffer,et al.  Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. , 2011, Current biology : CB.

[60]  Leonid Kruglyak,et al.  Catecholamine receptor polymorphisms affect decision-making in C. elegans , 2011, Nature.

[61]  David J. Anderson,et al.  Visualizing Neuromodulation In Vivo: TANGO-Mapping of Dopamine Signaling Reveals Appetite Control of Sugar Sensing , 2012, Cell.

[62]  R. Komuniecki,et al.  Monoamines and neuropeptides interact to inhibit aversive behaviour in Caenorhabditis elegans , 2012, The EMBO journal.