Dopamine Mediates Context-Dependent Modulation of Sensory Plasticity in C. elegans

Dopamine has been implicated in the modulation of diverse forms of behavioral plasticity, including appetitive learning and addiction. An important challenge is to understand how dopamine's effects at the cellular level alter the properties of neural circuits to modify behavior. In the nematode C. elegans, dopamine modulates habituation of an escape reflex triggered by body touch. In the absence of food, animals habituate more rapidly than in the presence of food; this contextual information about food availability is provided by dopaminergic mechanosensory neurons that sense the presence of bacteria. We find that dopamine alters habituation kinetics by selectively modulating the touch responses of the anterior-body mechanoreceptors; this modulation involves a D1-like dopamine receptor, a Gq/PLC-beta signaling pathway, and calcium release within the touch neurons. Interestingly, the body touch mechanoreceptors can themselves excite the dopamine neurons, forming a positive feedback loop capable of integrating context and experience to modulate mechanosensory attention.

[1]  K. Mirnics,et al.  Genes and subtypes of schizophrenia. , 2001, Trends in molecular medicine.

[2]  L. Ségalat,et al.  Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans , 1995, Science.

[3]  CR Yang,et al.  Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Rhea R. Kimpo,et al.  Cellular, Circuit, and Synaptic Mechanisms in Song Learning , 2004, Annals of the New York Academy of Sciences.

[5]  Paul W. Sternberg,et al.  An imaging system for standardized quantitative analysis of C. elegans behavior , 2004, BMC Bioinformatics.

[6]  D. Henze,et al.  Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. , 2000, Journal of neurophysiology.

[7]  E. Kandel,et al.  Learning to modulate transmitter release: themes and variations in synaptic plasticity. , 1993, Annual review of neuroscience.

[8]  Leon Avery,et al.  eat-11 encodes GPB-2, a Gβ5 ortholog that interacts with Goα and Gqα to regulate C. elegans behavior , 2001, Current Biology.

[9]  Tom Misteli,et al.  In vivo imaging. , 2003, Methods.

[10]  Piotr Mikolajczyk,et al.  A+A+C , 1964 .

[11]  Kevin M. Crisp,et al.  A 3-Synapse Positive Feedback Loop Regulates the Excitability of an Interneuron Critical for Sensitization in the Leech , 2006, The Journal of Neuroscience.

[12]  S. Hyman,et al.  Addiction, Dopamine, and the Molecular Mechanisms of Memory , 2000, Neuron.

[13]  M. Kazanietz,et al.  Divergence and complexities in DAG signaling: looking beyond PKC. , 2003, Trends in pharmacological sciences.

[14]  Mary A. Logan,et al.  DEPARTMENT OF BIOLOGY , 2003 .

[15]  N. Munakata.  [Genetics of Caenorhabditis elegans]. , 1989, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[16]  Koutarou D. Kimura,et al.  Diverse regulation of sensory signaling by C. elegans nPKC‐epsilon/eta TTX‐4 , 2005, The EMBO journal.

[17]  R. Jope,et al.  Comparison of [3H]Phosphatidylinositol and [3H]Phosphatidylinositol 4,5‐Bisphosphate Hydrolysis in Postmortem Human Brain Membranes and Characterization of Stimulation by Dopamine D1 Receptors , 1997, Journal of neurochemistry.

[18]  L. Avery,et al.  eat-11 encodes GPB-2, a Gbeta(5) ortholog that interacts with G(o)alpha and G(q)alpha to regulate C. elegans behavior. , 2001, Current biology : CB.

[19]  M. Chalfie,et al.  The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals , 2005, Nature Neuroscience.

[20]  S. Lockery,et al.  Active Currents Regulate Sensitivity and Dynamic Range in C. elegans Neurons , 1998, Neuron.

[21]  A. V. Maricq,et al.  Dopamine and Glutamate Control Area-Restricted Search Behavior in Caenorhabditis elegans , 2004, The Journal of Neuroscience.

[22]  In Hye Lee,et al.  AHNAK-mediated Activation of Phospholipase C-γ1 through Protein Kinase C* , 2004, Journal of Biological Chemistry.

[23]  M. Chalfie,et al.  Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. , 1989, Science.

[24]  David H. Hall,et al.  Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  H. Manji,et al.  Signalling pathways in the brain: cellular transduction of mood stabilisation in the treatment of manic-depressive illness. , 1999, The Australian and New Zealand journal of psychiatry.

[26]  G. Shepherd,et al.  Geometric and functional organization of cortical circuits , 2005, Nature Neuroscience.

[27]  M. Chalfie,et al.  The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration , 1991, Nature.

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

[29]  P. O’Donnell,et al.  D(1) dopamine receptors potentiate nmda-mediated excitability increase in layer V prefrontal cortical pyramidal neurons. , 2001, Cerebral cortex.

[30]  D. Jaffe,et al.  Dopamine Decreases the Excitability of Layer V Pyramidal Cells in the Rat Prefrontal Cortex , 1998, The Journal of Neuroscience.

[31]  R. Kerr,et al.  In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation , 2003, Neuron.

[32]  V. Taglietti,et al.  L-type calcium channel gating is modulated by bradykinin with a PKC-dependent mechanism in NG108-15 cells , 2005, European Biophysics Journal.

[33]  Monica Driscoll,et al.  Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans , 2002, Nature.

[34]  R. Kerr,et al.  In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents , 2005, The EMBO journal.

[35]  Yuichi Iino,et al.  Goα regulates olfactory adaptation by antagonizing Gqα-DAG signaling in Caenorhabditis elegans , 2006 .

[36]  P. Goldman-Rakic,et al.  Dual signaling regulated by calcyon, a D1 dopamine receptor interacting protein. , 2000, Science.

[37]  K. Miller,et al.  Goα and Diacylglycerol Kinase Negatively Regulate the Gqα Pathway in C. elegans , 1999, Neuron.

[38]  Paul J Shaw,et al.  Waking Experience Affects Sleep Need in Drosophila , 2006, Science.

[39]  C. Felder,et al.  Dopamine-1-mediated stimulation of phospholipase C activity in rat renal cortical membranes. , 1989, The Journal of biological chemistry.

[40]  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.

[41]  Edward A. Stern,et al.  Birdbrains could teach basal ganglia research a new song , 2005, Trends in Neurosciences.

[42]  Y. Tabuse.  Protein kinase C isotypes in C. elegans. , 2002, Journal of biochemistry.

[43]  A. Grace,et al.  Stimulation of D1-type dopamine receptors enhances excitability in prefrontal cortical pyramidal neurons in a state-dependent manner , 2001, Neuroscience.

[44]  J. Seamans,et al.  Developing a Neuronal Model for the Pathophysiology of Schizophrenia Based on the Nature of Electrophysiological Actions of Dopamine in the Prefrontal Cortex , 1999, Neuropsychopharmacology.

[45]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  M. D. Bono,et al.  Soluble Guanylate Cyclases Act in Neurons Exposed to the Body Fluid to Promote C. elegans Aggregation Behavior , 2004, Current Biology.

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

[48]  C. Rankin,et al.  A new group-training procedure for habituation demonstrates that presynaptic glutamate release contributes to long-term memory in Caenorhabditis elegans. , 2002, Learning & memory.

[49]  P. Goldman-Rakic,et al.  Up-regulation of the D1 dopamine receptor-interacting protein, calcyon, in patients with schizophrenia. , 2003, Archives of general psychiatry.

[50]  W. Schafer,et al.  A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans , 1995, Nature.

[51]  C. Rankin,et al.  GLR-1, a Non-NMDA Glutamate Receptor Homolog, Is Critical for Long-Term Memory in Caenorhabditis elegans , 2003, The Journal of Neuroscience.

[52]  R. Kerr,et al.  Serotonin and Go Modulate Functional States of Neurons and Muscles Controlling C. elegans Egg-Laying Behavior , 2003, Current Biology.

[53]  R. Tsien,et al.  Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin , 1997, Nature.

[54]  Nektarios Tavernarakis,et al.  Necrotic Cell Death in C. elegans Requires the Function of Calreticulin and Regulators of Ca2+ Release from the Endoplasmic Reticulum , 2001, Neuron.

[55]  K. Jamison,et al.  Life events and the course of bipolar disorder. , 1990, The American journal of psychiatry.

[56]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[57]  L. Avery,et al.  Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. , 1996, Neuron.

[58]  J. Sweatt,et al.  Protein Kinase C Overactivity Impairs Prefrontal Cortical Regulation of Working Memory , 2004, Science.

[59]  V. Ambros,et al.  Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. , 1991, The EMBO journal.

[60]  G. Patikoglou,et al.  Two RGS proteins that inhibit Galpha(o) and Galpha(q) signaling in C. elegans neurons require a Gbeta(5)-like subunit for function. , 2001, Current biology : CB.

[61]  S. R. Wicks,et al.  Integration of mechanosensory stimuli in Caenorhabditis elegans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  N. Spruston,et al.  Serotonin Receptor Activation Inhibits Sodium Current and Dendritic Excitability in Prefrontal Cortex via a Protein Kinase C-Dependent Mechanism , 2002, The Journal of Neuroscience.

[63]  C. Zuker,et al.  A Drosophila mechanosensory transduction channel. , 2000, Science.

[64]  M. Sohrmann,et al.  An activating mutation in a Caenorhabditis elegans Gs protein induces neural degeneration. , 1997, Genes & development.

[65]  C. Rankin,et al.  Factors affecting habituation and recovery from habituation in the nematode Caenorhabditis elegans. , 1992, Behavioral neuroscience.

[66]  J. Kaplan,et al.  Facilitation of Synaptic Transmission by EGL-30 Gqα and EGL-8 PLCβ DAG Binding to UNC-13 Is Required to Stimulate Acetylcholine Release , 1999, Neuron.

[67]  D. van der Kooy,et al.  Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans , 2004, The EMBO journal.

[68]  J. Sulston,et al.  Dopaminergic neurons in the nematode Caenorhabditis elegans , 1975, The Journal of comparative neurology.

[69]  P. Cosman,et al.  Machine vision based detection of omega bends and reversals in C. elegans , 2006, Journal of Neuroscience Methods.

[70]  J. Seamans,et al.  Contributions of Voltage-Gated Ca2+ Channels in the Proximal versus Distal Dendrites to Synaptic Integration in Prefrontal Cortical Neurons , 1997, The Journal of Neuroscience.

[71]  L. Avery,et al.  Mutations in a C. elegans Gqα Gene Disrupt Movement, Egg Laying, and Viability , 1996, Neuron.

[72]  T. Carew,et al.  Serotonin Release Evoked by Tail Nerve Stimulation in the CNS of Aplysia: Characterization and Relationship to Heterosynaptic Plasticity , 2002, The Journal of Neuroscience.

[73]  M Kaufman,et al.  Positive feedback circuits and memory. , 2000, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

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

[75]  S. R. Wicks,et al.  The integration of antagonistic reflexes revealed by laser ablation of identified neurons determines habituation kinetics of the Caenorhabditis elegans tap withdrawal response , 1996, Journal of Comparative Physiology A.

[76]  Yuichi Iino,et al.  Goalpha regulates olfactory adaptation by antagonizing Gqalpha-DAG signaling in Caenorhabditis elegans. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[77]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[78]  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.

[79]  Jeremy Mendel,et al.  Participation of the protein Go in multiple aspects of behavior in C. elegans , 1995, Science.

[80]  S. Ishiura,et al.  Cloning and characterization of a Caenorhabditis elegans D2‐like dopamine receptor , 2003, Journal of neurochemistry.

[81]  Rajesh Ranganathan,et al.  C. elegans Locomotory Rate Is Modulated by the Environment through a Dopaminergic Pathway and by Experience through a Serotonergic Pathway , 2000, Neuron.

[82]  D. Chklovskii,et al.  Neurogeometry and potential synaptic connectivity , 2005, Trends in Neurosciences.

[83]  J. Kaplan,et al.  Serotonin Inhibition of Synaptic Transmission Gαo Decreases the Abundance of UNC-13 at Release Sites , 1999, Neuron.

[84]  Paul W Sternberg,et al.  Caenorhabditis elegans Galphaq regulates egg-laying behavior via a PLCbeta-independent and serotonin-dependent signaling pathway and likely functions both in the nervous system and in muscle. , 2003, Genetics.

[85]  Zhen Yan,et al.  Potentiation of NMDA receptor currents by dopamine D1 receptors in prefrontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Xiaolong Jiang,et al.  The paradoxical effects of SKF83959, a novel dopamine D1-like receptor agonist, in the rat acoustic startle reflex paradigm , 2005, Neuroscience Letters.

[87]  In Hye Lee,et al.  AHNAK-mediated activation of phospholipase C-gamma1 through protein kinase C. , 2004, The Journal of biological chemistry.

[88]  C. H. Rankin,et al.  Caenorhabditis elegans: A new model system for the study of learning and memory , 1990, Behavioural Brain Research.

[89]  E. Maryon,et al.  unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction , 1996, The Journal of cell biology.

[90]  P. Sternberg,et al.  A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue , 2006, Nature.

[91]  S. Ishiura,et al.  Identification of a dopamine receptor from Caenorhabditis elegans , 2002, Neuroscience Letters.

[92]  Okihide Hikosaka,et al.  Reward-Dependent Gain and Bias of Visual Responses in Primate Superior Colliculus , 2003, Neuron.

[93]  Charles R. Yang,et al.  Dopamine D1/D5 Receptor Modulates State-Dependent Switching of Soma-Dendritic Ca2+ Potentials via Differential Protein Kinase A and C Activation in Rat Prefrontal Cortical Neurons , 2004, The Journal of Neuroscience.