Specific configurations of electrical synapses filter sensory information to drive choices in behavior

Synaptic configurations in precisely wired circuits underpin how sensory information is processed by the nervous system, and the emerging animal behavior. This is best understood for chemical synapses, but far less is known about how electrical synaptic configurations modulate, in vivo and in specific neurons, sensory information processing and context-specific behaviors. We discovered that INX-1, a gap junction protein that forms electrical synapses, is required to deploy context-specific behavioral strategies during C. elegans thermotaxis behavior. INX-1 couples two bilaterally symmetric interneurons, and this configuration is required for the integration of sensory information during migration of animals across temperature gradients. In inx-1 mutants, uncoupled interneurons display increased excitability and responses to subthreshold temperature stimuli, resulting in abnormally longer run durations and context-irrelevant tracking of isotherms. Our study uncovers a conserved configuration of electrical synapses that, by increasing neuronal capacitance, enables differential processing of sensory information and the deployment of context-specific behavioral strategies.

[1]  G. Awatramani,et al.  Hierarchical retinal computations rely on hybrid chemical-electrical signaling. , 2023, Cell reports.

[2]  Y. Fukada,et al.  Molecular encoding and synaptic decoding of context during salt chemotaxis in C. elegans , 2022, Nature Communications.

[3]  Vikas Bhandawat,et al.  Mechanisms of Variability Underlying Odor-Guided Locomotion , 2022, Frontiers in Behavioral Neuroscience.

[4]  Yun Zhang,et al.  Redundant neural circuits regulate olfactory integration , 2022, PLoS genetics.

[5]  S. Curti,et al.  Function and Plasticity of Electrical Synapses in the Mammalian Brain: Role of Non-Junctional Mechanisms , 2021, Biology.

[6]  Qiang Liu,et al.  C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program , 2021, Nature Communications.

[7]  Mingxi Hu,et al.  Presynaptic coupling by electrical synapses coordinates a rhythmic behavior by synchronizing the activities of a neuron pair , 2021, Proceedings of the National Academy of Sciences.

[8]  Gerald M. Rubin,et al.  A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection , 2020, bioRxiv.

[9]  Eugene Jennifer Jin,et al.  Gap junctions: historical discoveries and new findings in the Caenorhabditis elegans nervous system , 2020, Biology Open.

[10]  Yun Zhang,et al.  NMDAR-mediated modulation of gap junction circuit regulates olfactory learning in C. elegans , 2020, Nature Communications.

[11]  A. Pérez-Escudero,et al.  Inversion of pheromone preference optimizes foraging in C. elegans , 2020, bioRxiv.

[12]  Mark J Alkema,et al.  Flexible motor sequence generation during stereotyped escape responses , 2020, eLife.

[13]  Daniel R. Berger,et al.  Connectomes across development reveal principles of brain maturation in C. elegans , 2020, bioRxiv.

[14]  I. Mori,et al.  Neural Coding of Thermal Preferences in the Nematode Caenorhabditis elegans , 2020, eNeuro.

[15]  Wagner Steuer Costa,et al.  Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans , 2020, Proceedings of the National Academy of Sciences.

[16]  I. Rabinowitch,et al.  INX-18 and INX-19 play distinct roles in electrical synapses that modulate aversive behavior in Caenorhabditis elegans , 2019, bioRxiv.

[17]  Denise S Walker,et al.  Distinct roles for innexin gap junctions and hemichannels in mechanosensation , 2019, bioRxiv.

[18]  Andrew C. Lin,et al.  Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. , 2019, Current opinion in insect science.

[19]  A. Nose,et al.  Circuit architecture for somatotopic action selection in invertebrates , 2019, Neuroscience Research.

[20]  O. Hobert,et al.  Plasticity of the Electrical Connectome of C. elegans , 2018, Cell.

[21]  Michael J. Goard,et al.  Neural mechanisms of sensorimotor transformation and action selection , 2018, The European journal of neuroscience.

[22]  E. Soucy,et al.  Cholinergic Sensorimotor Integration Regulates Olfactory Steering , 2017, Neuron.

[23]  E. Hallem,et al.  A Single Set of Interneurons Drives Opposite Behaviors in C. elegans , 2017, Current Biology.

[24]  Aravinthan D. T. Samuel,et al.  Integration of Plasticity Mechanisms within a Single Sensory Neuron of C. elegans Actuates a Memory , 2017, Neuron.

[25]  Julie H. Simpson,et al.  Simultaneous activation of parallel sensory pathways promotes a grooming sequence in Drosophila , 2017, bioRxiv.

[26]  R. Mailler,et al.  Antidromic-rectifying gap junctions amplify chemical transmission at functionally mixed electrical-chemical synapses , 2017, Nature Communications.

[27]  Cornelia I Bargmann,et al.  Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans , 2017, Proceedings of the National Academy of Sciences.

[28]  Matthew S. Creamer,et al.  Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition , 2016, bioRxiv.

[29]  D. Hall Gap junctions in C. elegans: Their roles in behavior and development , 2016, Developmental neurobiology.

[30]  Todd R. Gruninger,et al.  DOP-2 D2-Like Receptor Regulates UNC-7 Innexins to Attenuate Recurrent Sensory Motor Neurons during C. elegans Copulation , 2015, The Journal of Neuroscience.

[31]  Zeynep F. Altun,et al.  High resolution map of caenorhabditis elegans gap junction proteins , 2015, Developmental dynamics : an official publication of the American Association of Anatomists.

[32]  D. Dickinson,et al.  Streamlined Genome Engineering with a Self-Excising Drug Selection Cassette , 2015, Genetics.

[33]  K. Hashimoto,et al.  Regulation of Experience-Dependent Bidirectional Chemotaxis by a Neural Circuit Switch in Caenorhabditis elegans , 2014, The Journal of Neuroscience.

[34]  Henry Pinkard,et al.  Advanced methods of microscope control using μManager software. , 2014, Journal of biological methods.

[35]  Zhaoyu Li,et al.  Encoding of Both Analog- and Digital-like Behavioral Outputs by One C. elegans Interneuron , 2014, Cell.

[36]  O. Chever,et al.  Connexons and pannexons: newcomers in neurophysiology , 2014, Front. Cell. Neurosci..

[37]  Alberto E. Pereda,et al.  Hemichannel composition and electrical synaptic transmission: molecular diversity and its implications for electrical rectification , 2014, Front. Cell. Neurosci..

[38]  E Jane Albert Hubbard,et al.  FLP/FRT and Cre/lox recombination technology in C. elegans. , 2014, Methods.

[39]  W. Schafer,et al.  Rewiring neural circuits by the insertion of ectopic electrical synapses in transgenic C. elegans , 2014, Nature Communications.

[40]  Aravinthan D. T. Samuel,et al.  Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons , 2014, Proceedings of the National Academy of Sciences.

[41]  Zeynep F. Altun,et al.  Six Innexins Contribute to Electrical Coupling of C. elegans Body-Wall Muscle , 2013, PloS one.

[42]  Yoshinori Fujiyoshi,et al.  Oligomeric Structure and Functional Characterization of Caenorhabditis elegans Innexin-6 Gap Junction Protein* , 2013, The Journal of Biological Chemistry.

[43]  Kevin M. Collins,et al.  Postsynaptic ERG Potassium Channels Limit Muscle Excitability to Allow Distinct Egg-Laying Behavior States in Caenorhabditis elegans , 2013, The Journal of Neuroscience.

[44]  Daniel Blankenberg,et al.  CloudMap: A Cloud-Based Pipeline for Analysis of Mutant Genome Sequences , 2012, Genetics.

[45]  S. Lockery,et al.  Neuronal microcircuits for decision making in C. elegans , 2012, Current Opinion in Neurobiology.

[46]  Zengcai V. Guo,et al.  Controlling interneuron activity in Caenorhabditis elegans to evoke chemotactic behavior , 2012, Nature.

[47]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[48]  Aravinthan D. T. Samuel,et al.  Controlling airborne cues to study small animal navigation , 2012, Nature Methods.

[49]  P. Sengupta,et al.  Degeneracy and Neuromodulation among Thermosensory Neurons Contribute to Robust Thermosensory Behaviors in Caenorhabditis elegans , 2011, The Journal of Neuroscience.

[50]  Atsushi Kuhara,et al.  Neural coding in a single sensory neuron controlling opposite seeking behaviours in Caenorhabditis elegans , 2011, Nature communications.

[51]  Paul W Sternberg,et al.  Transfer characteristics of a thermosensory synapse in Caenorhabditis elegans , 2011, Proceedings of the National Academy of Sciences.

[52]  Michelle D. Po,et al.  A Co-operative Regulation of Neuronal Excitability by UNC-7 Innexin and NCA/NALCN Leak Channel , 2011, Molecular Brain.

[53]  Oliver Hobert,et al.  C. elegans Mutant Identification with a One-Step Whole-Genome-Sequencing and SNP Mapping Strategy , 2010, PloS one.

[54]  S. Jarriault,et al.  A Strategy for Direct Mapping and Identification of Mutations by Whole-Genome Sequencing , 2010, Genetics.

[55]  G. Seydoux,et al.  Transgenic solutions for the germline , 2010, WormBook : the online review of C. elegans biology.

[56]  Zeynep F. Altun,et al.  High resolution map of Caenorhabditis elegans gap junction proteins , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[57]  J. E. Shaw,et al.  Interactions between innexins UNC-7 and UNC-9 mediate electrical synapse specificity in the Caenorhabditis elegans locomotory nervous system , 2009, Neural Development.

[58]  Aravinthan D. T. Samuel,et al.  An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior , 2008, Proceedings of the National Academy of Sciences.

[59]  Koutarou D. Kimura,et al.  Temperature Sensing by an Olfactory Neuron in a Circuit Controlling Behavior of C. elegans , 2008, Science.

[60]  K. J. Muller,et al.  Innexins form two types of channels , 2007, FEBS letters.

[61]  Sreekanth H. Chalasani,et al.  Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans , 2007, Nature.

[62]  Daniel A. Colón-Ramos,et al.  Glia Promote Local Synaptogenesis Through UNC-6 (Netrin) Signaling in C. elegans , 2007, Science.

[63]  Damon A. Clark,et al.  Sensorimotor control during isothermal tracking in Caenorhabditis elegans , 2006, Journal of Experimental Biology.

[64]  Damon A. Clark,et al.  The AFD Sensory Neurons Encode Multiple Functions Underlying Thermotactic Behavior in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[65]  Shin Murakami,et al.  Aging-Dependent and -Independent Modulation of Associative Learning Behavior by Insulin/Insulin-Like Growth Factor-1 Signal in Caenorhabditis elegans , 2005, The Journal of Neuroscience.

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

[67]  M. Hoch,et al.  Intercellular communication: the Drosophila innexin multiprotein family of gap junction proteins. , 2005, Chemistry & biology.

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

[69]  O. Hobert,et al.  Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. , 2003, Journal of neurobiology.

[70]  J. Satterlee,et al.  Specification of Thermosensory Neuron Fate in C. elegans Requires ttx-1, a Homolog of otd/Otx , 2001, Neuron.

[71]  R. Masland The fundamental plan of the retina , 2001, Nature Neuroscience.

[72]  S. Bloomfield,et al.  Rod Vision: Pathways and Processing in the Mammalian Retina , 2001, Progress in Retinal and Eye Research.

[73]  Edouard De Castro,et al.  Ca2+ Signaling via the Neuronal Calcium Sensor-1 Regulates Associative Learning and Memory in C. elegans , 2001, Neuron.

[74]  R. Wyman,et al.  Innexins: a family of invertebrate gap-junction proteins. , 1998, Trends in genetics : TIG.

[75]  G. Ruvkun,et al.  Regulation of Interneuron Function in the C. elegans Thermoregulatory Pathway by the ttx-3 LIM Homeobox Gene , 1997, Neuron.

[76]  I. Mori,et al.  Neural regulation of thermotaxis in Caenorhabditis elegans , 1995, Nature.

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

[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]  R. L. Russell,et al.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Ilona C. Grunwald Kadow,et al.  State-dependent plasticity of innate behavior in fruit flies , 2019, Current Opinion in Neurobiology.

[81]  Aravinthan D. T. Samuel,et al.  The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation , 2006, BMC Neuroscience.

[82]  Patrick W. Hullett,et al.  BMC Genomics BioMed Central Methodology article Rapid single nucleotide polymorphism mapping in C. elegans , 2005 .

[83]  D. Paul,et al.  Connexins, connexons, and intercellular communication. , 1996, Annual review of biochemistry.

[84]  R. Porter,et al.  DNA transformation. , 1988, Methods in enzymology.