Literature DB >> 25417153

Encoding of both analog- and digital-like behavioral outputs by one C. elegans interneuron.

Zhaoyu Li1, Jie Liu1, Maohua Zheng1, X Z Shawn Xu2.   

Abstract

Model organisms usually possess a small nervous system but nevertheless execute a large array of complex behaviors, suggesting that some neurons are likely multifunctional and may encode multiple behavioral outputs. Here, we show that the C. elegans interneuron AIY regulates two distinct behavioral outputs: locomotion speed and direction-switch by recruiting two different circuits. The "speed" circuit is excitatory with a wide dynamic range, which is well suited to encode speed, an analog-like output. The "direction-switch" circuit is inhibitory with a narrow dynamic range, which is ideal for encoding direction-switch, a digital-like output. Both circuits employ the neurotransmitter ACh but utilize distinct postsynaptic ACh receptors, whose distinct biophysical properties contribute to the distinct dynamic ranges of the two circuits. This mechanism enables graded C. elegans synapses to encode both analog- and digital-like outputs. Our studies illustrate how an interneuron in a simple organism encodes multiple behavioral outputs at the circuit, synaptic, and molecular levels.

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Year:  2014        PMID: 25417153      PMCID: PMC4243084          DOI: 10.1016/j.cell.2014.09.056

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  42 in total

1.  One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction.

Authors:  J E Richmond; E M Jorgensen
Journal:  Nat Neurosci       Date:  1999-09       Impact factor: 24.884

2.  The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans.

Authors:  Beverly J Piggott; Jie Liu; Zhaoyang Feng; Seth A Wescott; X Z Shawn Xu
Journal:  Cell       Date:  2011-11-11       Impact factor: 41.582

Review 3.  Multiple neural spike train data analysis: state-of-the-art and future challenges.

Authors:  Emery N Brown; Robert E Kass; Partha P Mitra
Journal:  Nat Neurosci       Date:  2004-05       Impact factor: 24.884

4.  Multimodal fast optical interrogation of neural circuitry.

Authors:  Feng Zhang; Li-Ping Wang; Martin Brauner; Jana F Liewald; Kenneth Kay; Natalie Watzke; Phillip G Wood; Ernst Bamberg; Georg Nagel; Alexander Gottschalk; Karl Deisseroth
Journal:  Nature       Date:  2007-04-05       Impact factor: 49.962

5.  The neural circuit for touch sensitivity in Caenorhabditis elegans.

Authors:  M Chalfie; J E Sulston; J G White; E Southgate; J N Thomson; S Brenner
Journal:  J Neurosci       Date:  1985-04       Impact factor: 6.167

6.  Neural regulation of thermotaxis in Caenorhabditis elegans.

Authors:  I Mori; Y Ohshima
Journal:  Nature       Date:  1995-07-27       Impact factor: 49.962

Review 7.  Neuronal substrates of complex behaviors in C. elegans.

Authors:  Mario de Bono; Andres Villu Maricq
Journal:  Annu Rev Neurosci       Date:  2005       Impact factor: 12.449

8.  The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter.

Authors:  A Alfonso; K Grundahl; J S Duerr; H P Han; J B Rand
Journal:  Science       Date:  1993-07-30       Impact factor: 47.728

9.  Sensory regulation of male mating behavior in Caenorhabditis elegans.

Authors:  K S Liu; P W Sternberg
Journal:  Neuron       Date:  1995-01       Impact factor: 17.173

10.  Motifs in brain networks.

Authors:  Olaf Sporns; Rolf Kötter
Journal:  PLoS Biol       Date:  2004-10-26       Impact factor: 8.029

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  46 in total

Review 1.  The Biology of Forgetting-A Perspective.

Authors:  Ronald L Davis; Yi Zhong
Journal:  Neuron       Date:  2017-08-02       Impact factor: 17.173

2.  Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans.

Authors:  Jeffrey P Nguyen; Frederick B Shipley; Ashley N Linder; George S Plummer; Mochi Liu; Sagar U Setru; Joshua W Shaevitz; Andrew M Leifer
Journal:  Proc Natl Acad Sci U S A       Date:  2015-12-28       Impact factor: 11.205

3.  Integration of Plasticity Mechanisms within a Single Sensory Neuron of C. elegans Actuates a Memory.

Authors:  Josh D Hawk; Ana C Calvo; Ping Liu; Agustin Almoril-Porras; Ahmad Aljobeh; María Luisa Torruella-Suárez; Ivy Ren; Nathan Cook; Joel Greenwood; Linjiao Luo; Zhao-Wen Wang; Aravinthan D T Samuel; Daniel A Colón-Ramos
Journal:  Neuron       Date:  2018-01-04       Impact factor: 17.173

4.  A quantitative model of conserved macroscopic dynamics predicts future motor commands.

Authors:  Connor Brennan; Alexander Proekt
Journal:  Elife       Date:  2019-07-11       Impact factor: 8.140

5.  TMC-1 Mediates Alkaline Sensation in C. elegans through Nociceptive Neurons.

Authors:  Xiang Wang; Guang Li; Jie Liu; Jianfeng Liu; X Z Shawn Xu
Journal:  Neuron       Date:  2016-06-16       Impact factor: 17.173

6.  Pharmacological characterization of a homomeric nicotinic acetylcholine receptor formed by Ancylostoma caninum ACR-16.

Authors:  Shivani Choudhary; James G Tipton; Melanie Abongwa; Matthew T Brewer; Jeba Jesudoss Chelladurai; Nicole Musselman; Richard J Martin; Alan P Robertson
Journal:  Invert Neurosci       Date:  2019-09-05

7.  Calcium dynamics regulating the timing of decision-making in C. elegans.

Authors:  Yuki Tanimoto; Akiko Yamazoe-Umemoto; Kosuke Fujita; Yuya Kawazoe; Yosuke Miyanishi; Shuhei J Yamazaki; Xianfeng Fei; Karl Emanuel Busch; Keiko Gengyo-Ando; Junichi Nakai; Yuichi Iino; Yuishi Iwasaki; Koichi Hashimoto; Koutarou D Kimura
Journal:  Elife       Date:  2017-05-23       Impact factor: 8.140

Review 8.  The Caenorhabditis elegans Transgenic Toolbox.

Authors:  Jeremy Nance; Christian Frøkjær-Jensen
Journal:  Genetics       Date:  2019-08       Impact factor: 4.562

9.  MicroRNA Regulation of nAChR Expression and Nicotine-Dependent Behavior in C. elegans.

Authors:  Manish Rauthan; Jianke Gong; Jinzhi Liu; Zhaoyu Li; Seth A Wescott; Jianfeng Liu; X Z Shawn Xu
Journal:  Cell Rep       Date:  2017-11-07       Impact factor: 9.423

Review 10.  What can a worm learn in a bacteria-rich habitat?

Authors:  He Liu; Yun Zhang
Journal:  J Neurogenet       Date:  2020-10-15       Impact factor: 1.250

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