Literature DB >> 29307713

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

Josh D Hawk1, Ana C Calvo1, Ping Liu2, Agustin Almoril-Porras1, Ahmad Aljobeh1, María Luisa Torruella-Suárez1, Ivy Ren1, Nathan Cook1, Joel Greenwood3, Linjiao Luo4, Zhao-Wen Wang2, Aravinthan D T Samuel5, Daniel A Colón-Ramos6.   

Abstract

Neural plasticity, the ability of neurons to change their properties in response to experiences, underpins the nervous system's capacity to form memories and actuate behaviors. How different plasticity mechanisms act together in vivo and at a cellular level to transform sensory information into behavior is not well understood. We show that in Caenorhabditis elegans two plasticity mechanisms-sensory adaptation and presynaptic plasticity-act within a single cell to encode thermosensory information and actuate a temperature preference memory. Sensory adaptation adjusts the temperature range of the sensory neuron (called AFD) to optimize detection of temperature fluctuations associated with migration. Presynaptic plasticity in AFD is regulated by the conserved kinase nPKCε and transforms thermosensory information into a behavioral preference. Bypassing AFD presynaptic plasticity predictably changes learned behavioral preferences without affecting sensory responses. Our findings indicate that two distinct neuroplasticity mechanisms function together through a single-cell logic system to enact thermotactic behavior. VIDEO ABSTRACT.
Copyright © 2017 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  C. elegans; learning and memory; presynaptic plasticity; sensory adaptation; synaptic plasticity; thermotaxis behavior

Mesh:

Substances:

Year:  2018        PMID: 29307713      PMCID: PMC5806692          DOI: 10.1016/j.neuron.2017.12.027

Source DB:  PubMed          Journal:  Neuron        ISSN: 0896-6273            Impact factor:   17.173


  62 in total

1.  Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined Thermal stimuli.

Authors:  William S Ryu; Aravinthan D T Samuel
Journal:  J Neurosci       Date:  2002-07-01       Impact factor: 6.167

2.  Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans.

Authors:  Matthew Beverly; Sriram Anbil; Piali Sengupta
Journal:  J Neurosci       Date:  2011-08-10       Impact factor: 6.167

Review 3.  Traces of Drosophila memory.

Authors:  Ronald L Davis
Journal:  Neuron       Date:  2011-04-14       Impact factor: 17.173

4.  Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene.

Authors:  O Hobert; I Mori; Y Yamashita; H Honda; Y Ohshima; Y Liu; G Ruvkun
Journal:  Neuron       Date:  1997-08       Impact factor: 17.173

Review 5.  DNA transformation.

Authors:  C Mello; A Fire
Journal:  Methods Cell Biol       Date:  1995       Impact factor: 1.441

6.  Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search.

Authors:  Cory M Root; Kang I Ko; Amir Jafari; Jing W Wang
Journal:  Cell       Date:  2011-04-01       Impact factor: 41.582

7.  CaMKI-dependent regulation of sensory gene expression mediates experience-dependent plasticity in the operating range of a thermosensory neuron.

Authors:  Yanxun V Yu; Harold W Bell; Dominique Glauser; Stephen D Van Hooser; Miriam B Goodman; Piali Sengupta
Journal:  Neuron       Date:  2014-11-20       Impact factor: 17.173

8.  A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans.

Authors:  David Biron; Mayumi Shibuya; Christopher Gabel; Sara M Wasserman; Damon A Clark; Adam Brown; Piali Sengupta; Aravinthan D T Samuel
Journal:  Nat Neurosci       Date:  2006-11-05       Impact factor: 24.884

9.  Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans.

Authors:  Daniel Ramot; Bronwyn L MacInnis; Miriam B Goodman
Journal:  Nat Neurosci       Date:  2008-08       Impact factor: 24.884

10.  Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons.

Authors:  Donovan Ventimiglia; Cornelia I Bargmann
Journal:  Elife       Date:  2017-11-21       Impact factor: 8.140

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  26 in total

1.  Maturation and Clearance of Autophagosomes in Neurons Depends on a Specific Cysteine Protease Isoform, ATG-4.2.

Authors:  Sarah E Hill; Karlina J Kauffman; Mia Krout; Janet E Richmond; Thomas J Melia; Daniel A Colón-Ramos
Journal:  Dev Cell       Date:  2019-03-14       Impact factor: 12.270

2.  Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans.

Authors:  Sophie Rengarajan; Kristen A Yankura; Manon L Guillermin; Wendy Fung; Elissa A Hallem
Journal:  Proc Natl Acad Sci U S A       Date:  2019-01-16       Impact factor: 11.205

3.  Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation.

Authors:  Domenica Ippolito; Saurabh Thapliyal; Dominique A Glauser
Journal:  Elife       Date:  2021-11-12       Impact factor: 8.140

4.  Diverse states and stimuli tune olfactory receptor expression levels to modulate food-seeking behavior.

Authors:  Talya S Kramer; Malvika Dua; Ian G McLachlan; Elizabeth M DiLoreto; Matthew A Gomes; Ugur Dag; Jagan Srinivasan; Steven W Flavell
Journal:  Elife       Date:  2022-08-31       Impact factor: 8.713

5.  The neural basis of heat seeking in a human-infective parasitic worm.

Authors:  Astra S Bryant; Felicitas Ruiz; Joon Ha Lee; Elissa A Hallem
Journal:  Curr Biol       Date:  2022-04-27       Impact factor: 10.900

6.  OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans.

Authors:  Ichiro Aoki; Paola Jurado; Kanji Nawa; Rumi Kondo; Riku Yamashiro; Hironori J Matsuyama; Isidre Ferrer; Shunji Nakano; Ikue Mori
Journal:  PLoS Genet       Date:  2022-06-08       Impact factor: 6.020

Review 7.  Temperature-dependent behaviors of parasitic helminths.

Authors:  Astra S Bryant; Elissa A Hallem
Journal:  Neurosci Lett       Date:  2018-10-15       Impact factor: 3.046

8.  Potential evidence of peripheral learning and memory in the arms of dwarf cuttlefish, Sepia bandensis.

Authors:  Jessica Bowers; Jack Wilson; Tahirah Nimi; Vinoth Sittaramane
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2021-06-14       Impact factor: 1.836

Review 9.  Temperature Sensation: From Molecular Thermosensors to Neural Circuits and Coding Principles.

Authors:  Rui Xiao; X Z Shawn Xu
Journal:  Annu Rev Physiol       Date:  2020-10-21       Impact factor: 19.318

10.  Soma-Targeted Imaging of Neural Circuits by Ribosome Tethering.

Authors:  Yiming Chen; Heeun Jang; Perry W E Spratt; Seher Kosar; David E Taylor; Rachel A Essner; Ling Bai; David E Leib; Tzu-Wei Kuo; Yen-Chu Lin; Mili Patel; Aygul Subkhangulova; Saul Kato; Evan H Feinberg; Kevin J Bender; Zachary A Knight; Jennifer L Garrison
Journal:  Neuron       Date:  2020-06-22       Impact factor: 18.688

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