Electric Shock Causes a Fleeing-like Persistent Behavioral Response in the Nematode Caenorhabditis Elegans

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 2023 Aug 18

PMID 37595066

Authors

Ling Fei Tee

Jared J Young

Keisuke Maruyama

Sota Kimura

Ryoga Suzuki

Yuto Endo

Koutarou D Kimura

Affiliations

Soon will be listed here.

Abstract

Behavioral persistency reflects internal brain states, which are the foundations of multiple brain functions. However, experimental paradigms enabling genetic analyses of behavioral persistency and its associated brain functions have been limited. Here, we report novel persistent behavioral responses caused by electric stimuli in the nematode Caenorhabditis elegans. When the animals on bacterial food are stimulated by alternating current, their movement speed suddenly increases 2- to 3-fold, persisting for more than 1 minute even after a 5-second stimulation. Genetic analyses reveal that voltage-gated channels in the neurons are required for the response, possibly as the sensors, and neuropeptide signaling regulates the duration of the persistent response. Additional behavioral analyses implicate that the animal's response to electric shock is scalable and has a negative valence. These properties, along with persistence, have been recently regarded as essential features of emotion, suggesting that C. elegans response to electric shock may reflect a form of emotion, akin to fear.

References

Bellono N, Leitch D, Julius D . Molecular basis of ancestral vertebrate electroreception. Nature. 2017; 543(7645):391-396. PMC: 5354974. DOI: 10.1038/nature21401. View

Schafer W, Kenyon C . A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature. 1995; 375(6526):73-8. DOI: 10.1038/375073a0. View

Mello C, Kramer J, Stinchcomb D, Ambros V . Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991; 10(12):3959-70. PMC: 453137. DOI: 10.1002/j.1460-2075.1991.tb04966.x. View

Kass J, Jacob T, Kim P, Kaplan J . The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J Neurosci. 2001; 21(23):9265-72. PMC: 6763909. View

Cheung B, Cohen M, Rogers C, Albayram O, De Bono M . Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr Biol. 2005; 15(10):905-17. DOI: 10.1016/j.cub.2005.04.017. View

Steger K, Shtonda B, Thacker C, Snutch T, Avery L . The C. elegans T-type calcium channel CCA-1 boosts neuromuscular transmission. J Exp Biol. 2005; 208(Pt 11):2191-203. PMC: 1382270. DOI: 10.1242/jeb.01616. View

van den Burg E, Stoop R . Neuropeptide signalling in the central nucleus of the amygdala. Cell Tissue Res. 2018; 375(1):93-101. DOI: 10.1007/s00441-018-2862-6. View

Kimura K, Fujita K, Katsura I . Enhancement of odor avoidance regulated by dopamine signaling in Caenorhabditis elegans. J Neurosci. 2010; 30(48):16365-75. PMC: 6634857. DOI: 10.1523/JNEUROSCI.6023-09.2010. View

Coburn C, Bargmann C . A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron. 1996; 17(4):695-706. DOI: 10.1016/s0896-6273(00)80201-9. View

10.

Toth I, Neumann I, Slattery D . Social fear conditioning: a novel and specific animal model to study social anxiety disorder. Neuropsychopharmacology. 2012; 37(6):1433-43. PMC: 3327848. DOI: 10.1038/npp.2011.329. View

11.

Goodman M, Sengupta P . How Senses Mechanical Stress, Temperature, and Other Physical Stimuli. Genetics. 2019; 212(1):25-51. PMC: 6499529. DOI: 10.1534/genetics.118.300241. View

12.

Gabel C, Gabel H, Pavlichin D, Kao A, Clark D, Samuel A . Neural circuits mediate electrosensory behavior in Caenorhabditis elegans. J Neurosci. 2007; 27(28):7586-96. PMC: 6672606. DOI: 10.1523/JNEUROSCI.0775-07.2007. View

13.

Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R . Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron. 2002; 35(2):307-18. DOI: 10.1016/s0896-6273(02)00757-2. View

14.

Yemini E, Jucikas T, Grundy L, Brown A, Schafer W . A database of Caenorhabditis elegans behavioral phenotypes. Nat Methods. 2013; 10(9):877-9. PMC: 3962822. DOI: 10.1038/nmeth.2560. View

15.

Comeras L, Herzog H, Tasan R . Neuropeptides at the crossroad of fear and hunger: a special focus on neuropeptide Y. Ann N Y Acad Sci. 2019; 1455(1):59-80. PMC: 6899945. DOI: 10.1111/nyas.14179. View

16.

Randi F, Leifer A . Measuring and modeling whole-brain neural dynamics in Caenorhabditis elegans. Curr Opin Neurobiol. 2020; 65:167-175. PMC: 7801769. DOI: 10.1016/j.conb.2020.11.001. View

17.

Bargmann C . Chemosensation in C. elegans. WormBook. 2007; :1-29. PMC: 4781564. DOI: 10.1895/wormbook.1.123.1. View

18.

Korte S, de Boer S, Bohus B . Fear-potentiation in the elevated plus-maze test depends on stressor controllability and fear conditioning. Stress. 2008; 3(1):27-40. DOI: 10.3109/10253899909001110. View

19.

Bowers M, Choi D, Ressler K . Neuropeptide regulation of fear and anxiety: Implications of cholecystokinin, endogenous opioids, and neuropeptide Y. Physiol Behav. 2012; 107(5):699-710. PMC: 3532931. DOI: 10.1016/j.physbeh.2012.03.004. View

20.

Mohammad F, Aryal S, Ho J, Stewart J, Norman N, Tan T . Ancient Anxiety Pathways Influence Drosophila Defense Behaviors. Curr Biol. 2016; 26(7):981-6. PMC: 4826436. DOI: 10.1016/j.cub.2016.02.031. View