#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Serotonin modulates behavior-related neural activity of RID interneuron in Caenorhabditis elegans


Autoři: Haruka Mori aff001;  Keita Ashida aff002;  Hisashi Shidara aff001;  Tatsuya Nikai aff001;  Kohji Hotta aff001;  Kotaro Oka aff001
Působiště autorů: Department of Bioscience and Informatics, Faculty of Science and Technology, Keio University, Hiyoshi, Kohoku-ku, Yokohama, Kanagawa, Japan aff001;  Universal Biology Institute, Graduate School of Science, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan aff002;  Department of Biological Sciences, Faculty of Science, Hokkaido University, Kita-ku, Sapporo, Hokkaido, Japan aff003;  Waseda Research Institute for Science and Engineering, Waseda University, Wakamatsucho, Shinjuku, Tokyo, Japan aff004;  Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226044

Souhrn

Animals change their behaviors in response to external stimuli, and numerous neurotransmitters are involved in these behavioral changes. In Caenorhabditis elegans, serotonin (5-HT) affects various behaviors such as inhibition of locomotion, stimulation of egg laying, and pharyngeal pumping. Previous research has shown that the neural activity of the RID interneuron increases when the worm moves forward, and the RID is necessary for sustaining forward locomotion. However, the relationship between 5-HT and neural activity of RID, and how it modulates the behavior of the worm has not been investigated. In this article, we reveal the relationship among 5-HT, RID activity, and the behavior of worms using a custom-made tracking and imaging system. We simultaneously measured the neural activity of the RID and behavior in worms with three conditions: mock animals, animals pre-exposed to 5-HT, and 5-HT receptor mod-1 mutants. As shown in previous research, the neural activity of the RID increased during the transition from backward to forward, whereas it decreased during the transition from forward to backward in mock animals. These changes in neural activity were not observed in animals pre-exposed to 5-HT and mod-1 mutants. Moreover, RID activity was correlated with the velocity of the worm in mock animals. However, this correlation was not observed in animals pre-exposed to 5-HT and mod-1 mutants. Our results demonstrate that 5-HT modulates the activity of the RID interneuron, and we infer that the RID plays a role in modulating forward locomotion by changing its activity through 5-HT.

Klíčová slova:

Animal behavior – Biological locomotion – Caenorhabditis elegans – Fluorescence imaging – Interneurons – Neuroimaging – Neurons – Serotonin


Zdroje

1. Browne CJ, Abela AR, Chu D, Li Z, Ji X, Lambe EK, et al. Dorsal raphe serotonin neurons inhibit operant responding for reward via inputs to the ventral tegmental area but not the nucleus accumbens: evidence from studies combining optogenetic stimulation and serotonin reuptake inhibition. Neuropsychopharmacology. 2019;44: 793–804. doi: 10.1038/s41386-018-0271-x 30420603

2. Pooryasin A, Fiala A. Identified serotonin-releasing neurons induce behavioral quiescence and suppress mating in Drosophila. J Neurosci. 2015;35: 12792–12812. doi: 10.1523/JNEUROSCI.1638-15.2015 26377467

3. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77: 71–94. Available: http://www.ncbi.nlm.nih.gov/pubmed/4366476 4366476

4. White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc B Biol Sci. 1986;314: 1–340. doi: 10.1098/rstb.1986.0056 22462104

5. Pierce-Shimomura JT, Morse TM, Lockery SR. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci. 1999;19: 9557–69. Available: http://www.ncbi.nlm.nih.gov/pubmed/10531458 doi: 10.1523/JNEUROSCI.19-21-09557.1999 10531458

6. Iino Y, Yoshida K. Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. J Neurosci. 2009;29: 5370–5380. doi: 10.1523/JNEUROSCI.3633-08.2009 19403805

7. Yoshimizu T, Shidara H, Ashida K, Hotta K, Oka K. Effect of interactions among individuals on the chemotaxis behaviours of Caenorhabditis elegans. J Exp Biol. 2018;221: jeb182790. doi: 10.1242/jeb.182790 29691312

8. Ashida K, Kato T, Hotta K, Oka K. Multiple tracking and machine learning reveal dopamine modulation for area-restricted foraging behaviors via velocity change in Caenorhabditis elegans. Neurosci Lett. 2019;706: 68–74. doi: 10.1016/j.neulet.2019.05.011 31082452

9. Sawin ER, Ranganathan R, Horvitz HR. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron. 2000;26: 619–631. doi: 10.1016/s0896-6273(00)81199-x 10896158

10. Weinshenker D, Garriga G, Thomas J. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci. 1995;15: 6975–6985. doi: 10.1523/JNEUROSCI.15-10-06975.1995 7472454

11. Rogers CM, Franks CJ, Walker RJ, Burke JF, Holden-Dye L. Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. J Neurobiol. 2001;49: 235–244. doi: 10.1002/neu.1078 11745661

12. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature. 2000;403:560–564. doi: 10.1038/35000609 10676966

13. Ranganathan R, Cannon SC, Horvitz HR. MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. elegans. Nature. 2000;408: 470–475. doi: 10.1038/35044083 11100728

14. Li Z, Li Y, Yi Y, Huang W, Yang S, Niu W, et al. Dissecting a central flip-flop circuit that integrates contradictory sensory cues in C. elegans feeding regulation. Nat Commun. 2012;3: 776. doi: 10.1038/ncomms1780 22491324

15. Lim MA, Chitturi J, Laskova V, Meng J, Findeis D, Wiekenberg A, et al. Neuroendocrine modulation sustains the C. elegans forward motor state. Elife. 2016;5: 1–33. doi: 10.7554/eLife.19887 27855782

16. Chew YL, Tanizawa Y, Cho Y, Zhao B, Yu AJ, Ardiel EL, Rabinowitch I, Bai J, Rankin CH, Lu H, Beets I, Schafer WR. An afferent neuropeptide system transmits mechanosensory signals triggering sensitization and arousal in C. elegans. Neuron. 2018;99(6):1233–1246.e6. doi: 10.1016/j.neuron.2018.08.003 30146306

17. Shidara H, Hotta K, Oka K. Compartmentalized cGMP responses of olfactory sensory neurons in Caenorhabditis elegans. J Neurosci. 2017;37: 3753–3763. doi: 10.1523/JNEUROSCI.2628-16.2017 28270568

18. Li W, Kang L, Piggott BJ, Feng Z, Xu XZS. The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat Commun. 2011;2: 315. doi: 10.1038/ncomms1308 21587232

19. Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science. 1982;216: 1012–4. Available: http://www.ncbi.nlm.nih.gov/pubmed/6805073 doi: 10.1126/science.6805073 6805073


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#