1,351
Views
9
CrossRef citations to date
0
Altmetric
Section 6: Survival, aging and disease

Neuromodulators: an essential part of survival

&
Pages 475-481 | Received 20 Aug 2020, Accepted 15 Oct 2020, Published online: 10 Nov 2020

References

  • Alkema, M.J., Hunter-Ensor, M., Ringstad, N., & Horvitz, H.R. (2005). Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron, 46(2), 247–260. doi:10.1016/j.neuron.2005.02.024
  • Aprison, E.Z., & Ruvinsky, I. (2019). Dynamic regulation of adult-specific functions of the nervous system by signaling from the reproductive system. Current Biology : CB, 29(23), 4116–4123.e4113. doi:10.1016/j.cub.2019.10.011
  • Ardiel, E.L., Giles, A.C., Yu, A.J., Lindsay, T.H., Lockery, S.R., & Rankin, C.H. (2016). Dopamine receptor DOP-4 modulates habituation to repetitive photoactivation of a C. elegans polymodal nociceptor. Learning & Memory (Cold Spring Harbor, N.Y.), 23(10), 495–503. doi:10.1101/lm.041830.116
  • Avery, L. and You, Y.J. C. elegans feeding, WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.150.1
  • Banerjee, N., Bhattacharya, R., Gorczyca, M., Collins, K.M., & Francis, M.M. (2017). Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior. PLoS Genetics, 13(4), e1006697. doi:10.1371/journal.pgen.1006697
  • Bargmann, C.I. (2012). Beyond the connectome: How neuromodulators shape neural circuits. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 34(6), 458–465. doi:10.1002/bies.201100185
  • Bargmann, C.I., & Marder, E. (2013). From the connectome to brain function. Nature Methods, 10(6), 483–490. doi:10.1038/nmeth.2451
  • Beets, I., Temmerman, L., Janssen, T., & Schoofs, L. (2013). Ancient neuromodulation by vasopressin/oxytocin-related peptides. Worm, 2(2), e24246. doi:10.4161/worm.24246
  • Bentley, B., Branicky, R., Barnes, C.L., Chew, Y.L., Yemini, E., Bullmore, E.T., … Schafer, W.R. (2016). The multilayer connectome of Caenorhabditis elegans. PLoS Computational Biology, 12(12), e1005283. doi:10.1371/journal.pcbi.1005283
  • Bettinger, J.C., & McIntire, S.L. (2004). State-dependency in C. elegans. Genes Brain, and Behavior, 3(5), 266–272. doi:10.1111/j.1601-183X.2004.00080.x
  • Bhattacharya, R., & Francis, M.M. (2015). In the proper context: Neuropeptide regulation of behavioral transitions during food searching. Worm, 4(3), e1062971. doi:10.1080/21624054.2015.1062971
  • Cassada, R.C., & Russell, R.L. (1975). The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Developmental Biology, 46(2), 326–342. doi:10.1016/0012-1606(75)90109-8
  • Cermak, N., Yu, S.K., Clark, R., Huang, Y.C., Baskoylu, S.N., & Flavell, S.W. (2020). Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans. eLife, 9, e57093. doi:10.7554/eLife.57093
  • Chalasani, S.H., Kato, S., Albrecht, D.R., Nakagawa, T., Abbott, L.F., & Bargmann, C.I. (2010). Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons. Nature Neuroscience, 13(5), 615–621. doi:10.1038/nn.2526
  • Chase, D.L., & Koelle, M.R. (2007). Biogenic amine neurotransmitters in C. elegans. WormBook, 1–15. doi:10.1895/wormbook.1.132.1
  • Chen, C., Itakura, E., Nelson, G.M., Sheng, M., Laurent, P., Fenk, L.A., … de Bono, M. (2017). IL-17 is a neuromodulator of Caenorhabditis elegans sensory responses. Nature, 542(7639), 43–48. doi:10.1038/nature20818
  • Chen, Y.C., Chen, H.J., Tseng, W.C., Hsu, J.M., Huang, T.T., Chen, C.H., & Pan, C.L. (2016). A C. elegans thermosensory circuit regulates longevity through crh-1/CREB-dependent flp-6 neuropeptide signaling . Developmental Cell, 39(2), 209–223. doi:10.1016/j.devcel.2016.08.021
  • Cheon, Y.-J., Hwang, H., & Kim, K. (2020). Plasticity of pheromone-mediated avoidance behavior in C. elegans. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1802723
  • Churgin, M.A., McCloskey, R.J., Peters, E., & Fang-Yen, C. (2017). Antagonistic serotonergic and octopaminergic neural circuits mediate food-dependent locomotory behavior in Caenorhabditis elegans. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 37(33), 7811–7823. doi:10.1523/JNEUROSCI.2636-16.2017
  • Chute, C.D., DiLoreto, E.M., Zhang, Y.K., Reilly, D.K., Rayes, D., Coyle, V.L., … Srinivasan, J. (2019). Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans. Nature Communications, 10(1), 3186. doi:10.1038/s41467-019-11240-7
  • Cruz-Corchado, J., Ooi, F.K., Das, S., & Prahlad, V. (2020). Global transcriptome changes that accompany alterations in serotonin levels in Caenorhabditis elegans. G3 (Bethesda, Md.), 10(4), 1225–1246. doi:10.1534/g3.120.401088
  • Curran, K.P., & Chalasani, S.H. (2012). Serotonin circuits and anxiety: What can invertebrates teach us? Invertebrate Neuroscience, 12(2), 81–92. doi:10.1007/s10158-012-0140-y
  • Di Giovangiulio, M., Verheijden, S., Bosmans, G., Stakenborg, N., Boeckxstaens, G.E., & Matteoli, G. (2015). The neuromodulation of the intestinal immune system and its relevance in inflammatory bowel disease. Frontiers in Immunology, 6, 590. doi:10.3389/fimmu.2015.00590
  • Du, X., Pang, T., & Hannan, A. (2013). A tale of two maladies? Pathogenesis of depression with and without the Huntington’s disease gene mutation. Frontiers in Neurology, 4, 81. doi:10.3389/fneur.2013.00081
  • Elsworthy, R.J., & Aldred, S. (2019). Depression in Alzheimer's disease: An alternative role for selective serotonin reuptake inhibitors? Journal of Alzheimer's Disease, 69(3), 651–661. doi:10.3233/JAD-180780
  • Ezcurra, M., Walker, D.S., Beets, I., Swoboda, P., & Schafer, W.R. (2016). Neuropeptidergic signaling and active feeding state inhibit nociception in Caenorhabditis elegans. Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 36(11), 3157–3169. doi:10.1523/JNEUROSCI.1128-15.2016
  • Fernandes de Abreu, D.A., Caballero, A., Fardel, P., Stroustrup, N., Chen, Z., Lee, K., … Ch'ng, Q. (2014). An insulin-to-insulin regulatory network orchestrates phenotypic specificity in development and physiology. PLoS Genetics, 10(3), e1004225. doi:10.1371/journal.pgen.1004225
  • Gems, D., Sutton, A.J., Sundermeyer, M.L., Albert, P.S., King, K.V., Edgley, M.L., … Riddle, D.L. (1998). Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics, 150(1), 129–155.
  • Ghosh, D.D., Sanders, T., Hong, S., McCurdy, L.Y., Chase, D.L., Cohen, N., … Nitabach, M.N. (2016). Neural architecture of hunger-dependent multisensory decision making in C. elegans. Neuron, 92(5), 1049–1062. doi:10.1016/j.neuron.2016.10.030
  • Glauser, D. A., Chen, W. C., Agin, R., Macinnis, B. L., Hellman, A. B., Garrity, P. A., Goodman, M. B. (2011). Heat avoidance is regulated by transient receptor potential (TRP) channels and a neuropeptide signaling pathway in Caenorhabditis elegans. Genetics, 188(1), 91–103. doi:10.1534/genetics.111.127100
  • Guo, M., Wu, T.-H., Song, Y.-X., Ge, M.-H., Su, C.-M., Niu, W.-P., … Wu, Z.-X. (2015). Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans. Nature Communications, 6, 5655. doi:10.1038/ncomms6655
  • Hapiak, V., Summers, P., Ortega, A., Law, W.J., Stein, A., & Komuniecki, R. (2013). Neuropeptides amplify and focus the monoaminergic inhibition of nociception in Caenorhabditis elegans. Journal of Neuroscience, 33(35), 14107–14116. doi:10.1523/JNEUROSCI.1324-13.2013
  • Hare, E.E., & Loer, C.M. (2004). Function and evolution of the serotonin-synthetic bas-1 gene and other aromatic amino acid decarboxylase genes in Caenorhabditis. BMC Evolutionary Biology, 4, 24. doi:10.1186/1471-2148-4-24
  • Hobert, O. (2013). The neuronal genome of Caenorhabditis elegans. WormBook, 1–106. doi:10.1895/wormbook.1.161.1
  • Honer, M., Buscemi, K., Barrett, N., Riazati, N., Orlando, G., & Nelson, M.D. (2020). Orcokinin neuropeptides regulate sleep in Caenorhabditis elegans. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1830084
  • Horvitz, H.R., Chalfie, M., Trent, C., Sulston, J.E., & Evans, P.D. (1982). Serotonin and octopamine in the nematode Caenorhabditis elegans. Science (New York, N.Y.), 216(4549), 1012–1014. doi:10.1126/science.6805073
  • Ishita, Y., Chihara, T., & Okumura, M. (2020). Serotonergic modulation of feeding behavior in Caenorhabditis elegans and other related nematodes. Neuroscience Research, 154, 9–19. doi:10.1016/j.neures.2019.04.006
  • Kagawa-Nagamura, Y., Gengyo-Ando, K., Ohkura, M., & Nakai, J. (2018). Role of tyramine in calcium dynamics of GABAergic neurons and escape behavior in Caenorhabditis elegans. Zoological Letters, 4, 19. doi:10.1186/s40851-018-0103-1
  • Kenyon, C., Chang, J., Gensch, E., Rudner, A., & Tabtiang, R. (1993). A C. elegans mutant that lives twice as long as wild type. Nature, 366(6454), 461–464. doi:10.1038/366461a0
  • Kenyon, C.J. (2010). The genetics of ageing. Nature, 464(7288), 504–512. doi:10.1038/nature08980
  • Kim, B., Lee, J., Kim, Y., & Lee, S.-J.V. (2020). Regulatory systems that mediate the effects of temperature on the lifespan of Caenorhabdities elegans. Journal of Neurogenetics, 34. doi: 10.1080/01677063.2020.1781849
  • Kim, D.H., & Flavell, S.W. (2020). Host-microbe interactions and the behavior of Caenorhabditis elegans. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1802724
  • Kimura, K.D., Tissenbaum, H.A., Liu, Y., & Ruvkun, G. (1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science (New York, N.Y.), 277(5328), 942–946. doi:10.1126/science.277.5328.942
  • Kupfermann, I. (1967). Stimulation of egg laying: Possible neuroendocrine function of bag cells of abdominal ganglion of Aplysia californica. Nature, 216(5117), 814–815. doi:10.1038/216814a0
  • Lee, J.S., Shih, P.Y., Schaedel, O.N., Quintero-Cadena, P., Rogers, A.K., & Sternberg, P.W. (2017). FMRFamide-like peptides expand the behavioral repertoire of a densely connected nervous system. Proceedings of the National Academy of Sciences of the United States of America, 114(50), E10726–E10735. doi:10.1073/pnas.1710374114
  • Lezi, E., Zhou, T., Koh, S., Chuang, M., Sharma, R., Pujol, N., … Yan, D. (2018). An antimicrobial peptide and its neuronal receptor regulate dendrite degeneration in aging and infection. Neuron, 97(1), 125–138.e125. doi:10.1016/j.neuron.2017.12.001
  • Li, C., & Kim, K. (2008). Neuropeptides. WormBook, 1–36. doi:10.1895/wormbook.1.142.1
  • Li, C., Kim, K., & Nelson, L.S. (1999). FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Research, 848(1–2), 26–34. doi:10.1016/S0006-8993(99)01972-1
  • Li, Y., Tiedemann, L., von Frieling, J., Nolte, S., El-Kholy, S., Stephano, F., … Roeder, T. (2017). The role of monoaminergic neurotransmission for metabolic control in the fruit fly Drosophila melanogaster. Frontiers in Systems Neuroscience, 11, 60. doi:10.3389/fnsys.2017.00060
  • Liang, J.J.H., McKinnon, I.A., & Rankin, C.H. (2020). The contribution of C. elegans neurogenetics to understanding neurodegenerative diseases. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1803302
  • Lints, R., & Emmons, S.W. (1999). Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFb family signaling pathway and a Hox gene. Development, 126(24), 5819–5831.
  • Liu, H., & Zhang, Y. (2020). What can a worm learn in a bacteria-rich habitat? Journal of Neurogenetics, 34. doi: 10.1080/01677063.2020.1829614
  • Loer, C.M., & Kenyon, C.J. (1993). Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 13(12), 5407–5417. doi:10.1523/JNEUROSCI.13-12-05407.1993
  • Loer, C.M., & Rivard, L. (2007). Evolution of neuronal patterning in free-living rhabditid nematodes I: Sex-specific serotonin-containing neurons. Journal of Comparative Neurology, 502(5), 736–767. doi:10.1002/cne.21288
  • Luedtke, S., O'Connor, V., Holden-Dye, L., & Walker, R.J. (2010). The regulation of feeding and metabolism in response to food deprivation in Caenorhabditis elegans. Invertebrate Neuroscience, 10(2), 63–76. doi:10.1007/s10158-010-0112-z
  • Macosko, E.Z., Pokala, N., Feinberg, E.H., Chalasani, S.H., Butcher, R.A., Clardy, J., & Bargmann, C.I. (2009). A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature, 458(7242), 1171–1175. doi:10.1038/nature07886
  • Marder, E. (2012). Neuromodulation of neuronal circuits: Back to the future. Neuron, 76(1), 1–11. doi:10.1016/j.neuron.2012.09.010
  • Mills, H., Wragg, R., Hapiak, V., Castelletto, M., Zahratka, J., Harris, G., … Komuniecki, R. (2012). Monoamines and neuropeptides interact to inhibit aversive behaviour in Caenorhabditis elegans. EMBO Journal, 31(3), 667–678. doi:10.1038/emboj.2011.422
  • Mor, D.E., Tsika, E., Mazzulli, J.R., Gould, N.S., Kim, H., Daniels, M.J., … Ischiropoulos, H. (2017). Dopamine induces soluble α-synuclein oligomers and nigrostriatal degeneration. Nature Neuroscience, 20(11), 1560–1568. doi:10.1038/nn.4641
  • Muirhead, C.S., & Srinivasan, J. (2020). Small molecule signals mediate social behaviors in C. elegans. Journal of Neurogenetics, 34. doi: 10.1080/01677063.2020.1808634
  • Mylenko, M., Boland, S., Penkov, S., Sampaio, J.L., Lombardot, B., Vorkel, D., … Kurzchalia, T.V. (2016). NAD + Is a food component that promotes exit from dauer diapause in Caenorhabditis elegans. PLoS One, 11(12), e0167208. doi:10.1371/journal.pone.0167208
  • Nathoo, A.N., Moeller, R.A., Westlund, B.A., & Hart, A.C. (2001). Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proceedings of the National Academy of Sciences of the United States of America, 98(24), 14000–14005. doi:10.1073/pnas.241231298
  • O'Donnell, M.P., Fox, B.W., Chao, P.H., Schroeder, F.C., & Sengupta, P. (2020). A neurotransmitter produced by gut bacteria modulates host sensory behaviour. Nature, 583(7816), 415–420. doi:10.1038/s41586-020-2395-5
  • Ohno, Y., Shimizu, S., Tokudome, K., Kunisawa, N., & Sasa, M. (2015). New insight into the therapeutic role of the serotonergic system in Parkinson's disease. Progress in Neurobiology, 134, 104–121. doi:10.1016/j.pneurobio.2015.09.005
  • Oranth, A., Schultheis, C., Tolstenkov, O., Erbguth, K., Nagpal, J., Hain, D., … Gottschalk, A. (2018). Food sensation modulates locomotion by dopamine and neuropeptide signaling in a distributed neuronal network. Neuron, 100(6), 1414–1428. e1410. doi:10.1016/j.neuron.2018.10.024
  • Park, S.K., Link, C.D., & Johnson, T.E. (2010). Life-span extension by dietary restriction is mediated by NLP-7 signaling and coelomocyte endocytosis in C. elegans. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 24(2), 383–392. doi:10.1096/fj.09-142984
  • Pierce, S.B., Costa, M., Wisotzkey, R., Devadhar, S., Homburger, S.A., Buchman, A.R., … Ruvkun, G. (2001). Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes & Development, 15(6), 672–686. doi:10.1101/gad.867301
  • Pocock, R., & Hobert, O. (2010). Hypoxia activates a latent circuit for processing gustatory information in C. elegans. Nature Neuroscience 13(5), 610–614. doi: 10.1038/nn.2537
  • Politis, M., & Niccolini, F. (2015). Serotonin in Parkinson's disease. Behavioural Brain Research, 277, 136–145. doi:10.1016/j.bbr.2014.07.037
  • Prahlad, V. (2020). The discovery and consequences of the central role of the nervous system in the control of protein homeostasis. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1771333
  • Qin, J., & Wheeler, A.R. (2007). Maze exploration and learning in C. elegans. Lab on a Chip, 7(2), 186–192. doi:10.1039/b613414a
  • Rankin, C.H. (2006). Nematode behavior: The taste of success, the smell of danger!. Current Biology, 16(3), R89–R91. doi:10.1016/j.cub.2006.01.025
  • Reddy, K. C., Andersen, E. C., Kruglyak, L., & Kim, D. H. (2009). A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science, 323(5912), 382-384. doi:10.1126/science.1166527
  • Rengarajan, S., Yankura, K.A., Guillermin, M.L., Fung, W., & Hallem, E.A. (2019). Feeding state sculpts a circuit for sensory valence in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 116(5), 1776–1781. doi:10.1073/pnas.1807454116
  • Riddle, D.L., Swanson, M.M., & Albert, P.S. (1981). Interacting genes in nematode dauer larva formation. Nature, 290(5808), 668–671. doi:10.1038/290668a0
  • Ringstad, N. (2017). Neuromodulation: The fevered mind of the worm. Current Biology, 27(8), R315–R317. doi:10.1016/j.cub.2017.03.005
  • Rivard, L., Srinivasan, J., Stone, A., Ochoa, S., Sternberg, P.W., & Loer, C.M. (2010). A comparison of experience-dependent locomotory behaviors and biogenic amine neurons in nematode relatives of Caenorhabditis elegans. BMC Neuroscience, 11, 22. doi:10.1186/1471-2202-11-22
  • Roeder, T. (2020). The control of metabolic traits by octopamine and tyramine in invertebrates. The Journal of Experimental Biology, 223(7), jeb194282. doi:10.1242/jeb.194282
  • Rogers, C., Reale, V., Kim, K., Chatwin, H., Li, C., Evans, P., & de Bono, M. (2003). Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat Neurosci, 6(11), 1178–1185. doi:10.1038/nn1140
  • Sanyal, S., Wintle, R.F., Kindt, K.S., Nuttley, W.M., Arvan, R., Fitzmaurice, P., … Van Tol, H.H.M. (2004). Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. The EMBO Journal, 23(2), 473–482. doi:10.1038/sj.emboj.7600057
  • Sawin, E.R., Ranganathan, R., & Horvitz, H.R. (2000). C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron, 26(3), 619–631. doi:10.1016/S0896-6273(00)81199-X
  • Schafer, W.F. (2006). Genetics of egg-laying in worms. Annual Review of Genetics, 40, 487–509. doi:10.1146/annurev.genet.40.110405.090527
  • Sellegounder, D., Yuan, C.H., Wibisono, P., Liu, Y., & Sun, J. (2018). Octopaminergic signaling mediates neural regulation of innate immunity in Caenorhabditis elegans. mBio, 9(5), e01645. doi:10.1128/mBio.01645-18
  • Serrano-Saiz, E., Pereira, L., Gendrel, M., Aghayeva, U., Bhattacharya, A., Howell, K., … Hobert, O. (2017). A neurotransmitter atlas of the Caenorhabditis elegans male nervous system reveals sexually dimorphic neurotransmitter usage. Genetics, 206(3), 1251–1269. doi:10.1534/genetics.117.202127
  • Sharp, T., & Cowen, P.J. (2011). 5-HT and depression: Is the glass half-full? Current Opinion in Pharmacology, 11(1), 45–51. doi:10.1016/j.coph.2011.02.003
  • Srinivasan, S. (2020). Neuroendocrine control of lipid metabolism: Lessons from C. elegans. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1777116
  • Strumwasser, F., Jacklet, J.W., & Alvarez, R.B. (1969). A seasonal rhythm in the neural extract induction of behavioral egg-laying in Aplysia. Comparative Biochemistry and Physiology, 29(1), 197–206. doi:10.1016/0010-406X(69)91735-6
  • Styer, K. L., Singh, V., Macosko, E., Steele, S. E., Bargmann, C. I., & Aballay, A. (2008). Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science, 322(5900), 460–464. doi:10.1126/science.1163673.
  • Sulston, J., Dew, M., & Brenner, S. (1975). Dopaminergic neurons in the nematode Caenorhabditis elegans. Journal of Comparative Neurology, 163(2), 215–226. doi:10.1002/cne.901630207
  • Suo, S., Culotti, J.G., & Van Tol, H.H. (2009). Dopamine counteracts octopamine signalling in a neural circuit mediating food response in C. elegans. The EMBO Journal, 28(16), 2437–2448. doi:10.1038/emboj.2009.194
  • Suo, S., Harada, K., Matsuda, S., Kyo, K., Wang, M., Maruyama, K., … Tsuboi, T. (2019). Sexually dimorphic regulation of behavioral states by dopamine in Caenorhabditis elegans. Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 39(24), 4668–4683. doi:10.1523/JNEUROSCI.2985-18.2019
  • Taghert, P.H., & Nitabach, M.N. (2012). Peptide neuromodulation in invertebrate model systems. Neuron, 76(1), 82–97. doi:10.1016/j.neuron.2012.08.035
  • Takeishi, A., Takagaki, N., & Kuhara, A. (2020). Temperature signaling underlying thermotaxis and cold tolerance in Caenorhabditis elegans. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1734001
  • Toevs, L.A., & Brackenbury, R.W. (1969). Bag cell-specific proteins and the humoral control of egg laying in Aplysia californica. Comparative Biochemistry and Physiology, 29(1), 207–216. doi:10.1016/0010-406X(69)91736-8
  • Wu, T., Duan, F., Yang, W., Liu, H., Caballero, A., Fernandes de Abreu, D.A., … Zhang, Y. (2019). Pheromones modulate learning by regulating the balanced signals of two insulin-like peptides. Neuron, 104(6), 1095–1109. e1095. doi:10.1016/j.neuron.2019.09.006
  • Yang, H., Lee, B.Y., Yim, H., & Lee, J. (2020). Neurogenetics of nictation, a dispersal strategy in nematodes. Journal of Neurogenetics, 34.doi: 10.1080/01677063.2020.1788552
  • Zang, K.E., Ho, E., & Ringstad, N. (2017). Inhibitory peptidergic modulation of C. elegans serotonin neurons is gated by T-type calcium channels. eLife, 6, e22771. doi:10.7554/eLife.22771

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.