2,074
Views
5
CrossRef citations to date
0
Altmetric
Section 3: From inputs to outputs

What can a worm learn in a bacteria-rich habitat?

&
Pages 369-377 | Received 23 Apr 2020, Accepted 17 Sep 2020, Published online: 15 Oct 2020

References

  • Alcedo, J., & Zhang, Y. (2013). Molecular and cellular circuits underlying Caenorhabditis elegans olfactory plasticity. In R. Menzel, and P. Benjamine, eds., Invertebrate learning and memory (pp. 112–123). San Diego, CA: Elsevier Academic Press Inc.
  • Aoki, I., & Mori, I. (2015). Molecular biology of thermosensory transduction in C. elegans. Current Opinion in Neurobiology, 34, 117–124. doi:10.1016/j.conb.2015.03.011
  • Aprison, E.Z., & Ruvinsky, I. (2019). Coordinated behavioral and physiological responses to a social signal are regulated by a shared neuronal circuit. Current Biology , 29 (23), 4108–4115 e4104. doi:10.1016/j.cub.2019.10.012
  • Bailey, C.H., & Chen, M. (1983). Morphological basis of long-term habituation and sensitization in Aplysia. Science, 220 (4592), 91–93. doi:10.1126/science.6828885
  • Bargmann, C.I. (2006). Chemosensation in C. elegans. WormBook, p. 1–29.
  • Bargmann, C.I., Hartwieg, E., & Horvitz, H.R. (1993). Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell, 74 (3), 515–527. doi:10.1016/0092-8674(93)80053-H
  • Bayer, E.A., & Hobert, O. (2018). Past experience shapes sexually dimorphic neuronal wiring through monoaminergic signalling. Nature, 561 (7721), 117–121. doi:10.1038/s41586-018-0452-0
  • Bharadwaj, P.S., & Hall, S.E. (2017). Endogenous RNAi pathways are required in neurons for Dauer formation in Caenorhabditis elegans. Genetics, 205 (4), 1503–1516. doi:10.1534/genetics.116.195438
  • Biron, D., Shibuya, M., Gabel, C., Wasserman, S.M., Clark, D.A., Brown, A., … Samuel, A.D. (2006). A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans. Nature Neuroscience, 9, 1499–1505. doi:10.1038/nn1796
  • Brandt, J.P., Aziz-Zaman, S., Juozaityte, V., Martinez-Velazquez, L.A., Petersen, J.G., Pocock, R., & Ringstad, N. (2012). A single gene target of an ETS-family transcription factor determines neuronal CO2-chemosensitivity. PLoS One, 7 (3), e34014. doi:10.1371/journal.pone.0034014
  • Brandt, J.P., & Ringstad, N. (2015). Toll-like receptor signaling promotes development and function of sensory neurons required for a C. elegans pathogen-avoidance behavior. Current Biology, 25 (17), 2228–2237. doi:10.1016/j.cub.2015.07.037
  • Bretscher, A.J., Busch, K.E., & de Bono, M. (2008). A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, 105 (23), 8044–8049. doi:10.1073/pnas.0707607105
  • Burton, N.O., Furuta, T., Webster, A.K., Kaplan, R.E., Baugh, L.R., Arur, S., & Horvitz, H.R. (2017). Insulin-like signalling to the maternal germline controls progeny response to osmotic stress. Nature Cell Biology, 19 (3), 252–257. doi:10.1038/ncb3470
  • Burton, N.O., Riccio, C., Dallaire, A., Price, J., Jenkins, B., Koulman, A., & Miska, E.A. (2019). C. elegans heritably adapts to P. vranovensis infection via a mechanism that requires the cysteine synthases cysl-1 and cysl-2. Nature Communications. doi:10.1038/s41467-020-15555-8
  • Butcher, R.A., Fujita, M., Schroeder, F.C., & Clardy, J. (2007). Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nature Chemical Biology, 3 (7), 420–422. doi:10.1038/nchembio.2007.3
  • Calhoun, A.J., Tong, A., Pokala, N., Fitzpatrick, J.A., Sharpee, T.O., & Chalasani, S.H. (2015). Neural mechanisms for evaluating environmental variability in Caenorhabditis elegans. Neuron, 86 (2), 428–441. doi:10.1016/j.neuron.2015.03.026
  • Chalasani, S.H., Chronis, N., Tsunozaki, M., Gray, J.M., Ramot, D., Goodman, M.B., & Bargmann, C.I. (2007). Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature, 450 (7166), 63–70. doi:10.1038/nature06292
  • Chalfie, M. (2009). Neurosensory mechanotransduction. Nature Reviews. Molecular Cell Biology, 10 (1), 44–52. doi:10.1038/nrm2595
  • Chang, H.C., Paek, J., & Kim, D.H. (2011). Natural polymorphisms in C. elegans HECW-1 E3 ligase affect pathogen avoidance behaviour. Nature, 480 (7378), 525–529. doi:10.1038/nature10643
  • Cheung, B.H., Cohen, M., Rogers, C., Albayram, O., & de Bono, M. (2005). Experience-dependent modulation of C. elegans behavior by ambient oxygen. Current Biology, 15 (10), 905–917. doi:10.1016/j.cub.2005.04.017
  • Choi, M.-K., Liu, H., Wu, T., Yang, W., & Zhang, Y. (2020). NMDAR-mediated modulation of gap junction circuit regulates olfactory learning in C. elegans. Nature Communications, 11 (1), 1–16. doi:10.1038/s41467-020-17218-0
  • Colbert, H.A., & Bargmann, C.I. (1995). Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron, 14 (4), 803–812. doi:10.1016/0896-6273(95)90224-4
  • Das, S., Ooi, F.K., Cruz Corchado, J., Fuller, L.C., Weiner, J.A., & Prahlad, V. (2020). Serotonin signaling by maternal neurons upon stress ensures progeny survival. eLife, 9, e55246. doi:10.7554/eLife.55246
  • de Bono, M., & Maricq, A.V. (2005). Neuronal substrates of complex behaviors in C. elegans. Annual Review of Neuroscience, 28, 451–501. doi:10.1146/annurev.neuro.27.070203.144259
  • Demoinet, E., Li, S., & Roy, R. (2017). AMPK blocks starvation-inducible transgenerational defects in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 114 (13), E2689–E2698. doi:10.1073/pnas.1616171114
  • Donnelly, J.L., Clark, C.M., Leifer, A.M., Pirri, J.K., Haburcak, M., Francis, M.M., … Alkema, M.J. (2013). Monoaminergic orchestration of motor programs in a complex C. elegans behavior. PLoS Biology, 11 (4), e1001529. doi:10.1371/journal.pbio.1001529
  • Felix, M.A., & Duveau, F. (2012). Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC Biology, 10, 59. doi:10.1186/1741-7007-10-59
  • Flavell, S.W., Pokala, N., Macosko, E.Z., Albrecht, D.R., Larsch, J., & Bargmann, C.I. (2013). Serotonin and the neuropeptide PDF initiate and extend opposing behavioral states in C. elegans. Cell, 154 (5), 1023–1035. doi:10.1016/j.cell.2013.08.001
  • Frezal, L., & Felix, M.A. (2015). C. elegans outside the Petri dish. Elife, 4, e05849. doi:10.7554/eLife.05849.
  • Golden, J.W., & Riddle, D.L. (1984). The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Developmental Biology, 102 (2), 368–378. doi:10.1016/0012-1606(84)90201-X
  • Goodman, M.B., Klein, M., Lasse, S., Luo, L., Mori, I., Samuel, A., … Wang, D. (2014). Thermotaxis navigation behavior. WormBook, ed. The C. elegans Research Community, WormBook, doi:10.1895/wormbook.1.168.1, http://www.wormbook.org.
  • Goodman, M.B., & Sengupta, P. (2019). How Caenorhabditis elegans senses mechanical stress, temperature, and other physical stimuli. Genetics, 212 (1), 25–51. doi:10.1534/genetics.118.300241
  • Gordus, A., Pokala, N., Levy, S., Flavell, S.W., & Bargmann, C.I. (2015). Feedback from network states generates variability in a probabilistic olfactory circuit. Cell, 161 (2), 215–227. doi:10.1016/j.cell.2015.02.018
  • Gramstrup Petersen, J., Rojo Romanos, T., Juozaityte, V., Redo Riveiro, A., Hums, I., Traunmuller, L., … Pocock, R. (2013). EGL-13/SoxD specifies distinct O2 and CO2 sensory neuron fates in Caenorhabditis elegans. PLoS Genetics, 9 (5), e1003511. doi:10.1371/journal.pgen.1003511
  • Gray, J.M., Hill, J.J., & Bargmann, C.I. (2005). A circuit for navigation in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 102 (9), 3184–3191. doi:10.1073/pnas.0409009101
  • Gray, J.M., Karow, D.S., Lu, H., Chang, A.J., Chang, J.S., Ellis, R.E., … Bargmann, C.I. (2004). Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature, 430 (6997), 317–322. doi:10.1038/nature02714
  • Greer, E.L., Maures, T.J., Ucar, D., Hauswirth, A.G., Mancini, E., Lim, J.P., … Brunet, A. (2011). Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature, 479 (7373), 365–371. doi:10.1038/nature10572
  • Ha, H.I., Hendricks, M., Shen, Y., Gabel, C.V., Fang-Yen, C., Qin, Y., … Zhang, Y. (2010). Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron, 68 (6), 1173–1186. doi:10.1016/j.neuron.2010.11.025
  • Hall, S.E., Beverly, M., Russ, C., Nusbaum, C., & Sengupta, P. (2010). A cellular memory of developmental history generates phenotypic diversity in C. elegans. Current Biology, 20 (2), 149–155. doi:10.1016/j.cub.2009.11.035
  • Hallem, E.A., Spencer, W.C., McWhirter, R.D., Zeller, G., Henz, S.R., Ratsch, G., … Ringstad, N. (2011). Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 108 (1), 254–259. doi:10.1073/pnas.1017354108
  • Hao, Y., Yang, W., Ren, J., Hall, Q., Zhang, Y., & Kaplan, J.M. (2018). Thioredoxin shapes the C. elegans sensory response to Pseudomonas produced nitric oxide. eLife, 7, e36833. doi:10.7554/eLife.36833
  • Harris, G., Wu, T., Linfield, G., Choi, M.K., Liu, H., & Zhang, Y. (2019). Molecular and cellular modulators for multisensory integration in C. elegans. PLoS Genetics, 15 (3), e1007706. doi:10.1371/journal.pgen.1007706
  • Hedgecock, E.M., & Russell, R.L. (1975). Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 72 (10), 4061–4065. doi:10.1073/pnas.72.10.4061
  • Hibshman, J.D., Hung, A., & Baugh, L.R. (2016). Maternal diet and insulin-like signaling control intergenerational plasticity of progeny size and starvation resistance. PLoS Genetics, 12 (10), e1006396. doi:10.1371/journal.pgen.1006396
  • Hoffman, C., & Aballay, A. (2019). Role of neurons in the control of immune defense. Current Opinion in Immunology, 60, 30–36. doi:10.1016/j.coi.2019.04.005
  • Hong H, , M., Ryu, L., Ow, M.C., Kim, J., Je, A.R., Chinta, S., … Choi, H. (2017). Early pheromone experience modifies a synaptic activity to influence adult pheromone responses of C. elegans. Current Biology, 27 (20), 3168–3177. e3163. doi:10.1016/j.cub.2017.08.068
  • Horspool, A.M., & Chang, H.C. (2017). Superoxide dismutase SOD-1 modulates C. elegans pathogen avoidance behavior. Scientific Reports, 7, 45128. doi:10.1038/srep45128
  • Iino, Y., & Yoshida, K. (2009). Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. The Journal of Neuroscience, 29 (17), 5370–5380. doi:10.1523/JNEUROSCI.3633-08.2009
  • Ikeda, M., Nakano, S., Giles, A.C., Xu, L., Costa, W.S., Gottschalk, A., & Mori, I. (2020). Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 117 (11), 6178–6188. doi:10.1073/pnas.1918528117
  • Inoue, A., Sawatari, E., Hisamoto, N., Kitazono, T., Teramoto, T., Fujiwara, M., … Ishihara, T. (2013). Forgetting in C. elegans is accelerated by neuronal communication via the TIR-1/JNK-1 pathway. Cell Reports, 3 (3), 808–819. doi:10.1016/j.celrep.2013.02.019
  • Irazoqui, J.E., Urbach, J.M., & Ausubel, F.M. (2010). Evolution of host innate defence: Insights from Caenorhabditis elegans and primitive invertebrates. Nature Reviews. Immunology, 10 (1), 47–58. doi:10.1038/nri2689
  • Jang, H., Kim, K., Neal, S.J., Macosko, E., Kim, D., Butcher, R.A., … Sengupta, P. (2012). Neuromodulatory state and sex specify alternative behaviors through antagonistic synaptic pathways in C. elegans. Neuron, 75 (4), 585–592. doi:10.1016/j.neuron.2012.06.034
  • Jeong, P.Y., Jung, M., Yim, Y.H., Kim, H., Park, M., Hong, E., … Paik, Y.K. (2005). Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature, 433 (7025), 541–545. doi:10.1038/nature03201
  • Jin, X., Pokala, N., & Bargmann, C.I. (2016). Distinct circuits for the formation and retrieval of an imprinted olfactory memory. Cell, 164 (4), 632–643. doi:10.1016/j.cell.2016.01.007
  • Juang, B.T., Gu, C., Starnes, L., Palladino, F., Goga, A., Kennedy, S., & L’Etoile, N.D. (2013). Endogenous nuclear RNAi mediates behavioral adaptation to odor. Cell, 154 (5), 1010–1022. doi:10.1016/j.cell.2013.08.006
  • Jobson, M.A., Jordan, J.M., Sandrof, M.A., Hibshman, J.D., Lennox, A.L., & Baugh, L.R. (2015). Transgenerational effects of early life starvation on growth, reproduction, and stress resistance in Caenorhabditis elegans. Genetics, 201 (1), 201–212. doi:10.1534/genetics.115.178699
  • Kaplan, H.S., Salazar Thula, O., Khoss, N., & Zimmer, M. (2020). Nested neuronal dynamics orchestrate a behavioral hierarchy across timescales. Neuron, 105 (3), 562–576. e569. doi:10.1016/j.neuron.2019.10.037
  • Kaplan, J.M., & Horvitz, H.R. (1993). A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 90 (6), 2227–2231. doi:10.1073/pnas.90.6.2227
  • Kato, S., Kaplan, H.S., Schrodel, T., Skora, S., Lindsay, T.H., Yemini, E., … Zimmer, M. (2015). Global brain dynamics embed the motor command sequence of Caenorhabditis elegans. Cell, 163 (3), 656–669. doi:10.1016/j.cell.2015.09.034
  • Kauffman, A.L., Ashraf, J.M., Corces-Zimmerman, M.R., Landis, J.N., & Murphy, C.T. (2010). Insulin signaling and dietary restriction differentially influence the decline of learning and memory with age. PLoS Biology, 8 (5), e1000372. doi:10.1371/journal.pbio.1000372
  • Kaye, J.A., Rose, N.C., Goldsworthy, B., Goga, A., & L’Etoile, N.D. (2009). A 3’UTR pumilio-binding element directs translational activation in olfactory sensory neurons. Neuron, 61 (1), 57–70. doi:10.1016/j.neuron.2008.11.012
  • Klosin, A., Casas, E., Hidalgo-Carcedo, C., Vavouri, T., & Lehner, B. (2017). Transgenerational transmission of environmental information in C. elegans. Science, 356 (6335), 320–323. doi:10.1126/science.aah6412
  • Kim, D.H., & Ewbank, J.J. (2018). Signaling in the innate immune response. WormBook: The Online Review of C. elegans Biology, 2018, 1–35. doi:10.1895/wormbook.1.83.2
  • Kim, D.H. & Flavell, S.W. (2020). Host-microbe interactions and the behavior of Caenorhabditis elegans. J Neurogenet. doi:10.1080/01677063.2020.1802724
  • Kim, K., Sato, K., Shibuya, M., Zeiger, D.M., Butcher, R.A., Ragains, J.R., … Sengupta, P. (2009). Two chemoreceptors mediate developmental effects of dauer pheromone in C. elegans. Science, 326 (5955), 994–998. doi:10.1126/science.1176331
  • Kunitomo, H., Sato, H., Iwata, R., Satoh, Y., Ohno, H., Yamada, K., & Iino, Y. (2013). Concentration memory-dependent synaptic plasticity of a taste circuit regulates salt concentration chemotaxis in Caenorhabditis elegans. Nature Communications, 4, 2210. doi:10.1038/ncomms3210
  • Lee, K., & Mylonakis, E. (2017). An intestine-derived neuropeptide controls avoidance behavior in Caenorhabditis elegans. Cell Reports, 20 (10), 2501–2512. doi:10.1016/j.celrep.2017.08.053
  • Li, Z., Liu, J., Zheng, M., & Xu, X.Z. (2014). Encoding of both analog- and digital-like behavioral outputs by one C. elegans interneuron. Cell , 159 (4), 751–765. doi:10.1016/j.cell.2014.09.056
  • Liu, A., & Urban, N.N. (2017). Prenatal and early postnatal odorant exposure heightens odor-evoked mitral cell responses in the mouse olfactory bulb. eNeuro, 4(5), ENEURO.0129-17.2017. doi:10.1523/ENEURO.0129-17.2017
  • Liu, H., Yang, W., Wu, T., Duan, F., Soucy, E., Jin, X., & Zhang, Y. (2018). Cholinergic sensorimotor integration regulates olfactory steering. Neuron, 97 (2), 390–405 e393. doi:10.1016/j.neuron.2017.12.003
  • Lorenz, K. (1935). Der kumpan in der umwelt des vogels. Journal of Ornithology, 83 (2), 137–213. doi:10.1007/BF01905355
  • Luo, L., Wen, Q., Ren, J., Hendricks, M., Gershow, M., Qin, Y., … Smith-Parker, H.K. (2014). Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit. Neuron, 82 (5), 1115–1128. doi:10.1016/j.neuron.2014.05.010
  • Ma, Y.C., Zhang, L., Dai, L.L., Khan, R.U., & Zou, C.G. (2017). mir-67 regulates P. aeruginosa avoidance behavior in C. elegans. Biochemical and Biophysical Research Communications, 494 (1–2), 120–125. doi:10.1016/j.bbrc.2017.10.069
  • 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
  • McDiarmid, T.A., Yu, A.J., & Rankin, C.H. (2019). Habituation is more than learning to ignore: Multiple Mechanisms serve to facilitate shifts in behavioral strategy. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 41 (9), e1900077 doi:10.1002/bies.201900077
  • Meisel, J.D., & Kim, D.H. (2014). Behavioral avoidance of pathogenic bacteria by Caenorhabditis elegans. Trends in Immunology, 35 (10), 465–470. doi:10.1016/j.it.2014.08.008
  • Meisel, J.D., Panda, O., Mahanti, P., Schroeder, F.C., & Kim, D.H. (2014). Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. elegans. Cell, 159 (2), 267–280. doi:10.1016/j.cell.2014.09.011
  • Miller, E.V., Grandi, L.N., Giannini, J.A., Robinson, J.D., & Powell, J.R. (2015). The conserved g-protein coupled receptor FSHR-1 regulates protective host responses to infection and oxidative stress. PLoS One, 10 (9), e0137403. doi:10.1371/journal.pone.0137403
  • Moore, R.S., Kaletsky, R., & Murphy, C.T. (2019). Piwi/PRG-1 argonaute and TGF-β mediate transgenerational learned pathogenic avoidance. Cell, 177 (7), 1827–1841 e1812. doi:10.1016/j.cell.2019.05.024
  • Mori, I., & Ohshima, Y. (1995). Neural regulation of thermotaxis in Caenorhabditis elegans. Nature, 376 (6538), 344–348. doi:10.1038/376344a0
  • Nehring, I., Kostka, T., von Kries, R., & Rehfuess, E.A. (2015). Impacts of in utero and early infant taste experiences on later taste acceptance: A systematic review. The Journal of Nutrition, 145 (6), 1271–1279. doi:10.3945/jn.114.203976
  • Nevitt, G.A., Dittman, A.H., Quinn, T.P., & Moody, W.J. Jr. (1994). Evidence for a peripheral olfactory memory in imprinted salmon. Proceedings of the National Academy of Sciences of the United States of America, 91(10), 4288–4292. doi:10.1073/pnas.91.10.4288
  • Ni, J.Z., Kalinava, N., Chen, E., Huang, A., Trinh, T., & Gu, S.G. (2016). A transgenerational role of the germline nuclear RNAi pathway in repressing heat stress-induced transcriptional activation in C. elegans. Epigenetics and Chromatin, 9(1), 1–15.
  • 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
  • Ooi, F.K., & Prahlad, V. (2017). Olfactory experience primes the heat shock transcription factor HSF-1 to enhance the expression of molecular chaperones in C. elegans. Science Signaling, 10(501), eaan4893. doi:10.1126/scisignal.aan4893
  • Ow, M.C., Borziak, K., Nichitean, A.M., Dorus, S., & Hall, S.E. (2018). Early experiences mediate distinct adult gene expression and reproductive programs in Caenorhabditis elegans. PLoS Genetics, 14 (2), e1007219. doi:10.1371/journal.pgen.1007219
  • Palominos, M.F., Verdugo, L., Gabaldon, C., Pollak, B., Ortiz-Severin, J., Varas, M.A., … Calixto, A. (2017). Transgenerational diapause as an avoidance strategy against bacterial pathogens in Caenorhabditis elegans. mBio, 8(5), e01234. doi:10.1128/mBio.01234-17
  • Pereira, A.G., Gracida, X., Kagias, K., & Zhang, Y. (2020). C. elegans aversive olfactory learning generates diverse intergenerational effects. J Neurogenet. doi: 10.1080/01677063.2020.1819265.
  • Pierce-Shimomura, J.T., Faumont, S., Gaston, M.R., Pearson, B.J., & Lockery, S.R. (2001). The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature, 410 (6829), 694–698. doi:10.1038/35070575
  • Pierce-Shimomura, J.T., Morse, T.M., & Lockery, S.R. (1999). The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. The Journal of Neuroscience, 19 (21), 9557–9569. doi:10.1523/JNEUROSCI.19-21-09557.1999
  • Posner, R., Toker, I.A., Antonova, O., Star, E., Anava, S., Azmon, E., … Rechavi, O. (2019). Neuronal small RNAs control behavior transgenerationally. Cell, 177 (7), 1814–1826 e1815. doi:10.1016/j.cell.2019.04.029
  • Pradel, E., Zhang, Y., Pujol, N., Matsuyama, T., Bargmann, C.I., & Ewbank, J.J. (2007). Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 104 (7), 2295–2300. doi:10.1073/pnas.0610281104
  • Pradhan, S., Quilez, S., Homer, K., & Hendricks, M. (2019). Environmental programming of adult foraging behavior in C. elegans. Current Biology, 29 (17), 2867–2879 e2864. doi:10.1016/j.cub.2019.07.045
  • Rankin, C.H., Beck, C.D., & Chiba, C.M. (1990). Caenorhabditis elegans: A new model system for the study of learning and memory. Behavioural Brain Research, 37 (1), 89–92. doi:10.1016/0166-4328(90)90074-O
  • Rechavi, O., Houri-Ze’evi, L., Anava, S., Goh, W.S.S., Kerk, S.Y., Hannon, G.J., & Hobert, O. (2014). Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell, 158 (2), 277–287. doi:10.1016/j.cell.2014.06.020
  • Reddy, K.C., Hunter, R.C., Bhatla, N., Newman, D.K., & Kim, D.H. (2011). Caenorhabditis elegans NPR-1-mediated behaviors are suppressed in the presence of mucoid bacteria. Proceedings of the National Academy of Sciences of the United States of America, 108 (31), 12887–12892. doi:10.1073/pnas.1108265108
  • Remy, J.J. (2010). Stable inheritance of an acquired behavior in Caenorhabditis elegans. Current Biology, 20 (20), R877–878. doi:10.1016/j.cub.2010.08.013
  • Remy, J.J., & Hobert, O. (2005). An interneuronal chemoreceptor required for olfactory imprinting in C. elegans. Science, 309 (5735), 787–790. doi:10.1126/science.1114209
  • Rhoades, J.L., Nelson, J.C., Nwabudike, I., Yu, S.K., McLachlan, I.G., Madan, G.K., … Flavell, S.W. (2019). ASICs mediate food responses in an enteric serotonergic neuron that controls foraging behaviors. Cell, 176 (1–2), 85–97 e14. doi:10.1016/j.cell.2018.11.023
  • Rose, J.K., Kaun, K.R., & Rankin, C.H. (2002). A new group-training procedure for habituation demonstrates that presynaptic glutamate release contributes to long-term memory in Caenorhabditis elegans. Learning & Memory, 9 (3), 130–137. doi:10.1101/lm.46802
  • Saeki, S., Yamamoto, M., & Iino, Y. (2001). Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. The Journal of Experimental Biology, 204 (Pt 10), 1757–1764.
  • Samuel, B.S., Rowedder, H., Braendle, C., Felix, M.A., & Ruvkun, G. (2016). Caenorhabditis elegans responses to bacteria from its natural habitats. Proceedings of the National Academy of Sciences of the United States of America, 113 (27), E3941–3949. doi:10.1073/pnas.1607183113
  • Sasakura, H., & Mori, I. (2013). Behavioral plasticity, learning, and memory in C. elegans. Current Opinion in Neurobiology, 23 (1), 92–99. doi:10.1016/j.conb.2012.09.005
  • 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.R. (2015). Mechanosensory molecules and circuits in C. elegans. Pflugers Archiv: European Journal of Physiology, 467 (1), 39–48. doi:10.1007/s00424-014-1574-3
  • Schott, D., Yanai, I., & Hunter, C.P. (2014). Natural RNA interference directs a heritable response to the environment. Scientific Reports, 4, 7387. doi:10.1038/srep07387
  • Schulenburg, H., & Felix, M.A. (2017). The natural biotic environment of Caenorhabditis elegans. Genetics, 206 (1), 55–86. doi:10.1534/genetics.116.195511
  • Singh, J., & Aballay, A. (2019). Intestinal infection regulates behavior and learning via neuroendocrine signaling. eLife, 8, e50033. doi:10.7554/eLife.50033
  • Spencer, W.A., Thompson, R.F., & Neilson, D.R. Jr. (1966). Response decrement of the flexion reflex in the acute spinal cat and transient restoration by strong stimuli. Journal of Neurophysiology, 29(2), 221–239. doi:10.1152/jn.1966.29.2.221
  • Srinivasan, J., Kaplan, F., Ajredini, R., Zachariah, C., Alborn, H.T., Teal, P.E., … Schroeder, F.C. (2008). A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature, 454 (7208), 1115–1118. doi:10.1038/nature07168
  • Srinivasan, J., von Reuss, S.H., Bose, N., Zaslaver, A., Mahanti, P., Ho, M.C., … Schroeder, F.C. (2012). A modular library of small molecule signals regulates social behaviors in Caenorhabditis elegans. PLoS Biology, 10 (1), e1001237. doi:10.1371/journal.pbio.1001237
  • Tan, M.W., Mahajan-Miklos, S., & Ausubel, F.M. (1999). Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proceedings of the National Academy of Sciences of the United States of America, 96 (2), 715–720. doi:10.1073/pnas.96.2.715
  • Tanimoto, Y., Yamazoe-Umemoto, A., Fujita, K., Kawazoe, Y., Miyanishi, Y., Yamazaki, S.J., … Nakai, J. (2017). Calcium dynamics regulating the timing of decision-making in C. elegans. eLife, 6, e21629. doi:10.7554/eLife.21629
  • Todrank, J., Heth, G., & Restrepo, D. (2011). Effects of in utero odorant exposure on neuroanatomical development of the olfactory bulb and odour preferences. Proceedings Biological Sciences, 278 (1714), 1949–1955. doi:10.1098/rspb.2010.2314
  • Tomioka, M., Adachi, T., Suzuki, H., Kunitomo, H., Schafer, W.R., & Iino, Y. (2006). The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron, 51 (5), 613–625. doi:10.1016/j.neuron.2006.07.024
  • Tran, A., Tang, A., O’Loughlin, C.T., Balistreri, A., Chang, E., Coto Villa, D., … Pyle, J., et al. (2017). C. elegans avoids toxin-producing Streptomyces using a seven transmembrane domain chemosensory receptor. eLife, 6, e23770. doi:10.7554/eLife.23770
  • Troemel, E.R., Chu, S.W., Reinke, V., Lee, S.S., Ausubel, F.M., & Kim, D.H. (2006). p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genetics, 2 (11), e183. doi:10.1371/journal.pgen.0020183
  • Tsalik, E.L., & Hobert, O. (2003). Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. Journal of Neurobiology, 56 (2), 178–197. doi:10.1002/neu.10245
  • Urrutia, A., Garcia-Angulo, V.A., Fuentes, A., Caneo, M., Legue, M., Urquiza, S., … Calixto, A. (2020). Bacterially produced metabolites protect C. elegans neurons from degeneration. PLoS Biology, 18 (3), e3000638. doi:10.1371/journal.pbio.3000638
  • Venkatachalam, V., Ji, N., Wang, X., Clark, C., Mitchell, J.K., Klein, M., … Greenwood, J. (2016). Pan-neuronal imaging in roaming Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 113 (8), E1082–E1088. doi:10.1073/pnas.1507109113
  • Wei, W., & Ruvkun, G. (2020). Lysosomal activity regulates Caenorhabditis elegans mitochondrial dynamics through vitamin B12 metabolism. Proceedings of the National Academy of Sciences of the United States of America, 117(33):19970–19981.
  • Wen, Q., Gao, S., & Zhen, M. (2018). Caenorhabditis elegans excitatory ventral cord motor neurons derive rhythm for body undulation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 373(1758):20170370. doi:10.1098/rstb.2017.0370
  • White, J.Q., & Jorgensen, E.M. (2012). Sensation in a single neuron pair represses male behavior in hermaphrodites. Neuron, 75 (4), 593–600. doi:10.1016/j.neuron.2012.03.044
  • White, J.Q., Nicholas, T.J., Gritton, J., Truong, L., Davidson, E.R., & Jorgensen, E.M. (2007). The sensory circuitry for sexual attraction in C. elegans males. Current Biology, 17 (21), 1847–1857. doi:10.1016/j.cub.2007.09.011
  • Wilson, D.A., & Sullivan, R.M. (1994). Neurobiology of associative learning in the neonate: Early olfactory learning. Behavioral and Neural Biology, 61 (1), 1–18. doi:10.1016/S0163-1047(05)80039-1
  • Wolfe, G.S., Tong, V.W., Povse, E., Merritt, D.M., Stegeman, G.W., Flibotte, S., & van der Kooy, D. (2019). A receptor tyrosine kinase plays separate roles in sensory integration and eneuro, 6(4), ENEURO.0244-18.2019. doi: 10.1523/ENEURO.0244-18.2019.
  • Zhang, Y., Lu, H., & Bargmann, C.I. (2005). Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature, 438(7065), 179–184. doi:10.1038/nature04216