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Modelling learning in Caenorhabditis elegans chemosensory and locomotive circuitry for T‐maze navigation

dc.contributor.authorSakelaris, Bennet G.
dc.contributor.authorLi, Zongyu
dc.contributor.authorSun, Jiawei
dc.contributor.authorBanerjee, Shurjo
dc.contributor.authorBooth, Victoria
dc.contributor.authorGourgou, Eleni
dc.date.accessioned2022-02-07T20:24:16Z
dc.date.available2023-02-07 15:24:12en
dc.date.available2022-02-07T20:24:16Z
dc.date.issued2022-01
dc.identifier.citationSakelaris, Bennet G.; Li, Zongyu; Sun, Jiawei; Banerjee, Shurjo; Booth, Victoria; Gourgou, Eleni (2022). "Modelling learning in Caenorhabditis elegans chemosensory and locomotive circuitry for T‐maze navigation." European Journal of Neuroscience 55(2): 354-376.
dc.identifier.issn0953-816X
dc.identifier.issn1460-9568
dc.identifier.urihttps://hdl.handle.net/2027.42/171574
dc.description.abstractRecently, a new type of Caenorhabditis elegans associative learning was reported, where nematodes learn to reach a target arm in an empty T‐maze, after they have successfully located reward (food) in the same side arm of a similar, baited, training maze. Here, we present a simplified mathematical model of C. elegans chemosensory and locomotive circuitry that replicates C. elegans navigation in a T‐maze and predicts the underlying mechanisms generating maze learning. Based on known neural circuitry, the model circuit responds to food‐released chemical cues by modulating motor neuron activity that drives simulated locomotion. We show that, through modulation of interneuron activity, such a circuit can mediate maze learning by acquiring a turning bias, even after a single training session. Simulated nematode maze navigation during training conditions in food‐baited mazes and during testing conditions in empty mazes is validated by comparing simulated behaviour with new experimental video data, extracted through the implementation of a custom‐made maze tracking algorithm. Our work provides a mathematical framework for investigating the neural mechanisms underlying this novel learning behaviour in C. elegans. Model results predict neuronal components involved in maze and spatial learning and identify target neurons and potential neural mechanisms for future experimental investigations into this learning behaviour.We present a mathematical framework and a model of C. elegans chemosensory and locomotive circuitry that replicates nematodes’ navigation and learning in a T‐maze and predicts the underlying mechanisms. We show that, through modulation of interneuron activity, such a circuit can mediate learning by acquiring a turning bias and strengthening key neuronal connections. Model results predict neuronal components involved in maze learning and identify potential targets for future experiments.
dc.publisherWiley Periodicals, Inc.
dc.publisherOxford University Press
dc.subject.othermaze navigation
dc.subject.otherC. elegans
dc.subject.otherlearning
dc.subject.otherlocomotion
dc.subject.othermathematical model
dc.subject.otherneuronal circuit dynamics
dc.titleModelling learning in Caenorhabditis elegans chemosensory and locomotive circuitry for T‐maze navigation
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelNeurosciences
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/171574/1/ejn15560_am.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/171574/2/ejn15560.pdf
dc.identifier.doi10.1111/ejn.15560
dc.identifier.sourceEuropean Journal of Neuroscience
dc.identifier.citedreferenceO’Hagan, R., Chalfie, M. & Goodman, M. B. The MEC‐4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nature Neuroscience 8, 43 – 50. http://www.nature.com/neuro/journal/v8/n1/suppinfo/nn1362_S1.html ( 2005 ).
dc.identifier.citedreferenceMorcom, A. M., Bullmore, E. T., Huppert, F. A., Lennox, B., Praseedom, A., Linnington, H., & Fletcher, P. C. ( 2010 ). Memory encoding and dopamine in the aging brain: A psychopharmacological neuroimaging study. Cerebral Cortex, 20, 743 – 757. https://doi.org/10.1093/cercor/bhp139
dc.identifier.citedreferenceNair, S. S., Paré, D., & Vicentic, A. ( 2016 ). Biologically based neural circuit modelling for the study of fear learning and extinction. npj Science of Learning, 1, 16015. https://doi.org/10.1038/npjscilearn.2016.15
dc.identifier.citedreferencePierce‐Shimomura, J. T., Morse, T. M., & Lockery, S. R. ( 1999 ). The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. The Journal of Neuroscience, 19, 9557 – 9569. https://doi.org/10.1523/jneurosci.19-21-09557.1999
dc.identifier.citedreferenceQin, J., & Wheeler, A. R. ( 2007 ). Maze exploration and learning in C. elegans. Lab on a Chip, 7, 186 – 192. https://doi.org/10.1039/b613414a
dc.identifier.citedreferenceRankin, C. H., Beck, C. D. O., & Chiba, C. M. ( 1990 ). Caenorhabditis elegans: A new model system for the study of learning and memory. Behavioural Brain Research, 37, 89 – 92. https://doi.org/10.1016/0166-4328(90)90074-O
dc.identifier.citedreferenceRankin, C. H., & Broster, B. S. ( 1992 ). Factors affecting habituation and recovery from habituation in the nematode Caenorhabditis elegans. Behavioral Neuroscience, 106, 239 – 249. https://doi.org/10.1037/0735-7044.106.2.239
dc.identifier.citedreferenceRoberts, W. M., Augustine, R., Lawton, K., Lindsay, T., Thiele, T., Izquierdo, E., Faumont, S., Lindsay, R., Britton, M., Pokala, N., Bargmann, C., & Lockery, E. ( 2016 ). A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans. eLife, 5, 125 – 172. https://doi.org/10.7554/eLife.12572
dc.identifier.citedreferenceSanyal, S., Wintle, R. F., Kindt, K. S., Nuttley, W. M., Arvan, R., Fitzmaurice, P., Bigras, E., Merz, D. C., Hébert, T. E., van der Kooy, D., Schafer, W. R., Culotti, J. G., & van Tol, H. H. M. ( 2004 ). Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. The EMBO Journal, 23, 473 – 482. https://doi.org/10.1038/sj.emboj.7600057
dc.identifier.citedreferenceSawin, E. R., Ranganathan, R., & Horvitz, H. R. C. ( 2000 ). Elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron, 26, 619 – 631. https://doi.org/10.1016/S0896-6273(00)81199-X
dc.identifier.citedreferenceScholz, M., Dinner, A. R., Levine, E., & Biron, D. ( 2017 ). Stochastic feeding dynamics arise from the need for information and energy. Proceedings of the National Academy of Sciences, 114, 9261 – 9266. https://doi.org/10.1073/pnas.1703958114
dc.identifier.citedreferenceSchultz, W. ( 2007 ). Behavioral dopamine signals. Trends in Neurosciences, 30, 203 – 210. https://doi.org/10.1016/j.tins.2007.03.007
dc.identifier.citedreferenceSchwarz, J., & Bringmann, H. ( 2017 ). Analysis of the NK2 homeobox gene ceh‐24 reveals sublateral motor neuron control of left‐right turning during sleep. eLife. 6, e24846. https://doi.org/10.7554/eLife.24846
dc.identifier.citedreferenceSegovia, G., Porras, A., del Arco, A., & Mora, F. ( 2001 ). Glutamatergic neurotransmission in aging: A critical perspective. Mechanisms of Ageing and Development, 122, 1 – 29. https://doi.org/10.1016/s0047-6374(00)00225-6
dc.identifier.citedreferenceSengupta, P., & Samuel, A. D. T. C. ( 2009 ). Elegans: A model system for systems neuroscience. Current Opinion in Neurobiology, 19, 637 – 643. https://doi.org/10.1016/j.conb.2009.09.009
dc.identifier.citedreferenceSingh, R. N., & Sulston, J. E. ( 1978 ). Some observations on moulting in Caenorhabditis Elegans. Nematologica, 24, 63 – 71. https://doi.org/10.1163/187529278X00074
dc.identifier.citedreferenceSoh, Z., Sakamoto, K., Suzuki, M., Iino, Y., & Tsuji, T. ( 2018 ). A computational model of internal representations of chemical gradients in environments for chemotaxis of Caenorhabditis elegans. Scientific Reports, 8, 17190. https://doi.org/10.1038/s41598-018-35157-1
dc.identifier.citedreferenceSulston, J., Dew, M., & Brenner, S. ( 1975 ). Dopaminergic neurons in the nematode Caenorhabditis elegans. Journal of Comparative Neurology, 163, 215 – 226. https://doi.org/10.1002/cne.901630207
dc.identifier.citedreferenceSuzuki, H., Thiele, T. R., Faumont, S., Ezcurra, M., Lockery, S. R., & Schafer, W. R. ( 2008 ). Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature, 454, 114 – 117. https://doi.org/10.1038/nature06927
dc.identifier.citedreferenceTanimoto, Y., et al. ( 2017 ). Calcium dynamics regulating the timing of decision‐making in C. elegans. eLife, 6, e21629. https://doi.org/10.7554/eLife.21629
dc.identifier.citedreferenceThiele, T. R., Faumont, S., & Lockery, S. R. ( 2009 ). The neural network for chemotaxis to Tastants in Caenorhabditis elegans is specialized for temporal differentiation. The Journal of Neuroscience, 29, 11904 – 11911. https://doi.org/10.1523/jneurosci.0594-09.2009
dc.identifier.citedreferenceTowlson, E. K., Vértes, P. E., Ahnert, S. E., Schafer, W. R., & Bullmore, E. T. ( 2013 ). The Rich Club of the C. elegans neuronal connectome. The Journal of Neuroscience, 33, 6380 – 6387. https://doi.org/10.1523/JNEUROSCI.3784-12.2013
dc.identifier.citedreferenceVarshney, L. R., Chen, B. L., Paniagua, E., Hall, D. H., & Chklovskii, D. B. ( 2011 ). Structural properties of the Caenorhabditis elegans neuronal network. PLoS Computational Biology, 7, e1001066. https://doi.org/10.1371/journal.pcbi.1001066
dc.identifier.citedreferenceWei, H., Dai, D., & Bu, Y. ( 2017 ). A plausible neural circuit for decision making and its formation based on reinforcement learning. Cognitive Neurodynamics, 11, 259 – 281. https://doi.org/10.1007/s11571-017-9426-4
dc.identifier.citedreferenceWhite, J. G., Southgate, E., Thomson, J. N., & Brenner, S. ( 1986 ). The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical transactions of the Royal Society of London. B, Biological Sciences, 314, 1 – 340. https://doi.org/10.1098/rstb.1986.0056
dc.identifier.citedreferenceWintle, R. F., & van Tol, H. H. M. ( 2001 ). Dopamine signaling in Caenorhabditis elegans —Potential for parkinsonism research. Parkinsonism & Related Disorders, 7, 177 – 183. https://doi.org/10.1016/S1353-8020(00)00055-9
dc.identifier.citedreferenceWise, R. A. ( 2004 ). Dopamine, learning and motivation. Nature Reviews. Neuroscience, 5, 483 – 494. https://doi.org/10.1038/nrn1406
dc.identifier.citedreferenceYeon, J., Kim, J., Kim, D.‐Y., Kim, H., Kim, J., Du, E. J., Kang, K. J., Lim, H.‐H., Moon, D., & Kim, K. ( 2018 ). A sensory‐motor neuron type mediates proprioceptive coordination of steering in C. elegans via two TRPC channels. PLoS Biology, 16, e2004929. https://doi.org/10.1371/journal.pbio.2004929
dc.identifier.citedreferenceArdiel, E. L., & Rankin, C. H. ( 2010 ). An elegant mind: Learning and memory in Caenorhabditis elegans. Learning & Memory, 17, 191 – 201. https://doi.org/10.1101/lm.960510
dc.identifier.citedreferenceArey, R. N., Stein, G. M., Kaletsky, R., Kauffman, A., & Murphy, C. T. ( 2018 ). Activation of Gαq signaling enhances memory consolidation and slows cognitive decline. Neuron, 98, 562 – 574.e5. https://doi.org/10.1016/j.neuron.2018.03.039
dc.identifier.citedreferenceArias‐Carrión, O., Stamelou, M., Murillo‐Rodríguez, E., Menéndez‐González, M., & Pöppel, E. ( 2010 ). Dopaminergic reward system: A short integrative review. International Archives of Medicine, 3, 24 – 24. https://doi.org/10.1186/1755-7682-3-24
dc.identifier.citedreferenceArnatkeviciute, A., Fulcher, B. D., Pocock, R., & Fornito, A. ( 2018 ). Hub connectivity, neuronal diversity, and gene expression in the Caenorhabditis elegans connectome. PLOS Computational Biology, 14 ( 2 ). https://doi.org/10.1371/journal.pcbi.1005989
dc.identifier.citedreferenceBackman, L., Nyberg, L., Lindenberger, U., Li, S. C., & Farde, L. ( 2006 ). The correlative triad among aging, dopamine, and cognition: Current status and future prospects. Neuroscience and Biobehavioral Reviews, 30, 791 – 807. https://doi.org/10.1016/j.neubiorev.2006.06.005
dc.identifier.citedreferenceBargmann, C. I. ( 2006 ). Chemosensation in C. elegans. In The C. elegans Research Community (Ed.), WormBook: the Online Review of C. elegans Biology (pp. 1 – 29 ). https://doi.org/10.1895/wormbook.1.123.1
dc.identifier.citedreferenceBranch, S. Y., Sharma, R., & Beckstead, M. J. ( 2014 ). Aging decreases L‐type calcium channel currents and pacemaker firing fidelity in substantia Nigra dopamine neurons. The Journal of Neuroscience, 34, 9310 – 9318. https://doi.org/10.1523/jneurosci.4228-13.2014
dc.identifier.citedreferenceCai, S. Q., & Sesti, F. ( 2009 ). Oxidation of a potassium channel causes progressive sensory function loss during aging. Nature Neuroscience, 12, 611 – 617. https://doi.org/10.1038/nn.2291
dc.identifier.citedreferenceCalhoun, A. J., Chalasani, S. H., & Sharpee, T. O. ( 2014 ). Maximally informative foraging by Caenorhabditis elegans. eLife, 3, e04220. https://doi.org/10.7554/eLife.04220
dc.identifier.citedreferenceChan, T. F., & Vese, L. A. ( 2001 ). Active contours without edges. IEEE Transactions on Image Processing, 10, 266 – 277. https://doi.org/10.1109/83.902291
dc.identifier.citedreferenceCohen, N., & Sanders, T. ( 2014 ). Nematode locomotion: Dissecting the neuronal‐environmental loop. Current Opinion in Neurobiology, 25, 99 – 106. https://doi.org/10.1016/j.conb.2013.12.003
dc.identifier.citedreferenceCompte, A., Brunel, N., Goldman‐Rakic, P. S., & Wang, X.‐J. ( 2000 ). Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cerebral Cortex, 10, 910 – 923. https://doi.org/10.1093/cercor/10.9.910
dc.identifier.citedreferenceConstantinidis, C., & Klingberg, T. ( 2016 ). The neuroscience of working memory capacity and training. Nature Reviews. Neuroscience, 17, 438 – 449. https://doi.org/10.1038/nrn.2016.43
dc.identifier.citedreferenceCook, S. J., Jarrell, T. A., Brittin, C. A., Wang, Y., Bloniarz, A. E., Yakovlev, M. A., Nguyen, K. C. Q., Tang, L. T. H., Bayer, E. A., Duerr, J. S., Bülow, H. E., Hobert, O., Hall, D. H., & Emmons, S. W. ( 2019 ). Whole‐animal connectomes of both Caenorhabditis elegans sexes. Nature, 571, 63 – 71. https://doi.org/10.1038/s41586-019-1352-7
dc.identifier.citedreferenceDemin, A. V., & Vityaev, E. E. ( 2014 ). Learning in a virtual model of the C. elegans nematode for locomotion and chemotaxis. Biologically Inspired Cognitive Architectures, 7, 9 – 14. https://doi.org/10.1016/j.bica.2013.11.005
dc.identifier.citedreferenceDusenbery, D. B. ( 1974 ). Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation. The Journal of Experimental Zoology, 188, 41 – 47. https://doi.org/10.1002/jez.1401880105
dc.identifier.citedreferenceDusenbery, D. B. ( 1980 ). Responses of the nematode Caenorhabditis elegans to controlled chemical stimulation. Journal of Comparative Physiology, 136, 327 – 331. https://doi.org/10.1007/bf00657352
dc.identifier.citedreferenceFaumont, S., Lindsay, T. H., & Lockery, S. R. ( 2012 ). Neuronal microcircuits for decision making in C. elegans. Current Opinion in Neurobiology, 22, 580 – 591. https://doi.org/10.1016/j.conb.2012.05.005
dc.identifier.citedreferenceGarst‐Orozco, J., Babadi, B., & Ölveczky, B. P. ( 2014 ). A neural circuit mechanism for regulating vocal variability during song learning in zebra finches. eLife, 3, e03697. https://doi.org/10.7554/eLife.03697
dc.identifier.citedreferenceGeffeney, S. L., Cueva, J. G., Glauser, D. A., Doll, J. C., Lee, T. H.‐C., Montoya, M., Karania, S., Garakani, A. M., Pruitt, B. L., & Goodman, M. B. ( 2011 ). DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron, 71, 845 – 857. https://doi.org/10.1016/j.neuron.2011.06.038
dc.identifier.citedreferenceGhosh, D. D., Sanders, T., Hong, S., McCurdy, L. Y., Chase, D. L., Cohen, N., Koelle, M. R., & Nitabach, M. N. ( 2016 ). Neural architecture of hunger‐dependent multisensory decision making in C. elegans. Neuron, 92, 1049 – 1062. https://doi.org/10.1016/j.neuron.2016.10.030
dc.identifier.citedreferenceGoldman‐Rakic, P. S. ( 1995 ). Cellular basis of working memory. Neuron, 14, 477 – 485. https://doi.org/10.1016/0896-6273(95)90304-6
dc.identifier.citedreferenceGoodman, M. B., Hall, D. H., Avery, L., & Lockery, S. R. ( 1998 ). Active currents regulate sensitivity and dynamic range in C. elegans neurons. Neuron, 20, 763 – 772. https://doi.org/10.1016/S0896-6273(00)81014-4
dc.identifier.citedreferenceGourgou, E., Adiga, K., Goettemoeller, A., Chen, C., & Hsu, A.‐L. ( 2021 ). Caenorhabditis elegans learning and decision‐making in a structured environment is a multisensory behavior. iScience, 24 ( 4 ), 102284. https://doi.org/10.1016/j.isci.2021.102284
dc.identifier.citedreferenceGower, J. C., & Dijksterhuis, G. B. ( 2004 ). Procrustes Problems (Vol. 30, p. 248 ). Oxford University Press.
dc.identifier.citedreferenceHan, B., Dong, Y., Zhang, L., Liu, Y., Rabinowitch, I., & Bai, J. ( 2017 ). Dopamine signaling tunes spatial pattern selectivity in C. elegans. eLife, 6, e22896. https://doi.org/10.7554/eLife.22896
dc.identifier.citedreferenceHart, A. C. C. WormBook: The Online Review of C. elegans Biology (ed V. Ambros ) ( The C. elegans Research Community, 2006 ).
dc.identifier.citedreferenceHasani, R. M., Fuchs, M., Beneder, V., & Grosu, R. ( 2017 ). Non‐associative learning representation in the nervous system of the nematode Caenorhabditis elegans. arXiv e‐print, 1703, 06264.
dc.identifier.citedreferenceHills, T., Brockie, P. J., & Maricq, A. V. ( 2004 ). Dopamine and glutamate control area‐restricted search behavior in Caenorhabditis elegans. The Journal of Neuroscience, 24, 1217 – 1225. https://doi.org/10.1523/jneurosci.1569-03.2004
dc.identifier.citedreferenceIino, Y., & Yoshida, K. ( 2009 ). Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. The Journal of neuroscience: the official journal of the Society for Neuroscience, 29, 5370 – 5380. https://doi.org/10.1523/JNEUROSCI.3633-08.2009
dc.identifier.citedreferenceIn C. elegans II (eds D. L. Riddle, T. Blumenthal, B. J. Meyer, & J. R. Priess) (Cold Spring Harbor Laboratory Press, 1997 ).
dc.identifier.citedreferenceIzquierdo, E. J., & Beer, R. D. ( 2016 ). The whole worm: Brain‐body‐environment models of C. elegans. Current Opinion in Neurobiology, 40, 23 – 30. https://doi.org/10.1016/j.conb.2016.06.005
dc.identifier.citedreferenceIzquierdo, E. J., & Lockery, S. R. ( 2010 ). Evolution and analysis of minimal neural circuits for Klinotaxis in Caenorhabditis elegans. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30, 12908 – 12917. https://doi.org/10.1523/JNEUROSCI.2606-10.2010
dc.identifier.citedreferenceJarrell, T. A., Wang, Y., Bloniarz, A. E., Brittin, C. A., Xu, M., Thomson, J. N., Albertson, D. G., Hall, D. H., & Emmons, S. W. ( 2012 ). The connectome of a decision‐making neural network. Science, 337, 437 – 444. https://doi.org/10.1126/science.1221762
dc.identifier.citedreferenceKaplan, 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, 2227 – 2231. https://doi.org/10.1073/pnas.90.6.2227
dc.identifier.citedreferenceKarbowski, J. ( 2019 ). Deciphering neural circuits for Caenorhabditis elegans behavior by computations and perturbations to genome and connectome. Current Opinion in Systems Biology, 13, 44 – 51. https://doi.org/10.1016/j.coisb.2018.09.008
dc.identifier.citedreferenceKato, S., Xu, Y., Cho, C. E., Abbott, L. F., & Bargmann, C. I. ( 2014 ). Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics. Neuron, 81, 616 – 628. https://doi.org/10.1016/j.neuron.2013.11.020
dc.identifier.citedreferenceKausler, B. ( 1994 ). Learning and Memory in Normal Aging. Academic Press.
dc.identifier.citedreferenceKindt, K. S., Quast, K. B., Giles, A. C., de, S., Hendrey, D., Nicastro, I., Rankin, C. H., & Schafer, W. R. ( 2007 ). Dopamine mediates context‐dependent modulation of sensory plasticity in C. elegans. Neuron, 55, 662 – 676. https://doi.org/10.1016/j.neuron.2007.07.023
dc.identifier.citedreferenceKlein, M., et al. ( 2017 ). Exploratory search during directed navigation in C. elegans and Drosophila larva. eLife, 6, e30503. https://doi.org/10.7554/eLife.30503
dc.identifier.citedreferenceKlingberg, T. ( 2010 ). Training and plasticity of working memory. Trends in Cognitive Sciences, 14, 317 – 324. https://doi.org/10.1016/j.tics.2010.05.002
dc.identifier.citedreferenceLarsch, J., Ventimiglia, D., Bargmann, C. I., & Albrecht, D. R. ( 2013 ). High‐throughput imaging of neuronal activity in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 110, E4266 – E4273. https://doi.org/10.1073/pnas.1318325110
dc.identifier.citedreferenceLeinwand, S. G., Yang, C. J., Bazopoulou, D., Chronis, N., Srinivasan, J., & Chalasani, S. H. ( 2015 ). Circuit mechanisms encoding odors and driving aging‐associated behavioral declines in Caenorhabditis elegans. eLife, 4, e10181. https://doi.org/10.7554/eLife.10181
dc.identifier.citedreferenceLeung, N. T., Tam, H. M., Chu, L. W., Kwok, T. C., Chan, F., Lam, L. C., Woo, J., & Lee, T. M. ( 2015 ). Neural plastic effects of cognitive training on aging brain. Neural Plasticity, 2015, 535618. https://doi.org/10.1155/2015/535618
dc.identifier.citedreferenceLi, W., Feng, Z., Sternberg, P. W., & Xu, X. Z. A. C. ( 2006 ). Elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature, 440, 684 – 687. https://doi.org/10.1038/nature04538
dc.identifier.citedreferenceLindsay, T. H., Thiele, T. R., & Lockery, S. R. ( 2011 ). Optogenetic analysis of synaptic transmission in the central nervous system of the nematode Caenorhabditis elegans. Nature Communications, 2, 306. https://doi.org/10.1038/ncomms1304
dc.identifier.citedreferenceLippa, A. S., Critchett, D. J., Ehlert, F., Yamamura, H. I., Enna, S. J., & Bartus, R. T. ( 1981 ). Age‐related alterations in neurotransmitter receptors: An electrophysiological and biochemical analysis. Neurobiology of Aging, 2, 3 – 8. https://doi.org/10.1016/0197-4580(81)90052-X
dc.identifier.citedreferenceLiu, P., Ge, Q., Chen, B., Salkoff, L., Kotlikoff, M. I., & Wang, Z. W. ( 2011 ). Genetic dissection of ion currents underlying all‐or‐none action potentials in C. elegans body‐wall muscle cells. The Journal of Physiology, 589, 101 – 117. https://doi.org/10.1113/jphysiol.2010.200683
dc.identifier.citedreferenceLiu, Q., Hollopeter, G., & Jorgensen, E. M. ( 2009 ). Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proceedings of the National Academy of Sciences of the United States of America, 106, 10823 – 10828. https://doi.org/10.1073/pnas.0903570106
dc.identifier.citedreferenceLiu, Q., Kidd, P. B., Dobosiewicz, M. & Bargmann, C. I. C. Elegans AWA olfactory neurons fire calcium‐mediated all‐or‐none action potentials. Cell 175, 57 – 70.e17, https://doi.org/10.1016/j.cell.2018.08.018 ( 2018 ).
dc.identifier.citedreferenceMaass, W., Joshi, P., & Sontag, E. D. ( 2007 ). Computational aspects of feedback in neural circuits. PLoS Computational Biology, 3, e165. https://doi.org/10.1371/journal.pcbi.0020165
dc.identifier.citedreferenceMarder, E. ( 1984 ). Mechanisms underlying neurotransmitter modulation of a neuronal circuit. Trends in Neurosciences, 7, 48 – 53. https://doi.org/10.1016/S0166-2236(84)80277-5
dc.identifier.citedreferenceMarder, E. ( 2012 ). Neuromodulation of neuronal circuits: Back to the future. Neuron, 76, 1 – 11. https://doi.org/10.1016/j.neuron.2012.09.010
dc.identifier.citedreferenceMattay, V. S., Fera, F., Tessitore, A., Hariri, A. R., Berman, K. F., Das, S., Meyer‐Lindenberg, A., Goldberg, T. E., Callicott, J. H., & Weinberger, D. R. ( 2006 ). Neurophysiological correlates of age‐related changes in working memory capacity. Neuroscience Letters, 392, 32 – 37. https://doi.org/10.1016/j.neulet.2005.09.025
dc.identifier.citedreferenceMellem, J. E., Brockie, P. J., Madsen, D. M., & Maricq, A. V. ( 2008 ). Action potentials contribute to neuronal signaling in C. elegans. Nature Neuroscience, 11, 865 – 867. https://doi.org/10.1038/nn.2131
dc.identifier.citedreferenceMirzakhalili, E., Epureanu, B. I., & Gourgou, E. ( 2018 ). A mathematical and computational model of the calcium dynamics in Caenorhabditis elegans ASH sensory neuron. PLoS ONE, 13, e0201302. https://doi.org/10.1371/journal.pone.0201302
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