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A navigational system for investigating multi-sensory integration in Caenorhabditis elegans

  • 1.

    Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230027, China

  • 2.

    Department of Physics, Nanjing University, Nanjing 210093, China

Cite this:
https://doi.org/10.52396/JUST-2021-0096
  • Received Date: 02 April 2021
  • Rev Recd Date: 25 May 2021
  • Publish Date: 31 May 2021
    Abstract

  • Abstract

    Animals use different sensory cues to guide their behaviors. How a nervous system performs multi-sensory integration remains an open question in neuroscience. Here, we study how the nematode Caenorhabditis elegans integrates temperature and salt stimuli, two environmental cues that are essential for survival. We report the development of a navigational system that allows stable, linear, and orthogonal temperature gradient and salt gradient to be simultaneously presented to an animal. By combining this setup with a tracking and calcium imaging system, we analyze the behavioral strategies of C. elegans and investigate the functions of two cilia sensory neurons—AFD and ASER—that attend the behavior. Our work opens a new window into interrogating the neural mechanisms for multi-sensory integration in a compact nervous system.

    Abstract

    Animals use different sensory cues to guide their behaviors. How a nervous system performs multi-sensory integration remains an open question in neuroscience. Here, we study how the nematode Caenorhabditis elegans integrates temperature and salt stimuli, two environmental cues that are essential for survival. We report the development of a navigational system that allows stable, linear, and orthogonal temperature gradient and salt gradient to be simultaneously presented to an animal. By combining this setup with a tracking and calcium imaging system, we analyze the behavioral strategies of C. elegans and investigate the functions of two cilia sensory neurons—AFD and ASER—that attend the behavior. Our work opens a new window into interrogating the neural mechanisms for multi-sensory integration in a compact nervous system.
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    • References(49)
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    Meredith M A, Stein B E. Interactions among converging sensory inputs in the superior colliculus.Science, 1983, 221(4608): 389-391.
    [2]
    Meredith M A, Stein B E. Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration.Journal of Neurophysiology, 1986, 56(3): 640-662.
    [3]
    Meredith M,Nemitz J, Stein B. Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors. The Journal of Neuroscience, 1987, 7(10): 3215-3229.
    [4]
    Miller E K, Cohen J D. An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 2001, 24(1): 167-202.
    [5]
    Aizenman C D, Felch D L, Khakhalin A S. Multisensory integration in the developing tectum is constrained by the balance of excitation and inhibition. eLife, 2016, 5: e15600.
    [6]
    Meredith M A, Stein B E. Spatial determinants of multisensory integration in cat superior colliculus neurons.Journal of Neurophysiology, 1996, 75(5): 1843-1857.
    [7]
    Stevenson R A, James T W. Audiovisual integration in human superior temporal sulcus: Inverse effectiveness and the neural processing of speech and object recognition. NeuroImage, 2009, 44(3): 1210-1223.
    [8]
    Senkowski D, Saint-Amour D, Höfle M, et al. Multisensory interactions in early evoked brain activity follow the principle of inverse effectiveness. NeuroImage, 2011, 56(4): 2200-2208.
    [9]
    Cuppini C, Magosso E, Rowland B, et al. Hebbian mechanisms help explain development of multisensory integration in the superior colliculus: A neural network model. Biological Cybernetics, 2012, 106(11/12): 691-713.
    [10]
    Truszkowski T L, Carrillo O A, Bleier J, et al. A cellular mechanism for inverse effectiveness in multisensory integration. eLife, 2017, 6: e25392.
    [11]
    Joiner M L A, Griffith L C. Visual input regulates circuit configuration in courtship conditioning of Drosophila melanogaster. Learning and Memory, 2000, 7(1): 32-42.
    [12]
    Kinoshita M, Stewart F J,Omura H. Multisensory integration in Lepidoptera: Insights into flower-visitor interactions. BioEssays, 2017, 39(4): 93-98.
    [13]
    Makoto S, Hiroto O. Multisensory enhancement of burst activity in an insect auditory neuron. Journal of Neurophysiology, 2018, 120(1): 139-148.
    [14]
    White J G, Southgate E, Thomson J N, et al. The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society B: Biological Sciences, 1986, 314(1165): 1-340.
    [15]
    Troemel E R, Chou J H, Dwyer N D, et al. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell, 1995, 83(2): 207-218.
    [16]
    Bargmann C I, Horvitz H R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron, 1991, 7(5): 729-742.
    [17]
    Luo L, Wen Q, Ren J, et al. Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit. Neuron, 2014, 82(5): 1115-1128.
    [18]
    Hedgecock E M, Russell R L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 1975, 72(10): 4061-4065.
    [19]
    Hawk J D, Calvo A C, Liu P, et al. Integration of plasticity mechanisms within a single sensory neuron of C. elegans actuates a memory. Neuron, 2018, 97(2): 356-367.
    [20]
    Chalfie M, Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Developmental Biology, 1981, 82(2): 358-370.
    [21]
    Ward A, Liu J, Feng Z, et al. Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nature Neuroscience, 2008, 11(8): 916-922.
    [22]
    Bargmann C I. Genetic and cellular analysis of behavior in C. elegans. Annual Review of Neuroscience, 1993, 16(1): 47-71.
    [23]
    Mori I, OhshimaY. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature, 1995, 376: 344-348.
    [24]
    Bargmann C I, Kaplan J M. Signal transduction in the Caenorhabditis elegans nervous system. Annual Review of Neuroscience, 1998, 21(1): 279-308.
    [25]
    Allee W C. The orientation of animals. Ecology, 1941, 22(3): 350-350.
    [26]
    Pierce-Shimomura J T, Morse T M, Lockery S R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. Journal of Neuroscience, 1999, 19(21): 9557-9569.
    [27]
    Pierce-Shimomura J T, Dores M, Lockery S R. Analysis of the effects of turning bias on chemotaxis in C. elegans. Journal of Experimental Biology, 2005, 208(24):4727-4733.
    [28]
    Luo L, Cook N, Venkatachalam V, et al. Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(7): 2776-2781.
    [29]
    Jansen G, Weinkove D, Plasterk R H A. The G-protein γ subunit gpc-1 of the nematode C.elegans is involved in taste adaptation. The EMBO Journal, 2002, 21(5): 986-994.
    [30]
    Ikeda M, Nakano S, Giles A C, et al. Context-dependent operation of neural circuits under-lies a navigation behavior in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(11): 6178-6188.
    [31]
    Iino Y, Yoshida K. Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. Journal of Neuroscience, 2009, 29(17): 5370-5380.
    [32]
    Ryu W S, Samuel A. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined thermal stimuli. The Journal of Neuroscience, 2002, 22(13): 5727-5733.
    [33]
    Clark D A, Gabel C V, Lee T M, et al. Short-term adaptation and temporal processing in the cryophilic response of Caenorhabditis elegans. Journal of Neurophysiology, 2006, 97(3): 1903-1910.
    [34]
    Leifer A M, Fang-Yen C, Gershow M, et al. Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nature Methods, 2011, 8(2): 147-152.
    [35]
    Kunitomo H, Sato H, Iwata R, et al. Concentration memory-dependent synaptic plasticity of a taste circuit regulates salt concentration chemotaxis in Caenorhabditis elegans. Nature Communications, 2013, 4: 2210.
    [36]
    Gong J, Liu J, Ronan E A, et al. A Cold-sensing receptor encoded by a glutamate receptor gene. Cell, 2019, 178(6): 1375-1386.e11.
    [37]
    Clark D A, Biron D, Sengupta P, et al. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. Journal of Neuroscience, 2006, 26(28): 7444-7451.
    [38]
    Clark D A, Gabel C V, Gabel H, et al. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. Journal of Neuroscience, 2007, 27(23): 6083-6090.
    [39]
    Tomioka M, Adachi T, Suzuki H, et al. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron, 2006, 51(5): 613-625.
    [40]
    Suzuki H, Thiele T R, Faumont S, et al. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature, 2008, 454: 114-117.
    [41]
    Thiele T R, Fa Umont S, Lockery S R. The neural network for chemotaxis to tastants in Caenorhabditis elegans is specialized for temporal differentiation. Journal of Neuroscience, 2009, 29(38): 11904-11911.
    [42]
    Kimata T, Sasakura H, Ohnishi N, et al. Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity. Worm, 2012, 1(1): 31-41.
    [43]
    Dusenbery D B, Sheridan R E, Russell R L. Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. Genetics, 1975, 80(2): 297-309.
    [44]
    Komatsu H, Mori I, Rhee J S, et al. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron, 1996, 17(4): 707-718.
    [45]
    Li Z, Liu J, Zheng M, et al. Encoding of both analog- and digital-like behavioral outputs by one C. elegans interneuron. Cell, 2014, 159(4): 751-765.
    [46]
    Wang Y, Zhang X, Xin Q, et al. Flexible motor sequence generation during stereotyped escape responses. Elife, 2020, 9: e56942.
    [47]
    Kato S, Kaplan H S, Schrödel T, et al. Global brain dynamics embed the motor command sequence of Caenorhabditis elegans. Cell, 2015, 163(3): 656-669.
    [48]
    Stringer C, Pachitariu M, Steinmetz N, et al. Spontaneous behaviors drive multidimensional, brainwide activity. Science, 2019, 364(6437): 255.
    [49]
    Rumyantsev O I, Lecoq J A, Hernandez O, et al. Fundamental bounds on the fidelity of sensory cortical coding. Nature, 2020, 580(7801): 100-105.
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    [1]
    Meredith M A, Stein B E. Interactions among converging sensory inputs in the superior colliculus.Science, 1983, 221(4608): 389-391.
    [2]
    Meredith M A, Stein B E. Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration.Journal of Neurophysiology, 1986, 56(3): 640-662.
    [3]
    Meredith M,Nemitz J, Stein B. Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors. The Journal of Neuroscience, 1987, 7(10): 3215-3229.
    [4]
    Miller E K, Cohen J D. An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 2001, 24(1): 167-202.
    [5]
    Aizenman C D, Felch D L, Khakhalin A S. Multisensory integration in the developing tectum is constrained by the balance of excitation and inhibition. eLife, 2016, 5: e15600.
    [6]
    Meredith M A, Stein B E. Spatial determinants of multisensory integration in cat superior colliculus neurons.Journal of Neurophysiology, 1996, 75(5): 1843-1857.
    [7]
    Stevenson R A, James T W. Audiovisual integration in human superior temporal sulcus: Inverse effectiveness and the neural processing of speech and object recognition. NeuroImage, 2009, 44(3): 1210-1223.
    [8]
    Senkowski D, Saint-Amour D, Höfle M, et al. Multisensory interactions in early evoked brain activity follow the principle of inverse effectiveness. NeuroImage, 2011, 56(4): 2200-2208.
    [9]
    Cuppini C, Magosso E, Rowland B, et al. Hebbian mechanisms help explain development of multisensory integration in the superior colliculus: A neural network model. Biological Cybernetics, 2012, 106(11/12): 691-713.
    [10]
    Truszkowski T L, Carrillo O A, Bleier J, et al. A cellular mechanism for inverse effectiveness in multisensory integration. eLife, 2017, 6: e25392.
    [11]
    Joiner M L A, Griffith L C. Visual input regulates circuit configuration in courtship conditioning of Drosophila melanogaster. Learning and Memory, 2000, 7(1): 32-42.
    [12]
    Kinoshita M, Stewart F J,Omura H. Multisensory integration in Lepidoptera: Insights into flower-visitor interactions. BioEssays, 2017, 39(4): 93-98.
    [13]
    Makoto S, Hiroto O. Multisensory enhancement of burst activity in an insect auditory neuron. Journal of Neurophysiology, 2018, 120(1): 139-148.
    [14]
    White J G, Southgate E, Thomson J N, et al. The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society B: Biological Sciences, 1986, 314(1165): 1-340.
    [15]
    Troemel E R, Chou J H, Dwyer N D, et al. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell, 1995, 83(2): 207-218.
    [16]
    Bargmann C I, Horvitz H R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron, 1991, 7(5): 729-742.
    [17]
    Luo L, Wen Q, Ren J, et al. Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit. Neuron, 2014, 82(5): 1115-1128.
    [18]
    Hedgecock E M, Russell R L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 1975, 72(10): 4061-4065.
    [19]
    Hawk J D, Calvo A C, Liu P, et al. Integration of plasticity mechanisms within a single sensory neuron of C. elegans actuates a memory. Neuron, 2018, 97(2): 356-367.
    [20]
    Chalfie M, Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Developmental Biology, 1981, 82(2): 358-370.
    [21]
    Ward A, Liu J, Feng Z, et al. Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nature Neuroscience, 2008, 11(8): 916-922.
    [22]
    Bargmann C I. Genetic and cellular analysis of behavior in C. elegans. Annual Review of Neuroscience, 1993, 16(1): 47-71.
    [23]
    Mori I, OhshimaY. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature, 1995, 376: 344-348.
    [24]
    Bargmann C I, Kaplan J M. Signal transduction in the Caenorhabditis elegans nervous system. Annual Review of Neuroscience, 1998, 21(1): 279-308.
    [25]
    Allee W C. The orientation of animals. Ecology, 1941, 22(3): 350-350.
    [26]
    Pierce-Shimomura J T, Morse T M, Lockery S R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. Journal of Neuroscience, 1999, 19(21): 9557-9569.
    [27]
    Pierce-Shimomura J T, Dores M, Lockery S R. Analysis of the effects of turning bias on chemotaxis in C. elegans. Journal of Experimental Biology, 2005, 208(24):4727-4733.
    [28]
    Luo L, Cook N, Venkatachalam V, et al. Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(7): 2776-2781.
    [29]
    Jansen G, Weinkove D, Plasterk R H A. The G-protein γ subunit gpc-1 of the nematode C.elegans is involved in taste adaptation. The EMBO Journal, 2002, 21(5): 986-994.
    [30]
    Ikeda M, Nakano S, Giles A C, et al. Context-dependent operation of neural circuits under-lies a navigation behavior in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(11): 6178-6188.
    [31]
    Iino Y, Yoshida K. Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. Journal of Neuroscience, 2009, 29(17): 5370-5380.
    [32]
    Ryu W S, Samuel A. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined thermal stimuli. The Journal of Neuroscience, 2002, 22(13): 5727-5733.
    [33]
    Clark D A, Gabel C V, Lee T M, et al. Short-term adaptation and temporal processing in the cryophilic response of Caenorhabditis elegans. Journal of Neurophysiology, 2006, 97(3): 1903-1910.
    [34]
    Leifer A M, Fang-Yen C, Gershow M, et al. Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nature Methods, 2011, 8(2): 147-152.
    [35]
    Kunitomo H, Sato H, Iwata R, et al. Concentration memory-dependent synaptic plasticity of a taste circuit regulates salt concentration chemotaxis in Caenorhabditis elegans. Nature Communications, 2013, 4: 2210.
    [36]
    Gong J, Liu J, Ronan E A, et al. A Cold-sensing receptor encoded by a glutamate receptor gene. Cell, 2019, 178(6): 1375-1386.e11.
    [37]
    Clark D A, Biron D, Sengupta P, et al. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. Journal of Neuroscience, 2006, 26(28): 7444-7451.
    [38]
    Clark D A, Gabel C V, Gabel H, et al. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. Journal of Neuroscience, 2007, 27(23): 6083-6090.
    [39]
    Tomioka M, Adachi T, Suzuki H, et al. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron, 2006, 51(5): 613-625.
    [40]
    Suzuki H, Thiele T R, Faumont S, et al. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature, 2008, 454: 114-117.
    [41]
    Thiele T R, Fa Umont S, Lockery S R. The neural network for chemotaxis to tastants in Caenorhabditis elegans is specialized for temporal differentiation. Journal of Neuroscience, 2009, 29(38): 11904-11911.
    [42]
    Kimata T, Sasakura H, Ohnishi N, et al. Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity. Worm, 2012, 1(1): 31-41.
    [43]
    Dusenbery D B, Sheridan R E, Russell R L. Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. Genetics, 1975, 80(2): 297-309.
    [44]
    Komatsu H, Mori I, Rhee J S, et al. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron, 1996, 17(4): 707-718.
    [45]
    Li Z, Liu J, Zheng M, et al. Encoding of both analog- and digital-like behavioral outputs by one C. elegans interneuron. Cell, 2014, 159(4): 751-765.
    [46]
    Wang Y, Zhang X, Xin Q, et al. Flexible motor sequence generation during stereotyped escape responses. Elife, 2020, 9: e56942.
    [47]
    Kato S, Kaplan H S, Schrödel T, et al. Global brain dynamics embed the motor command sequence of Caenorhabditis elegans. Cell, 2015, 163(3): 656-669.
    [48]
    Stringer C, Pachitariu M, Steinmetz N, et al. Spontaneous behaviors drive multidimensional, brainwide activity. Science, 2019, 364(6437): 255.
    [49]
    Rumyantsev O I, Lecoq J A, Hernandez O, et al. Fundamental bounds on the fidelity of sensory cortical coding. Nature, 2020, 580(7801): 100-105.
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