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The Contribution of Sensory Stimulation to Motor Performance in Insects

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Abstract

Rapid adaptation of insects to changes in the environment is largely due to the plasticity of their response to biologically significant external signals. The generation of behavior by the nervous system of an insect, like that in other animals, consists of the sensory, integrative, and motor components. Sensory inputs of different modalities adjust the behavioral response at all the levels of neural processing. The integrative component ends with the formation of a motor command which is then carried out by the circuits coordinating motor neurons. The motor nerve centers adjust to the current situation at two levels: local and central. Adaptation of the insect’s movements to the local situation is based on sensory feedback from proprioceptors carrying information about the leg position. At the organism level, exteroceptor signals of different modalities facilitate control of the command neurons. The role of these signals remains largely unstudied, even though they underlie high adaptability of insect behavior.

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REFERENCES

  1. Abram, P.K., Boivin, G., Moiroux, J., and Brodeur, J., Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity, Biol. Rev., 2017, vol. 92, no. 4, p. 1859. https://doi.org/10.1111/brv.12312

    Article  PubMed  Google Scholar 

  2. Ache, J.M., Haupt, S.S., and Dürr, V., A direct descending pathway informing locomotor networks about tactile sensor movement, J. Neurosci., 2015, vol. 35, no. 9, p. 4081. https://doi.org/10.1523/JNEUROSCI.3350-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Adamo, S.A., Linn, C.E., and Hoy, R.R., The role of neurohormonal octopamine during “fight or flightˮ behaviour in the field cricket Gryllus bimaculatus, J. Exp. Biol., 1995, vol. 198, p. 1691. https://doi.org/10.1242/jeb.198.8.1691

  4. Akay, T., Tourtellotte, W.G., Arber, S., and Jessell, T.M., Degradation of mouse locomotor pattern in the absence of proprioceptive sensory feedback, Proc. Natl. Acad. Sci., 2014, vol. 111, no. 47, p. 16877. https://doi.org/10.1073/pnas.1419045111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Andrés, M., Seifert, M., Spalthoff, Ch., Warren, B., Weiss, L., Giraldo, D., Winkler, M., Pauls, S., and Göpfert, M.C., Auditory efferent system modulates mosquito hearing, Curr. Biol., 2016, vol. 26, p. 2028 https://doi.org/10.1016/j.cub.2016.05.077

    Article  CAS  PubMed  Google Scholar 

  6. Anton, S., Evengaard, K., Barrozo, R.B., Anderson, P., and Skals, N., Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect, Proc. Natl. Acad. Sci., 2011, vol. 108, p. 3401. https://doi.org/10.1073/pnas.1008840108

    Article  PubMed  PubMed Central  Google Scholar 

  7. Aranda, L.C. and Luco, J.V., Further studies on an electric correlate to learning. Experiments in an isolated insect ganglion, Physiol. Behav., 1969, vol. 4, p. 133. https://doi.org/10.1016/0031-9384(69)90068-7

    Article  Google Scholar 

  8. Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K.R., Vogt, K., Belliart-Guérin, G., Plaçais, P.Y., Robie, A.A., Yamagata, N., Schnaitmann, C., Rowell, W.J., Johnston, R.M., Ngo, T.B., Chen, N., Korff, W., Nitabach, M.N., Heberlein, U., Preat, T., Branson, R.M., Tanimoto, H., and Rubin, G.M., The neuronal architecture of the mushroom body provides a logic for associative learning, eLife, 2014, vol. 3: e04577. https://doi.org/10.7554/eLife.04577

  9. Awata, H., Watanabe, T., Hamanaka, Y., Mito, T., Noji, S., and Mizunami, M., Knockout crickets for the study of learning and memory: Dopamine receptor Dop1 mediates aversive but not appetitive reinforcement in crickets, Sci. Rep., 2015, vol. 5: 15885. https://doi.org/10.1038/srep15885

  10. Ayali, A., Borgmann, A., Büschges, A., Couzin-Fuchs, E., Gruhn, S.D., and Holmes, P., The comparative investigation of the stick insect and cockroach models in the study of insect locomotion, Curr. Opin. Ins. Sci., 2015, vol. 12, p. 1. https://doi.org/10.1016/j.cois.2015.07.004

    Article  Google Scholar 

  11. Barron, A.B. and Klein, C., What insects can tell us about the origins of consciousness, Proc. Natl. Acad. Sci., 2016, vol. 113, no. 18, p. 4900. https://doi.org/10.1073/pnas.1520084113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Barroso, J.G., Pedro, L.M., Gonçalves, M.A., Figueiredo, A.C., Miguel, M.G., and Almeida, M.L., Toxic effects of three essential oils on Ceratitis capitata, J. Essent. Oil-Bear. Plants, 2010, vol. 13, no. 191. https://doi.org/10.1080/0972060X.2010.10643811

  13. Berry, J.A., Phan, A., and Davis, R.L., Dopamine neurons mediate learning and forgetting through bidirectional modulation of a memory trace, Cell Rep., 2018, vol. 25, no. 3, p. 651. https://doi.org/10.1016/j.celrep.2018.09.051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bidaye, S.S., Bockemühl, T., and Büschges, A., Six-legged walking in insects: how CPGs, peripheral feedback, and descending signals generate coordinated and adaptive motor rhythms, J. Neurophysiol., 2018, vol. 119, no. 2, p. 459. https://doi.org/10.1152/jn.00658.2017

    Article  PubMed  Google Scholar 

  15. Birmingham, J.T. and Tauck, D.L., Neuromodulation in invertebrate sensory systems: from biophysics to behavior, J. Exp. Biol., 2003, vol. 206, p. 3541. https://doi.org/10.1242/jeb.00601

    Article  PubMed  Google Scholar 

  16. Blanckenhorn, W.U., Behavioral, plastic, and evolutionary responses to a changing world, in Insect Behavior: From Mechanisms to Ecological and Evolutionary Consequences, Córdoba-Aguilar, A., González-Tokman, D., and GonzálezSantoyo, I., Eds., Oxford Univ. Press, 2018, p. 292. https://doi.org/10.1093/oso/9780198797500.003.0019

  17. Borgmann, A. and Büschges, A., Insect motor control: methodological advances, descending control and inter-leg coordination on the move, Curr. Opin. Neurobiol., 2015, vol. 33, p. 8. https://doi.org/10.1016/j.conb.2014.12.010

    Article  CAS  PubMed  Google Scholar 

  18. Böröczky, K., Wada-Katsumata, A., Batchelor, D., Zhukovskaya, M., and Schal, C., Insects groom their antennae to enhance olfactory acuity, Proc. Natl. Acad. Sci., 2013, vol. 110, no. 9, p. 3615. https://doi.org/10.1073/pnas.1212466110

    Article  PubMed  PubMed Central  Google Scholar 

  19. Borst, A. and Helmstaedter, M., Common circuit design in fly and mammalian motion vision, Nat. Neurosci., 2015, vol. 18, p. 1067. https://doi.org/10.1038/nn.4050

    Article  CAS  PubMed  Google Scholar 

  20. Burdohan, J.A. and Comer, C.M., Cellular organization of an antennal mechanosensory pathway in the cockroach, Periplaneta americana, J. Neurosci., 1996, vol. 16, p. 5830. https://doi.org/10.1523/JNEUROSCI.16-18-05830

  21. Burrows, M. and Newland, P.L., Correlation between the receptive fields of locust interneurons, their dendritic morphology, and the central projections of mechanosensory neurons, J. Comp. Neurol., 1993, vol. 329, no. 3, p. 412. https://doi.org/10.1002/cne.903290311

    Article  CAS  PubMed  Google Scholar 

  22. Büschges, A. and Gruhn, M., Mechanosensory feedback in walking: from joint control to locomotor patterns, Adv. Insect Physiol., 2007, vol. 27, no. 12, p. 3285. https://doi.org/10.1016/S0065-2806(07)34004-6

    Article  Google Scholar 

  23. Calabrese, R.L., Oscillation in motor pattern-generating networks, Curr. Opin. Neurobiol., 1995, vol. 5, no. 6, p. 816. https://doi.org/10.1016/0959-4388(95)80111-1

    Article  CAS  PubMed  Google Scholar 

  24. Cao, L.H., Jing, B.Y., Yang, D., Zeng, X., Shen, Y., Tu, Y., and Luo, D.G., Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons, Proc. Natl. Acad. Sci., 2016, vol. 113, no. 7, p. 902. https://doi.org/10.1073/pnas.1518329113

  25. Chow, D.M. and Frye, M.A., The neuro-ecology of resource localization in Drosophila: behavioral components of perception and search, Fly, 2009, vol. 3, p. 50. https://doi.org/10.4161/fly.3.1.7775

  26. Chow, D.M., Theobald, J.C., and Frye, M.A., An olfactory circuit increases the fidelity of visual behavior, J. Neurosci., 2011, vol. 31, no. 42, p. 15035. https://doi.org/10.1523/JNEUROSCI.1736-11.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. DiCaprio, R.A., Wolf, H., and Büschges, A., Activity-dependent sensitivity of proprioceptive sensory neurons in the stick insect femoral chordotonal organ, J. Neurophysiol., 2002, vol. 88, no. 5, p. 2387. https://doi.org/10.1152/jn.00339.2002

    Article  CAS  PubMed  Google Scholar 

  28. Eaton, R.C., Lee, R.K.K., and Foreman, M.B., The Mauthner cell and other identified neurons of the brainstem escape network of fish, Progr. Neurobiol., 2001, vol. 63, no. 4, p. 467. https://doi.org/10.1016/S0301-0082(00)00047-2

    Article  CAS  Google Scholar 

  29. Eisenstein, E.M. and Cohen, M.J., Learning in an isolated prothoracic insect ganglion, Anim. Behav., 1965, vol. 13, p. 104. https://doi.org/10.1016/0003-3472(65)90079-5

    Article  Google Scholar 

  30. Fain, G.L., Hardie, R., and Laughlin, S.B., Phototransduction and the evolution of photoreceptors, Curr. Biol., 2010, vol. 20, no. 3, p. R114. https://doi.org/10.1016/j.cub.2009.12.006

  31. Farhan, A., Gulati, J., Groβe-Wilde, E., Vogel, H., Hansson, B., and Knaden, M., The CCHamide 1 receptor modulates sensory perception and olfactory behavior in starved Drosophila, Sci. Rep., 2013, vol. 3, no. 1, p. 1. https://doi.org/10.1038/srep02765

  32. Farris, S.M., Evolution of complex higher brain centers and behaviors: behavioral correlates of mushroom body elaboration in insects, Brain Behav. Evol., 2013, vol. 82, no. 1, p. 9. https://doi.org/10.1159/000352057

    Article  PubMed  Google Scholar 

  33. Flecke, C. and Stengl, M., Octopamine and tyramine modulate pheromone-sensitive olfactory sensilla of the hawkmoth Manduca sexta in a time-dependent manner, J. Comp. Physiol. Ser. A, 2009, vol. 195, p. 529. https://doi.org/10.1007/s00359-009-0429-4

  34. Fox, A.N., Pitts, R.J., Robertson, H.M., Carlson, J., and Zwiebel, L.J., Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding, Proc. Natl. Acad. Sci., 2001, vol. 98, p. 14693. https://doi.org/10.1073/pnas.261432998

  35. French, A.S. and Torkkeli, P.H., The basis of rapid adaptation in mechanoreceptors, Physiology, 1994, vol. 9, no. 4, p. 158. https://doi.org/10.1152/physiologyonline.1994.9.4.158

    Article  Google Scholar 

  36. Frolov, R.V., Current advances in invertebrate vision: insights from patch-clamp studies of photoreceptors in apposition eyes, J. Neurophysiol., 2016, vol. 116, p. 709. https://doi.org/10.1152/jn.00288.2016

    Article  CAS  PubMed  Google Scholar 

  37. Frye, M.A., Multisensory systems integration for high-performance motor control in flies, Curr. Opin. Neurobiol., 2010, vol. 20, no. 3, p. 347. https://doi.org/10.1016/j.conb.2010.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Fuchs, E., Holmes, P., Kiemel, T., and Ayali, A., Inter-segmental coordination of cockroach locomotion: adaptive control of centrally coupled pattern generator circuits, Front. Neural Circuits, 2011, vol. 4, p. 125. https://doi.org/10.3389/fncir.2010.00125

    Article  PubMed  PubMed Central  Google Scholar 

  39. Gal, R. and Libersat, F., On predatory wasps and zombie cockroaches: Investigations of free will and spontaneous behavior in insects, Comm. Integr. Biol., 2010, vol. 3, no. 5, p. 458. https://doi.org/10.4161/cib.3.5.12472

    Article  Google Scholar 

  40. Ganeshina, O. and Menzel, R., GABA immunoreactive neurons in the mushroom bodies of the honeybee: An electron microscopic study, J. Comp. Neurol., 2001, vol. 437, p. 335. https://doi.org/10.1002/cne.1287

    Article  CAS  PubMed  Google Scholar 

  41. Ghalichi, N.S., Heinen-Kay, J.L., and Zuk, M., Acoustic experience interacts with perceived risk of predation in shaping female response in crickets, J. Insect Behav., 2020, vol. 33, p. 38. https://doi.org/10.1007/s10905-020-09744-y

    Article  Google Scholar 

  42. Golovin, R.M., Vest, J., Vita, D.J., and Broadie, K., Activitydependent remodeling of Drosophila olfactory sensory neuron brain innervation during an early-life critical period, J. Neurosci., 2019, vol. 39, no. 16, p. 2995. https://doi.org/10.1523/JNEUROSCI.2223-18.2019

  43. Gorelkin, V.S. and Severina, I.Yu., Role of central and peripheral mechanisms in control of excitability of segmental motor centers in insects, J. Evol. Biochem. Physiol., 2004, vol. 40, no. 6, p. 508. https://doi.org/10.1007/s10893-005-0019-1

    Article  CAS  Google Scholar 

  44. Gorelkin, V.S., Severina, I.Yu., Isavnina, I.L., and Sviderskii, V.L., 2008. Effect of static load on motor behavior of the cockroach Periplaneta americana, J. Evol. Biochem. Physiol., 2008, vol. 44, no. 3, p. 245. https://doi.org/10.1134/S0022093008030046

  45. Gorelkin, V.S., Severina, I.Yu., and Isavnina, I.L., Functional role of leg receptors of the cockroach Periplaneta americana in the system of walking control, J. Evol. Biochem. Physiol., 2012, vol. 48, no. 6, p. 577. https://doi.org/10.1134/S0022093013030092

  46. Gribakin, F.G., Mekhanizmy fotoretseptsii nasekomykh (Mechanisms of Photoreception in Insects), Leningrad: Nauka, 1981.

  47. Gronenberg, W. and Schmitz, H., Afferent projections of infrared-sensitive sensilla in the beetle Melanophila acuminata (Coleoptera: Buprestidae), Cell Tissue Res., 1999, vol. 297, no. 2, p. 311.

  48. Gu, Y., Oberwinkler, J., Postma, M., and Hardie, R.C., Mechanisms of light adaptation in Drosophila photoreceptors, Curr. Biol., 2005, vol. 15, p. 1228. https://doi.org/10.1016/j.cub.2005.05.058

  49. Guerrieri, E., Giorgini, M., Cascone, P., Carpenito, S., and van Achterberg, C., Species diversity in the parasitoid genus Asobara (Hymenoptera: Braconidae) from the native area of the fruit fly pest Drosophila suzukii (Diptera: Drosophilidae), PLoS ONE, 2016, vol. 11, no. 2: e0147382. https://doi.org/10.1371/journal.pone.0147382

  50. Guo, H., Kunwar, K., and Smith, D., Odorant receptor sensitivity modulation in Drosophila, J. Neurosci., 2017, vol. 37, no. 39, p. 9465. https://doi.org/10.1523/JNEUROSCI.1573-17.2017

  51. Haenicke, J., Yamagata, N., Zwaka, H., Nawrot, M., and Menzel, R., Neural correlates of odor learning in the presynaptic microglomerular circuitry in the honeybee mushroom body calyx, eNeuro, 2018, vol. 5, no. 3, p. 1. https://doi.org/10.1523/ENEURO.0128-18.2018

    Article  Google Scholar 

  52. Hammer, M., An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees, Nature, 1993, vol. 366, p. 59. https://doi.org/10.1038/366059a0

    Article  CAS  PubMed  Google Scholar 

  53. Hammer, M. and Menzel, R., Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees, Learn. Mem., 1998, vol. 5, no. 1, p. 146.

    Article  CAS  Google Scholar 

  54. Han, Q., Hansson, B.S., and Anton, S., Interactions of mechanical stimuli and sex pheromone information in antennal lobe neurons of a male moth, Spodoptera littoralis, J. Comp. Physiol. A, 2005, vol. 191, no. 6, p. 521. https://doi.org/10.1007/s00359-005-0618-8

  55. Haney, S., Saha, D., Raman, B., and Bazhenov, M., Differential effects of adaptation on odor discrimination, J. Neurophysiol., 2018, vol. 120, p. 171. https://doi.org/10.1152/jn.00389.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Harris, J.T. and Eisenstein, E.M., Transfer of learned information between ganglia in the insect ventral nerve cord, Behav. Brain Res., 1999, vol. 103, no. 2, p. 211. https://doi.org/10.1016/S0166-4328(99)00039-X

    Article  CAS  PubMed  Google Scholar 

  57. Hildebrandt, K.J., Benda, J., and Hennig, R.M., The origin of adaptation in the auditory pathway of locusts is specific to cell type and function, J. Neurosci., 2009, vol. 29, no. 8, p. 2626. https://doi.org/10.1523/JNEUROSCI.4800-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hildebrandt, K.J., Benda, J., and Hennig, R.M., Computational themes of peripheral processing in the auditory pathway of insects, J. Comp. Physiol. A, 2015, vol. 201, no. 1, p. 39. https://doi.org/10.1007/s00359-014-0956-5

    Article  Google Scholar 

  59. Hill, S.R., Ghaninia, M., and Ignell, R., Blood meal induced regulation of gene expression in the maxillary palps, a chemosensory organ of the mosquito Aedes aegypti, Front. Ecol. Evol., 2019, vol. 7, p. 336. https://doi.org/10.3389/fevo.2019.00336

  60. Hinz, M., Klein, A., Schmitz, A., and Schmitz, H., The impact of infrared radiation in flight control in the Australian “firebeetle” Merimna atrata, PLoS ONE, 2018, vol. 13, no. 2: e0192865. https://doi.org/10.1371/journal.pone.0192865

  61. Hoy, R., Neurobiology: tuning in by turning off, Nature, 2002, vol. 418, no. 6900, p. 831. https://doi.org/10.1038/418831a

    Article  CAS  PubMed  Google Scholar 

  62. Hughes, G.M. and Wiersma, C.A.G., The co-ordination of swimmeret movements in the crayfish, Procambarus clarkii (Girard), J. Exp. Biol., 1960, vol. 37, p. 657. https://doi.org/10.1242/jeb.37.4.657

  63. Hunt, J.H., A conceptual model for the origin of worker behaviour and adaptation of eusociality, J. Evol. Biol., 2012, vol. 25, no. 1, p. 1. https://doi.org/10.1111/j.1420-9101.2011.02421.x

    Article  PubMed  Google Scholar 

  64. Hustert, R. and Mashaly, A.M., Spontaneous behavioral rhythms in the isolated CNS of insects – Presenting new model systems, J. Physiol. Paris, 2013, vol. 107, no. 1, p. 147. https://doi.org/10.1016/j.jphysparis.2012.05.001

    Article  CAS  PubMed  Google Scholar 

  65. Immonen, E.V., Ignatova, I., Gislen, A., Warrant, E., Vähäsöyrinki, M., Weckström, M., and Frolov, R., Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer, Proc. R. Soc. B, 2014, vol. 281: 20141177. https://doi.org/10.1098/rspb.2014.1177

  66. Iwano, M., Hill, E.S., Mori, A., Mishima, T., Mishima, T., Ito, K., and Kanzaki, R., Neurons associated with the flip-flop activity in the lateral accessory lobe and ventral protocerebrum of the silkworm moth brain, J. Comp. Neurol., 2010, vol. 518, p. 366. https://doi.org/10.1002/cne.22224

    Article  PubMed  Google Scholar 

  67. Jang, E.B., Effects of mating and accessory gland injections on olfactory-mediated behavior in the female Mediterranean fruit fly, Ceratitis capitata, J. Insect Physiol., 1995, vol. 41, no. 8, p. 705. https://doi.org/10.1016/0022-1910(95)00015-M

  68. Kaissling, K.E., Zack Strausfeld, C., and Rumbo, E.R., Adaptation processes in insect olfactory receptors. Mechanisms and behavioral significance, Ann. N. Y. Acad. Sci., 1987, vol. 510, no. 104. https://doi.org/10.1111/j.1749-6632.1987.tb43475.x

  69. Kanzaki, R., Ikeda, A., and Shibuya, T., Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori, J. Comp. Physiol. A, 1994, vol. 175, p. 1. https://doi.org/10.1111/j.1749-6632.1987.tb43475.x

  70. Kapitsky, S.V. and Zhukovskaya, M.I., Modulation of sensitivity to the sex pheromone in the male cockroach Periplaneta americana L.: Octopamine changes the sensillum response, Sens. Sist., 2001, vol. 15, no. 2, p. 147.

  71. Kasparyan, D.R., The main trends in evolution of parasitism in Hymenoptera, Entomol. Obozr., 1996, vol. 75, no. 4, p. 756.

    Google Scholar 

  72. Kaufman, B.Z., Photo- and thermopreferential behavior of crickets Acheta domestica L. and Gryllus bimaculatus Deg. (Orthoptera, Gryllidae) in relation to some peculiarities of their evolution, Entomol. Obozr., 1999, vol. 78, no. 1, p. 15.

  73. Kerkut, G.A. and Taylor, B., A temperature receptor in the tarsus of the cockroach, Periplaneta americana, J. Exp. Biol., 1957, vol. 34, p. 486.

  74. Kien, J. and Altman, J.S., Descending interneurons from the brain and subesophageal ganglia and their roles in the control of locust behaviour, J. Insect Physiol., 1984, vol. 30, p. 59. https://doi.org/10.1016/0022-1910(84)90108-2

    Article  Google Scholar 

  75. Knebel, D., Ayali, A., Pflüger, H.J., and Rillich, J., Rigidity and flexibility: the central basis of inter-leg coordination in the locust, Front. Neural Circuits, 2017, vol. 10, p. 112. https://doi.org/10.3389/fncir.2016.00112

    Article  PubMed  PubMed Central  Google Scholar 

  76. Krapp, H.G., Hengstenberg, B., and Hengstenberg, R., Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly, J. Neurophysiol., 1998, vol. 79, no. 4, p. 1902.

    Article  CAS  Google Scholar 

  77. Kühne, R., Silver, S., and Lewis, B., Processing of vibratory and acoustic signals by ventral cord neurons in the cricket Gryllus campestris, J. Insect Physiol., 1984, vol. 30, p. 575. https://doi.org/10.1016/0022-1910(84)90086-6

  78. Kukillaya, R., Proctor, J., and Holmes, P., Neuromechanical models for insect locomotion: Stability, maneuverability, and proprioceptive feedback, Chaos Interdiscip. J. Nonlinear Sci., 2009, vol. 19, no. 2: 026107. https://doi.org/10.1063/1.3141306

  79. Latif, T. and Bozkurt, A., Line following terrestrial insect biobots, in Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2012. https://doi.org/10.1109/embc.2012.6346095

  80. Latorre-Estivalis, J.M., Sterkel, M., Ons, S., and Lorenzo, M., Transcriptomics supports local sensory regulation in the antenna of the kissing-bug Rhodnius prolixus, BMC Genomics, 2020, vol. 21, no. 1, p. 1. https://doi.org/10.1186/s12864-020-6514-3

  81. Laughlin, S.B. and Hardie, R.C., Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly, J. Comp. Physiol., 1978, vol. 128, no. 4, p. 319.

    Article  Google Scholar 

  82. Laurent, G., Thoracic intersegmental interneurons in the locust with mechanoreceptive inputs from a leg, J. Comp. Physiol. A, 1986, vol. 159, p. 171. https://doi.org/10.1007/BF00612300

    Article  Google Scholar 

  83. Lee, J., Moon, S., Cha, Y., and Chung, Y.D., Drosophila TRPN (= NOMPC) channel localizes to the distal end of mechanosensory cilia, PLoS ONE, 2010, vol. 5, no. 6: e11012. https://doi.org/10.1371/journal.pone.0011012

  84. Libersat, F., Modulation of flight by the giant interneurons of the cockroach, J. Comp. Physiol. A, 1992, vol. 170, p. 379. https://doi.org/10.1007/BF00191427

    Article  Google Scholar 

  85. Linn, C.E.Jr., Poole, K.R., and Roelofs, W.L., Studies on biogenic amines and their metabolites in nervous tissue and hemolymph of adult male cabbage looper moths. I. Quantitation of photoperiod changes, Comp. Biochem. Physiol. C, 1994, vol. 108, no. 1, p. 73. https://doi.org/10.1016/1367-8280(94)90092-2

    Article  Google Scholar 

  86. Ludwar, B.C., Göritz, M.L., and Schmidt, J., Intersegmental coordination of walking movements in stick insects, J. Neurophysiol., 2005, vol. 93, no. 3, p. 1255. https://doi.org/10.1152/jn.00727.2004

    Article  PubMed  Google Scholar 

  87. Marder, E., Bucher, D., Schulz, D.J., and Taylor, A.L., Invertebrate central pattern generation moves along, Curr. Biol., 2005, vol. 15, no. 17, p. R685. https://doi.org/10.1016/j.cub.2005.08.022

  88. Mazokhin-Porshnyakov, G.A., Rukovodstvo po fiziologii organov chuvstv nasekomykh (Physiology of the Insect Sensory Organs: a Study Guide), Moscow: Mosk. Univ., 1977.

  89. McDiarmid, T.A., Yu, A.J., and Rankin, C.H., Habituation is more than learning to ignore: multiple mechanisms serve to facilitate shifts in behavioral strategy, BioEssays, 2019, vol. 41, no. 9: 1900077. https://doi.org/10.1002/bies.201900077

  90. McGorry, C.A., Newman, C.N., and Triblehorn, J.D., Neural responses from the wind-sensitive interneuron population in four cockroach species, J. Insect Physiol., 2014, vol. 66, p. 59. https://doi.org/10.1016/j.jinsphys.2014.05.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Menzel, R., The honeybee as a model for understanding the basis of cognition, Nat. Rev. Neurosci., 2012, vol. 13, no. 11, p. 758. https://doi.org/10.1038/nrn3357

    Article  CAS  PubMed  Google Scholar 

  92. Menzel, R. and Knaut, R., Pigment movement during light and chromatic adaptation in the retinula cells of Formica polyctena (Hymenoptera, Formicidae), J. Comp. Physiol. A, 1973, vol. 86, p. 125. https://doi.org/10.1007/BF00702533

  93. Meola, S.M. and Sittertz-Bhatkar, H., Neuroendocrine modulation of olfactory sensory neuron signal reception via axodendritic synapses in the antennae of the mosquito, Aedes aegypti, J. Mol. Neurosci., 2002, vol. 18, p. 239. https://doi.org/10.1385/JMN:18:3:239

  94. Nagel, K.I. and Wilson, R.I., Biophysical mechanisms underlying olfactory receptor neuron dynamics, Nat. Neurosci., 2011, vol. 14, no. 2, p. 208. https://doi.org/10.1038/nn.2725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Namiki, S., Iwabuchi, S., Pansopha Kono, P., and Kanzaki, R., Information flow through neural circuits for pheromone orientation, Nat. Comm., 2014, vol. 5, p. 5919. https://doi.org/10.1038/ncomms6919

    Article  CAS  Google Scholar 

  96. Namiki, S., Wada, S., and Kanzaki, R., Descending neurons from the lateral accessory lobe and posterior slope in the brain of the silkmoth Bombyx mori, Sci. Rep., 2018, vol. 8, no. 1, p. 9663. https://doi.org/10.1038/s41598-018-27954-5

  97. Narendra, A., Greiner, B., Ribi, W.A., and Zeil, J., Light and dark adaptation mechanisms in the compound eyes of Myrmecia ants that occupy discrete temporal niches, J. Exp. Biol., 2016, vol. 219, no. 16, p. 2435. https://doi.org/10.1242/jeb.142018

  98. Newland, P.L., Rogers, S.M., Gaaboub, I., and Matheson, T., Parallel somatotopic maps of gustatory and mechanosensory neurons in the central nervous system of an insect, J. Comp. Neurol., 2000, vol. 425, no. 1, p. 82. https://doi.org/10.1002/1096-9861(20000911)425:1<82::

    Article  CAS  PubMed  Google Scholar 

  99. Novikova, E.S. and Zhukovskaya, M.I., Bright light induced freezing behavior in American cockroach, Periplaneta americana, Sens. Sist., 2017, vol. 31, no. 1, p. 42.

  100. Okada, R., Sakura, M., and Mizunami, M., Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain, J. Comp. Neurol., 2003, vol. 458, p. 158. https://doi.org/10.1002/cne.10580

    Article  PubMed  Google Scholar 

  101. Okada, R., Rybak, J., Manz, G., and Menzel, R., Learningrelated plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain, J. Neurosci., 2007, vol. 27, no. 43, p. 11736. https://doi.org/10.1523/JNEUROSCI.2216-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ou, J. and Cleland, C.L., Escape strategies of the Madagascar hissing cockroach (Gromphadorhina portentosa) in response to looming and localized heat stimuli, J. Insect Behav., 2019, vol. 32, no. 4, p. 315. https://doi.org/10.1007/s10905-019-09737-6

  103. Perry, C.J. and Barron, A.B., Neural mechanisms of reward in insects, Annu. Rev. Entomol., 2013, vol. 58, p. 543. https://doi.org/10.1146/annurev-ento-120811-153631

    Article  CAS  PubMed  Google Scholar 

  104. Pflüger, H.J., Motor pattern selection and initiation in invertebrates with an emphasis on insects, in Neurobiology of Motor Control: Fundamental Concepts and New Directions, Hooper, S.L. and Büschges, A., Eds., Hoboken: John Wiley and Sons, 2017, p. 195.

  105. Polyanovsky, A.D. and Alekseeva, T.M., Mechanotransduction in invertebrates: molecular mechanisms and ultrastructural correlates, Sens. Sist., 2001, vol. 15, no. 2, p. 155.

    Google Scholar 

  106. Pophof, B., Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons, J. Comp. Physiol., A, 2000, vol. 186, p. 307. https://doi.org/10.1007/s003590050431

    Article  CAS  Google Scholar 

  107. Reinouts Van Haga, H. and Mitchell, B., Temperature receptors on tarsi of the tsetse fly Glossina morsitans West., Nature, 1975, vol. 255, p. 225. https://doi.org/10.1038/255225a0

  108. Reisenman, C.E., Riffell, J.A., Duffy, K., and Pesque, A., Species-specific effects of herbivory on the oviposition behavior of the moth Manduca sexta, J. Chem. Ecol., 2013, vol. 39, no. 1, p. 76. https://doi.org/10.1007/s10886-012-0228-1

  109. Rillich, J. and Stevenson, P.A., Releasing stimuli and aggression in crickets: octopamine promotes escalation and maintenance but not initiation, Front. Behav. Neurosci., 2015, vol. 9, p. 95. https://doi.org/10.3389/fnbeh.2015.00095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Rillich, J., Stevenson, P.A., and Pflueger, H.J., Flight and walking in locusts – cholinergic co-activation, temporal coupling and its modulation by biogenic amines, PLoS One, 2013, vol. 8, no. 5: e62899. https://doi.org/10.1371/journal.pone.0062899

  111. Rind, F.C. and Bramwell, D.I., Neural network based on the input organization of an identified neuron signaling impending collision, J. Neurophysiol., 1996, vol. 75, no. 3, p. 967. https://doi.org/10.1152/jn.1996.75.3.967

    Article  CAS  PubMed  Google Scholar 

  112. Rings, A. and Goodwin, S.F., To court or not to court – a multimodal sensory decision in Drosophila males, Curr. Opin. Insect Sci., 2019, vol. 35, p. 48. https://doi.org/10.1016/j.cois.2019.06.009

  113. Ritzmann, R.E., Pollack, A.J., and Tobias, M.L., Flight activity mediated by intracellular stimulation of dorsal giant interneurons of the cockroach Periplaneta americana, J. Comp. Physiol., 1982, vol. 147, no. 3, p. 313. https://doi.org/10.1007/BF00609665

  114. Ritzmann, R.E., Pollack, A.J., Hudson, S.E., and Hyvonen, A., Convergence of multi-modal sensory signals at thoracic interneurons of the escape system of the cockroach, Periplaneta americana, Brain Res., 1991, vol. 563, p. 175. https://doi.org/10.1016/0006-8993(91)91531-5

  115. Scheiner, R., Responsiveness to sucrose and habituation of the proboscis extension response in honey bees, J. Comp. Physiol. A, 2004, vol. 190, no. 9, p. 727. https://doi.org/10.1007/s00359-004-0531-6

    Article  CAS  Google Scholar 

  116. Schendzielorz, T., Peters, W., Boekhoff, I., and Stengl, M., Time of day changes in cyclic nucleotides are modified via octopamine and pheromone in antennae of the Madeira cockroach, J. Biol. Rhythms, 2012, vol. 27, p. 388. https://doi.org/10.1177/0748730412456265

    Article  CAS  PubMed  Google Scholar 

  117. Schendzielorz, T., Schirmer, K., Stolte, P., and Stengl, M., Octopamine regulates antennal sensory neurons via daytimedependent changes in cAMP and IP3 levels in the hawkmoth Manduca sexta, PLoS One, 2015, vol. 10, no. 3: e0121230. https://doi.org/10.1371/journal.pone.0121230

  118. Schmitz, A., Schätzel, H., and Schmitz, H., Distribution and functional morphology of photomechanic infrared sensilla in flat bugs of the genus Aradus (Heteroptera, Aradidae), Arthropod Struct. Dev., 2010, vol. 39, no. 1, p. 17. https://doi.org/10.1016/j.asd.2009.10.007

  119. Schmitz, H., Schmitz, A., and Bleckmann, H., Morphology of a thermosensitive multipolar neuron in the infrared organ of Merimna atrata (Coleoptera, Buprestidae), Arthropod Struct. Dev., 2001, vol. 30, no. 2, p. 99. https://doi.org/10.1016/S1467-8039(01)00028-7

  120. Sen, R., Wu, M., Branson, K., Robie, A., Rubin, G.M., and Dickson, B.J., Moonwalker descending neurons mediate visually evoked retreat in Drosophila, Curr. Biol., 2017, vol. 27, no. 5, p. 766. https://doi.org/10.1016/j.cub.2017.02.008

  121. Severina, I.Yu., Isavnina, I.L., and Knyazev, A.N., Topographic anatomy of ascending and descending neurons of the supraesophageal, meso- and metathoracic ganglia in paleo- and neopterous insects, J. Evol. Biochem. Physiol., 2016, vol. 52, no. 5, p. 362. https://doi.org/10.1134/S0022093016050082

    Article  Google Scholar 

  122. Severina, I.Yu., Isavnina, I.L., and Knyazev, A.N., Intersegmental thoracic descending interneurons in the cockroach Periplaneta americana, J. Evol. Biochem. Physiol., 2018, vol. 54, no. 6, p. 421. https://doi.org/10.1134/S0044452918060074

  123. Simpson, B.S., Ritzmann, R.E., and Pollack, A.J., A comparison of the escape behaviors of the cockroaches Blaberus craniifer and Periplaneta americana, J. Neurobiol., 1986, vol. 17, no. 5, p. 405. https://doi.org/10.1002/neu.480170505

  124. Someya, M. and Ogawa, H., Multisensory enhancement of burst activity in an insect auditory neuron, J. Neurophysiol., 2018, vol. 120, no. 1, p. 139. https://doi.org/10.1152/jn.00798.2017

    Article  CAS  PubMed  Google Scholar 

  125. Staudacher, E., Distribution and morphology of descending brain neurons in the cricket Gryllus bimaculatus, Cell Tissue Res., 1998, vol. 294, p. 187. https://doi.org/10.1007/s004410051169

  126. Strausfeld, N.J. and Hirth, F., Deep homology of arthropod central complex and vertebrate basal ganglia, Science, 2013, vol. 340, no. 6129, p. 157. https://doi.org/10.1126/science.1231828

    Article  CAS  PubMed  Google Scholar 

  127. Strausfeld, N.J., Bassemir, U., Singh, R.N., and Bacon, J.P., Organizational principles of outputs from dipteran brains, J. Insect Physiol., 1984, vol. 30, p. 73. https://doi.org/10.1016/0022-1910(84)90109-4

    Article  Google Scholar 

  128. Strube-Bloss, M.F., Nawrot, M.P., and Menzel, R., Mushroom body output neurons encode odor–reward associations, J. Neurosci., 2011, vol. 31, no. 8, p. 3129. https://doi.org/10.1523/JNEUROSCI.2583-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Szczecinski, N.S., Brown, A.E., Bender, J.A., and Quinn, R.D., A neuromechanical simulation of insect walking and transition to turning of the cockroach Blaberus discoidalis, Biol. Cybern., 2014, vol. 108, no. 1, p. 1. https://doi.org/10.1007/s00422-013-0573-3

  130. Taylor, B.E. and Lukowiak, K., The respiratory central pattern generator of Lymnaea: a model, measured and malleable, Respir. Physiol., 2000, vol. 122, no. 2, p. 197. https://doi.org/10.1016/S0034-5687(00)00159-6

  131. Turner-Evans, D.B. and Jayaraman, V., The insect central complex, Curr. Biol., 2016, vol. 26, no. 11, p. R453. https://doi.org/10.1016/j.cub.2016.04.006

  132. Tuthill, J.C. and Wilson, R.I., Mechanosensation and adaptive motor control in insects, Curr. Biol., 2016, vol. 26, no. 20, p. R1022. https://doi.org/10.1016/j.cub.2016.06.070

  133. Verburgt, L., Ferreira, M., and Ferguson, J.W.H., Male field cricket song reflects age, allowing females to prefer young males, Anim. Behav., 2011, vol. 81, no. 1, p. 19. https://doi.org/10.1016/j.anbehav.2010.09.010

    Article  Google Scholar 

  134. Vergoz, V., Roussel, E., Sandoz, J.C., and Giurfa, M., Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex, PLoS One, 2007, vol. 2, e288. https://doi.org/10.1371/journal.pone.0000288

  135. Vergoz, V.H., McQuillan, J., Geddes, L.H., Pullar, K., Nicholson, B.J., Paulin, M.G., and Mercer, A.R., Peripheral modulation of worker bee responses to queen mandibular pheromone, Proc. Natl. Acad. Sci., 2009, vol. 106, p. 20930. https://doi.org/10.1073/pnas.0907563106

    Article  PubMed  PubMed Central  Google Scholar 

  136. Wada-Katsumata, A. and Schal, C., Antennal grooming facilitates courtship performance in a group-living insect, the German cockroach Blattella germanica, Sci. Rep., 2019, vol. 9, no. 1, p. 2942. https://doi.org/10.1038/s41598-019-39868-x

  137. Westin, J., Langberg, J.J., and Camhi, J.M., Responses of giant interneurons of the cockroach Periplaneta americana to wind puffs of different directions and velocities, J. Comp. Physiol., 1977, vol. 121, p. 307. https://doi.org/10.1007/BF00613011

  138. Wicher, D., Tuning insect odorant receptors, Front. Cell. Neurosci., 2018, vol. 12, p. 94. https://doi.org/10.3389/fncel.2018.00094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Wiese, K., Influence of vibration on cricket hearing: interaction of low frequency vibration and acoustic stimuli in the omega neuron, J. Comp. Physiol., 1981, vol. 143, no. 1, p. 135. https://doi.org/10.1007/BF00606077

    Article  Google Scholar 

  140. Wu, Q., Zhao, Z., and Shen, P., Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems, Nat. Neurosci., 2005, vol. 8, no. 10, p. 1350. https://doi.org/10.1038/nn1540

  141. Zeiner, R. and Tichy, H., Combined effects of olfactory and mechanical inputs in antennal lobe neurons of the cockroach, J. Comp. Physiol. A, 1998, vol. 182, p. 467. https://doi.org/10.1007/s003590050194

    Article  Google Scholar 

  142. Zhao, X., Pfuhl, G., Surlykke, A., Tro, J., and Berg, B.G., A multisensory centrifugal neuron in the olfactory pathway of heliothine moths, J. Comp. Neurol., 2013, vol. 521, no. 1, p. 152. https://doi.org/10.1002/cne.23166

    Article  CAS  PubMed  Google Scholar 

  143. Zhemchuzhnikov, M.K. and Knyazev, A.N., Change in the character of directional motor reactions of female crickets Gryllus argetinus Sauss. to intraspecies signals under conditions of sensory pathology at different stages of imaginal ontogenesis, J. Evol. Biochem. Physiol., 2011, vol. 47, no. 6, p. 480. https://doi.org/10.1134/S0022093011060093

  144. Zhou, S., Stone, E.A., Mackay, T.F., and Anholt, R.R., Plasticity of the chemoreceptor repertoire in Drosophila melanogaster, PLoS Gen., 2009, vol. 5, no. 10: e1000681. https://doi.org/10.1371/journal.pgen.1000681

  145. Zhukovskaya, M.I., Aminergic regulation of pheromone sensillae in the cockroach Periplaneta americana, J. Evol. Biochem. Physiol., 2007, vol. 43, no. 3, p. 265. https://doi.org/10.1134/S0022093007030064

  146. Zhukovskaya, M.I., Odorant dependent changes in the cuticular secretions on the antenna of the cockroach Periplaneta americana, Sens. Sist., 2011, vol. 25, no. 1, p. 78.

  147. Zhukovskaya, M.I., Modulation by octopamine of olfactory responses to nonpheromone odorants in the cockroach, Periplaneta americana L., Chem. Senses, 2012, vol. 37, no. 5, p. 421. https://doi.org/10.1093/chemse/bjr121

  148. Zhukovskaya, M.I. and Kapitsky, S.V., Activity modulation in cockroach sensillum: The role of octopamine, J. Insect Physiol., 2006, vol. 52, p. 76. https://doi.org/10.1016/j.jinsphys.2005.09.005

    Article  CAS  PubMed  Google Scholar 

  149. Zhukovskaya, M.I. and Polyanovsky, A.D., Biogenic amines in insect antennae, Front. Systems Neurosci., 2017, vol. 11, p. 45. https://doi.org/10.3389/fnsys.2017.00045

    Article  CAS  Google Scholar 

  150. Zhukovskaya, M.I., Yanagawa, A., and Forschler, B.T., Grooming behavior as a mechanism of insect disease defense, Insects, 2013, vol. 4, no. 4, p. 609. https://doi.org/10.3390/insects4040609

    Article  PubMed  PubMed Central  Google Scholar 

  151. Zill, S.N., A model of pattern generation of cockroach walking reconsidered, J. Neurobiol., 1986, vol. 17, no. 4, p. 317. https://doi.org/10.1002/neu.480170406

    Article  CAS  PubMed  Google Scholar 

  152. Zill, S.N., Büschges, A., and Schmitz, J., Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus, J. Comp. Physiol. A, 2011, vol. 197, no. 8, p. 851. https://doi.org/10.1007/s00359-011-0647-4

  153. Zill, S.N., Chaudhry, S., Büschges, A., and Schmitz, J., Force feedback reinforces muscle synergies in insect legs, Arthropod Struct. Dev., 2015, vol. 44, no. 6A, p. 541. https://doi.org/10.1016/j.asd.2015.07.001

    Article  PubMed  Google Scholar 

  154. Zorović, M. and Hedwig, B., Descending brain neurons in the cricket Gryllus bimaculatus (de Geer): auditory responses and impact on walking, J. Comp. Physiol. A, 2013, vol. 199, no. 1, p. 25. https://doi.org/10.1007/s00359-012-0765-7

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This study was carried out within the framework of State research assignment AAAA-A18-118013090245-6.

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  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194223, St. Petersburg, Russia

    M. I. Zhukovskaya, I. Ju. Severina, I. L. Isavnina & A. N. Knyazev

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  3. I. L. Isavnina
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Zhukovskaya, M.I., Severina, I.J., Isavnina, I.L. et al. The Contribution of Sensory Stimulation to Motor Performance in Insects. Entmol. Rev. 101, 863–877 (2021). https://doi.org/10.1134/S0013873821070010

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