Lateralized motor responses in anuran amphibians — an overview of methods and perspectives of studies
DOI:
https://doi.org/10.21638/spbu03.2018.402Abstract
Anuran amphibians represent the most usual subjects for experimental biological research and a divergent group of extant vertebrates comprising species adapted to a variety of environments from aquatic to arboreal. Thus, they become excellent models in research of motor lateralization due to their different phylogenetic position and their anatomical and ecological diversity throughout their evolutionary history, as well as variety of locomotive habits and a diversity of limb use during walking, swimming, feeding and other activities. From the first works in mid-1990’s to the present day, a noticeable progress, a noticeable progress in the study of motor lateralization in anurans is made favored by a set of methodological approaches and their application to various species and life stages. Together, these advances foretell a plethora of interesting developments in the world of laterality research with the anuran amphibian model. Here, the discovery of right-pawedness in toads through the development of a set of different techniques to assess motor lateralization in anuran amphibians, and, as a consequence — important results revealing behavioral and morphological correlates are reviewed and discussed in evolutionary and eco-morphological perspective.
Keywords:
anuran amphibians, lateralization, motor asymmetries, C-start, tadpoles, frogs, snout-wiping response, righting response, asynchronous locomotion, evolution of motor skills
Downloads
Download data is not yet available.
References
Abourachid, A. and Green, D. M. 1999. Origins of the frogkick? Alternate-leg swimming in primitive frogs, families Leiopelmatidae and Ascaphidae. Journal of Herpetology 33:657–663. https://doi.org/10.2307/1565583
Adler, K. and Taylor, D. H. 1981. Toad orientation: variability of response and its relationship to individuality and environmental parameters. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 144:45–51. https://doi.org/10.1007/BF00612796
Almli, C. R. and Fisher, R. S. 1977. Infant rats: sensorimotor ontogeny and effects of substantia nigra destruction. Brain Research Bulletin 2:425–459. https://doi.org/10.1016/0361-9230(77)90052-1
Andrew, R. J. and Dharmaretnam, M. 1991. A timetable of development; 166–176 in: Neural and Behavioural Plasticity: The use of the chick as a model, edited by Andrew, R. J. Oxford: Oxford University Press.
Andrew, R. J., Tommasi, L., and Ford, N. 2000. Motor control by vision and the evolution of cerebral lateralization. Brain and Language 73:220–235. https://doi.org/10.1006/brln.2000.2304
Bezgina, E. N., Moshkov, D. A., Nikitin, V. A., Savel’eva, L. N., and Uteshev, V. K. 1999. Morphogenesis of Mauthner neurons in Xenopus laevis tadpoles following early unilateral eye enucleation. Morphologiia 115(3):49–52.
Bianki, V. L. 1963. Asymmetry of electric reactions of the frog’s brain in response to differentially positioned light sources. Journal of the Higher Neural Activity 13(6):1087–1095.
Bianki, V. L. 1981. Lateralization of functions in the animal brain. International Journal of Neuroscience 15(1-2):37–47. https://doi.org/10.3109/00207458108985844
Bisazza, A., De Santi, A., Bonso, S., and Sovrano, V. A. 2002. Frogs and toads in front of a mirror: lateralization of response to social stimuli in five tadpole amphibians. Behavioural Brain Research 134(1-2):417–424. https://doi.org/10.1016/S0166-4328(02)00055-4
Bisazza, A., Cantalupo, C., Robins, A., Rogers, L. J., and Vallortigara, G. 1996. Right-pawedness in toads. Nature 379:408. https://doi.org/10.1038/379408a0
Bisazza, A., Cantalupo, C., Robins, A., Rogers, L. J., and Vallortigara, G. 1997. Pawedness and motor asymmetries in toads. Laterality 2:49–64. https://doi.org/10.1080/713754252
Blight, A. R. 1978. Golgi-staining of “primary” and “secondary” motoneurons in thedeveloping spinal cord of an amphibian. Journal of Comparative Neurology 180:679–690. https://doi.org/10.1002/cne.901800403
Borkhvardt, V. G. and Ivashintsova, E. B. 1995. Arciferal pectoral girdle of amphibians — an instrument for recognizing right- and left-handedness? Russian Journal of Herpetology 2:34–35.
Borkin, L. J., Litvinchuk, S. N., Rosanov, J. M., and Milto, K. D. 2001. Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): evidence from DNA flow cytometry. Amphibia-Reptilia 22:387–396. https://doi.org/10.1163/15685380152770354
Brácha, V., Zhuravin, I. A., and Bures, J. 1990. The reaching reaction in the rat: a part of the digging pattern? Behavioural Brain Research 36:53–64. https://doi.org/10.1016/0166-4328(90)90159-C
Briggs-Gonzalez, V. S. and Gonzalez, S. C. 2016. Lateralized turning biases in two neotropical tadpoles. Ethology 122:582–587. https://doi.org/10.1111/eth.12503
Canfield, J. G. 2003. Temporal constraints on visually directed C-start responses: Behavioral and physiological correlates. Brain, Behaviour and Evolution 61:148–158. https://doi.org/10.1159/000069751
Casey, M. B. and Lickliter, R. 1998. Prenatal visual experience influences the development of turning bias in bobwhite quail chicks (Colinus virginianus). Neuropsychologia 33:1637–1646. https://doi.org/10.1002/(SICI)1098-2302(199805)32:4<327::AID-DEV7>3.0.CO;2-P
Dadda, M. 2005. Social aggregation and lateralised response to social stimuli in tadpoles (Bufo bufo): Influence of developmental stage. Laterality 10(4):345–352. https://doi.org/10.1080/13576500442000139
Dill, L. M. 1977. ‘Handedness’ in the pacific tree frog (Hyla regilla). Canadian Journal of Zoology 55:1926–1929. https://doi.org/10.1139/z77-248
Downes, H. and Courogen, P. M. 1996. Contrasting effects of anesthetics in tadpole bioassays. Journal of Pharmacology and Experimental Therapeutics 278:284–296.
Emerson, S. B. 1979. The ilio-sacral articulation in frogs: form and function. Biological Journal of the Linnean Society 11:153–168. https://doi.org/j.1095-8312.1979.tb00032.x
Emerson, S. B. 1982. Frog postcranial morphology: identification of a functional complex. Copeia 1982:603–613. https://doi.org/10.2307/1444660
Ewert, J.-P. 1980. Functional areas in the visual system of vertebrates: comparative aspects; 129–146 in: Neuro-Ethology, edited by Ewert, J.-P. Berlin: Springer-Verlag. https://doi.org/10.1007/978-3-642-67500-3_5
Fernand, R. D. 1987. More than meets the eye. Behavioral and Brain Science 10:378–379. https://doi.org/10.1017/S0140525X00023244
Fetcho, J. R. 1990. Morphological variability, segmental relationship, and functional role of a class of commissural interneurons in the spinal cord of goldfish. The Journal of Comparative Neurology 299(3):283–298. https://doi.org/10.1002/cne.902990303
Fetcho, J. R. 1991. Spinal network of the Mauthner cell. Brain, Behaviour and Evolution 37:298–316. https://doi.org/10.1159/000114367
Fetcho, J. R. 1992. Excitation of motoneurons by the Mauthner axon in goldfish: complexities in a “simple” reticulospinal pathway. Journal of Neurophysiology 67:1574–1586. https://doi.org/10.1152/jn.1992.67.6.1574
Fetcho, J. R. and Faber, D. S. 1988. Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish. Journal of Neuroscience 8:4192–4213. https://doi.org/10.1523/JNEUROSCI.08-11-04192.1988
Firestone, S. and Firestone, L. L. 1995. Staurosporine, a protein kinase inhibitor, increases the intoxicating potenties of ethanol and other n-alkanols in Rana pipiens tadpoles. Alcoholism: Clinical and Experimental Research 19:416–419. https://doi.org/10.1111/j.1530-0277.1995.tb01524.x
Gaillard, F. 1990. Visual units in the central nervous system of the frog. Comparative Biochemistry and Physiology, A 96:357–371. https://doi.org/10.1016/0300-9629(90)90097-C
Giljov, A., Karenina, K., and Malashichev, Y. 2011. History of the study of motor lateralization in birds. The Russian Journal of Ornithology 20(664):1151–1165.
Giljov, A., Karenina, K., Ingram, J., and Malashichev, Y. 2015. Parallel emergence of true handedness in the evolution of marsupials and placentals. Current Biology 25(14):1878–1884. https://doi.org/10.1016/j.cub.2015.05.043
Golubitsky, M., Stewart, I., Buono, P.-L., and Collins, J. J. 1999. Symmetry in locomotor central pattern generators and animal gaits. Nature 401:693–695. https://doi.org/10.1038/44416
Goree, B. and Wassersug, R. J. 2001. Are archeobatrachian anurans ambidextrous? — Assessing handedness in Bombina orientalis. Journal of Herpetology 35(4):538–541. https://doi.org/10.2307/1565980
Gosner, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190.
Gray, L. A., O’Reilly, J. C., and Nishikawa, K. 1997. Evolution of forelimb movement patterns for prey manipulation in anurans. Journal of Experimental Zoology 277:417–424. https://doi.org/10.1002/(SICI)1097-010X(19970415)277:6<417::AIDJEZ1>3.0.CO;2-R
Greer, A. E. and Mills, A. C. 1997. Directional asymmetry in the amphibian pectoral girdle: additional data and a brief overview. Journal of Herpetology 31:594–596. https://doi.org/10.2307/1565619
Grillner, S. and Wallen, P. 1985. Central pattern generators for locomotion, with special reference to vertebrates. Annual Review of Neuroscience 8:233–261. https://doi.org/10.1146/annurev.ne.08.030185.001313
Harris, L. J. 1989. Footedness in parrots: Three centuries of research, theory, and mere surmise. Canadian Journal of Psychology / Revue canadienne de psychologie 43(3):369–396. https://doi.org/10.1037/h0084228
Harvey, C. B., Ellis, C., and Tate, M. 1976. Inhibition of the righting reflex in the common bullfrog (Rana catespbeiana) employing an operant-avoidance procedure. Bulletin of the Psychonomic Society 7:57–58. https://doi.org/10.3758/BF03337120
Hughes, A. 1976. Metamorphic changes in the brain and spinal cord; 856–863. in: Frog Neurobiology, edited by Llinas, R. and Precht, W. Berlin: Springer-Verlag. https://doi.org/10.1007/978-3-642-66316-1_30
Ingle, D. J. 1976. The visual system; 421–441 in: Physiology of the Amphibians, edited by Lofts, B. New York: Academic Press.
Iordansky, N. N. 1990. Evolution of complex adaptations: jaw apparatus of amphibians and reptiles. Moscow: Nauka.
Izvekov, E. I., Pavlova, V. V., Ognevaja, E. M., Nepomnyashchikh, V. A., and Malashichev, Y. B. 2018. Pattern of lateralized behaviors in a caudate amphibian, Ambystoma mexicanum. Russian Journal of Herpetology 25(1):31–42.
Jones, R. B. and Faure, J. M. 1981. Sex and strain comparisons of tonic immobility (“righting time”) in the domestic fowl and the effects of various methods of induction. Behavioural Processes 6:47–55. https://doi.org/10.1016/0376-6357(81)90015-2
Klemm, W. R. 1977. Identity of sensory and motor systems that are critical to the immobility reflex (animal hypnosis). Psychological Record 27:145–159. https://doi.org/10.1002/jnr.490020108
Kostylev, M. A. and Malashichev, Y. 2007. Correlation of the shoulder girdle asymmetry with the limb skeleton asymmetry in Xenopus laevis. Doklady Biological Sciences 416(1):374–376. https://doi.org/10.1134/S0012496607050146
Lapin, I. P., Oxenkrug, G. F., Osipova, S. V., and Uskova, N. V. 1970. The frog as a subject for screening thymoleptic drugs. Journal of Pharmacy and Pharmacology 22(10):781–782. https://doi.org/10.1111/j.2042-7158.1970.tb08429.x
Lippolis, G., Bisazza, A., Rogers, L. J., and Vallortigara, G. 2002. Lateralization of predator avoidance responses in three species of toads. Laterality 7(2):163–183. https://doi.org/10.1080/13576500143000221
Malashichev, Y. B. 2002. Asymmetries in amphibians: A review of morphology and behaviour. Laterality 7(3):197–217. https://doi.org/10.1080/13576500244000030
Malashichev, Y. B. 2006a. One-sided limb preference is linked to alternating-limb locomotion in anuran amphibians. Journal of Comparative Psychology 120(4):401–410. https://doi.org/10.1037/0735-7036.120.4.401
Malashichev, Y. B. 2006b. Is there a link between visceral and neurobehavioral asymmetries in development and evolution?; 33–44 in: Behavioral and Morphological Asymmetries in Veretbrates, edited by Malashichev, Y. B. and Deckel, W. Georgetown, TX: Landes Bioscience Malashichev, Y. B. 2016. Asymmetry of righting reflexes in sea turtles and its behavioral correlates. Physiology and Behavior 157:1–8. https://doi.org/10.1016/j.physbeh.2016.01.001
Malashichev, Y. B. and Nikitina, N. G. 2002. Preferential limb use in relation to epicoracoid overlap in the shoulder girdle of toads. Laterality 7(1):1–18. https://doi.org/10.1080/13576500143000032
Malashichev, Y. B. and Rogers, L. J. 2002. Behavioural and Morphological Asymmetries in Amphibians and Reptiles: Psychology Press Ltd.
Malashichev, Y. B. and Wassersug, R. J. 2004. Left and right in the amphibian world: which way to develop and where to turn? BioEssays 26(5):512–522. https://doi.org/10.1002/bies.20036
Markel, P. D., DeFries, J. C., and Johnson, T. E. 1995. Use of repeated measures in an analysis of ethanol-induced loss of righting reflex in inbred long-sleep and short-sleep mice. Alcoholism Clinical and Experimental Research 19:299–304. https://doi.org/10.1111/j.1530-0277.1995.tb01506.x
Mason, A. M., Wolfe, L. D., and Johnson, J. C. 1995. Hand preference in the sifaka (Propithecus verreauxi coquereli) during feeding in captivity. Primates 36:275–280. https://doi.org/10.1007/BF02381353
McGrew, W. C. and Marchant, L. F. 1992. Chimpanzees, tools, and termites: hand preference of handedness? Current Anthropology 33:114–119. https://doi.org/10.1086/204041
Mead, L. A. and Hampson, E. 1996. A sex difference in turning bias in humans. Behavioural Brain Research 78:73–79. https://doi.org/10.1016/0166-4328(95)00233-2
Murphy, J. B. 1976. Pedal luring in the leptodactylid frog, Ceratophrys calcarata Boulenger. Herpetologica 32(3):339–341.
Naitoh, T. and Wassersug, R. J. 1996. Why are toads right-handed? Nature 380:30–31. https://doi.org/10.1038/380030b0
Nekaris, K. A. I. and Tab Rasmussen, D. 2003. Diet and feeding behavior of mysore slender lorises. International Journal of Primatology 24(1):33–46. https://doi.org/10.1023/A:1021442411455
Nordlander, R. H., Baden, S. T., and Ryba, T. 1985. Development of early brainstem projections to the tail spinal cord of Xenopus. Journal of Comparative Neurology 231:519–529. https://doi.org/10.1002/cne.902310409
Oseen, K. L., Newhook, L. K. D., and Wassersug, R. J. 2001. Turning bias in Woodfrog (Rana sylvatica) tadpoles. Herpetologica 57(4):432–437.
Pellis, S. M., Pellis, V. C., Morrissey, T. K., and Teitelbaum, P. 1989. Visual modulation of vestibularly-triggered air-righting in the rat. Behavioural Brain Research 74:207–211. https://doi.org/10.1016/S0166-4328(89)80004-X
Radcliffe, C. W., Chiszar, D., Estep, K., Murphy, J. B., and Smith, H. M. 1986. Observations on pedal luring and pedal movements in leptodactylid frogs. Journal of Herpetology 20:300–306. https://doi.org/10.2307/1564496
Reilly, S. M., Essner, R., Wren, S., Easton, L., and Bishop, P. J. 2015. Movement patterns in leiopelmatid frogs: insights into the locomotor repertoire of basal anurans. Behavioural Processes 121:43–53. https://doi.org/10.1016/j.beproc.2015.10.001
Reilly, S. M., Montuelle, S. J., Schmidt, A., Naylor, E., Jorgensen, M. E., Halsey, L. G., and Essner, R. J. 2015. Conquering the world in leaps and bounds: hopping locomotion in toads is actually bounding. Functional Ecology 29(10):1308–1316. https://doi.org/10.1111/1365-2435.12414
Requintina, P. J., Oxenkrug, G. F., Yuwiler, A., and Oxenkrug, A. G. 1994. Synergistic sedative effect of selective MAO-A, but no MAO-B, inhibitors and melatonin in frogs. Journal of Neural Transmission (Suppl) 41:141–144. https://doi.org/10.1007/978-3-7091-9324-2_19
Richter, J. A., Harris, P. S., and Hanford, P. V. 1982. Similar development of tolerance to barbital-induced inhibition of avoidance behavior and loss of righting reflex in rats. Pharmacology, Biochemistry and Behavior 16:467–471. https://doi.org/10.1016/0091-3057(82)90454-3
Robins, A. 2002. Visual ad motor lateralization in two anuran species, Bufo marinus and Litoria caerulea. Ph. D. Research Thesis, University of New England, Armidale, Australia.
Robins, A. and Rogers, L. J. 2002. Limb preference and skeletal asymmetry in the cane toad, Bufo marinus (Anura: Bufonidae). Laterality 7(3):261–275. https://doi.org/10.1080/13576500244000049
Robins, A., Lippolis, G., Bisazza, A., Vallortigara, G., and Rogers, L. J. 1998. Lateralized agonistic responses and hind-limb use in toads. Animal Behaviour 56(4):875–881. https://doi.org/10.1006/anbe.1998.0877
Rogers, L. J. 1991. Development of brain lateralization; 507–535 in: Neural and behavioural plasticity: The use of the chick as a model, edited by Andrew, R. J. Oxford: Oxford University Press.
Rogers, L. J. 2002. Lateralised brain function in anurans: comparison to lateralisation in other vertebrates. Laterality 7(3):219–239. https://doi.org/10.1080/13576500244000012
Rogers, L. J. and Workman, L. 1993. Footedness in birds. Animal Behaviour 45:409–411. https://doi.org/10.1006/anbe.1993.1049
Rogers, L. J., Ward, J. P., and Stanford, D. 1994. Eye dominance in the small-eared bushbaby, Otolemur garnettii. Neuropsychologia 32(2):257–264. https://doi.org/10.1016/0028-3932(94)90011-6
Rutledge, R. and Hunt, G. R. 2004. Lateralized tool use in wild New Caledonian crows. Animal Behaviour 67:327–332. https://doi.org/10.1016/j.anbehav.2003.07.002
Singh, I. 1971. One-sided dominance in the limbs of rabbits and frogs, as evidenced by asymmetry in bone weight. Journal of Anatomy 109:271–275.
Sovrano, V. A. 2007. A note on asymmetric use of the forelimbs during feeding in the European green toad (Bufo viridis). Laterality 12(5):458–463. https://doi.org/10.1080/13576500701479822
Stehouwer, D. J. 1986. Behavior of larval and juvenile bullfrogs (Rana catesbeiana) following chronic spinal transection. Behavioral and Neural Biology 45:120–134. https://doi.org/10.1016/S0163-1047(86)80011-5
Sullivan, R. A. 2018. Handedness is not linked to locomotion in a basal anuran (ProQuest No. 10808549). Master Thesis, Southern Illinois University, Edwardsville.
Taylor, G. M., Nol, E., and Boire, D. 1995. Brain regions and encephalization in anurans: adaptations or stability? Brain, Behaviour and Evolution 45:96–109. https://doi.org/10.1159/000113543
Tommasi, L. and Vallortigara, G. 1998. Footedness in binocular and monocular chicks. Laterality 4:89–95. https://doi.org/10.1080/713754325
Uziel, D., Lopesconceicao, M. C., Luiz, R. R., and Lent, R. 1996. Lateralization of rotational behavior in developing and adult hamsters. Behavioural Brain Research 75:169–177. https://doi.org/10.1016/0166-4328(96)00205-7
Uziel, D., Lopesconceicao, M. C., Simpson, D., and Lent, R. 1998. Ontogenesis of lateralized rotational behavior in hamsters — a time series study. Behavioural Brain Research 92:47–53. https://doi.org/10.1016/S0166-4328(97)00122-8
Vallortigara, G. and Bisazza, A. 2002. How ancient is brain lateralization?; 9–69 in: Comparative vertebrate lateralization, edited by Rogers, L. J. and Andrew, R. J. Cambridge: Cambridge University Press.
Walton, B. M., Peterson, C. C., and Bennett, A. F. 1994. Is walking costly for anurans? The energetic cost of walking in the Northern toad Bufo boreas halophilus. Journal of Experimental Biology 197:165–178.
Ward, J. P., Milliken, G. W., and Stafford, D. K. 1993. Patterns of lateralized behavior in prosimians; 43–74. in: Primate Laterality: Current Behavioral Evidence of Primate Asymmetries, edited by Ward, J. P. and Hopkins, W. D. New York: Springer Verlag. https://doi.org/10.1007/978-1-4612-4370-0_2
Wassersug, R. J. and Yamashita, M. 2002. Assessing and interpreting lateralized behaviours in anuran larvae. Laterality 7(3):241–260. https://doi.org/10.1080/13576500244000003
Wassersug, R. J., Naitoh, T., and Yamashita, M. 1999. Turning bias in tadpoles. Journal of Herpetology 33(4):543–548. https://doi.org/10.2307/1565570
Weldon, P. J. and Hoffman, D. L. 1975. Unique form of tool-using in two gastropod molluscs (Trochidae). Nature 256:720–721. https://doi.org/10.1038/256720a0
Will, U. 1986. Mauthner neurons survive metamorphosis in anurans: A comparative HRP study on the cytoarchitecture of Mauthner neurons in amphibians. The Journal of Comparative Neurology 244(1):111–120. https://doi.org/10.1002/cne.902440109
Will, U. 1991. Amphibian Mauthner cells. Brain, Behaviour and Evolution 37:317–332. https://doi.org/10.1159/000114368
Yamashita, M., Naitoh, T., and Wassersug, R. J. 2000. Startle response and turning bias in Microhyla tadpoles. Zoological Sceince 17:185–189. https://doi.org/10.2108/zsj.17.185
Downloads
Published
2019-03-26
How to Cite
Malashichev, Y., & Robins, A. (2019). Lateralized motor responses in anuran amphibians — an overview of methods and perspectives of studies. Biological Communications, 63(4), 210–242. https://doi.org/10.21638/spbu03.2018.402
License
Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.
