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Sensory-evoked turning locomotion in red-eared turtles: kinematic analysis and electromyography

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Abstract

We examined the limb kinematics and motor patterns that underlie sensory-evoked turning locomotion in red-eared turtles. Intact animals were held by a band-clamp in a water-filled tank. Turn-swimming was evoked by slowly rotating turtles to the right or left via a motor connected to the shaft of the band-clamp. Animals executed sustained forward turn-swimming against the direction of the imposed rotation. We recorded video of turn-swimming and computer-analyzed the limb and head movements. In a subset of turtles, we also recorded electromyograms from identified limb muscles. Turning exhibited a stereotyped pattern of (1) coordinated forward swimming in the hindlimb and forelimb on the outer side of the turn, (2) back-paddling in the hindlimb on the inner side, (3) a nearly stationary, “braking” forelimb on the inner side, and (4) neck bending toward the direction of the turn. Reversing the rotation caused animals to switch the direction of their turns and the asymmetric pattern of right and left limb activities. Preliminary evidence suggested that vestibular inputs were sufficient to drive the behavior. Sensory-evoked turning may provide a useful experimental platform to examine the brainstem commands and spinal neural networks that underlie the activation and switching of different locomotor forms.

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Abbreviations

BP:

Back-paddle

EE:

Elbow extensor

EMG:

Electromyogram

FS:

Forward swim

HP:

Hip protractor

HR:

Hip retractor

KE:

Knee extensor

SP:

Shoulder protractor

SR:

Shoulder retractor

References

  • Ashley LM (1955) Laboratory anatomy of the turtle. WC Brown Co, Dubuque, pp 12–17

    Google Scholar 

  • Avens L, Wang JH, Johnsen S, Dukes P, Lohmann KJ (2003) Responses of hatchling sea turtles to rotational displacements. J Exp Mar Biol Ecol 288:111–124

    Article  Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic Press, New York

    Google Scholar 

  • Bell WJ, Schal C (1980) Patterns of turning in courtship orientation of the male German cockroach. Anim Behav 28:86–94

    Article  Google Scholar 

  • Berkowitz A, Stein PSG (1994) Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses. J Neurosci 14:5105–5119

    CAS  PubMed  Google Scholar 

  • Carr A (1952) Handbook of turtles. Cornell University Press, Ithaca

    Google Scholar 

  • Cruse H, Silva Saavedra MG (1996) Curve walking in crayfish. J Exp Biol 199:1477–1482

    PubMed  Google Scholar 

  • Currie SN (2003) Fictive locomotion evoked by electrical stimulation of the brainstem in decerebrate immobilized turtles. Soc Neur Abstr 29

  • Davenport J, Munks SA, Oxford PJ (1984) A comparison of swimming in marine and freshwater turtles. Proc R Soc Lond B Biol Sci 220:447–475

    Article  Google Scholar 

  • Earhart GM, Stein PSG (2000) Step, swim and scratch motor patterns in the turtle. J Neurophysiol 84:2181–2190

    CAS  PubMed  Google Scholar 

  • Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, Ullen F (2001) Lateral turns in the lamprey. II. Activity of reticulospinal neurons during generation of fictive turns. J Neurophysiol 86:2257–2265

    CAS  PubMed  Google Scholar 

  • Fan TX, Scudder C, Ariel M (1997) Neuronal responses to turtle head rotation in vitro. J Neurobiol 33:99–117

    Article  CAS  PubMed  Google Scholar 

  • Field EC, Stein PSG (1997a) Spinal cord coordination of hindlimb movements in the turtle: intralimb temporal relationships during scratching and swimming. J Neurophysiol 78:394–1403

    Google Scholar 

  • Field EC, Stein PSG (1997b) Spinal cord coordination of hindlimb movements in the turtle: interlimb temporal relationships during bilateral scratching and swimming. J Neurophysiol 78:1404–1413

    CAS  PubMed  Google Scholar 

  • Fish FE, Nicastro AJ (2003) Aquatic turning performance by the whirligig beetle: constraints on maneuverability by a rigid biological system. J Exp Biol 206:1649–1656

    Article  PubMed  Google Scholar 

  • Gillis GB, Blob RW (2001) How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates. Comp Biochem Physiol A Physiol 131:61–75

    Article  CAS  Google Scholar 

  • Gray J (1933) Directional control of fish movement. Proc R Soc Lond B 113:115–125

    Article  Google Scholar 

  • Gruhn M, Zehl L, Büschges A (2009) Straight walking and turning on a slippery surface. J Exp Biol 212:194–209

    Article  PubMed  Google Scholar 

  • Herrel A, Van Damme J, Aerts P (2007) Cervical anatomy and function in turtles. In: Wyneken J, Godfrey MH, Bels V (eds) Biology of turtles. CRC Press, Boca Raton, pp 163–185

    Chapter  Google Scholar 

  • Jones MS, Ariel M (2008) Morphology, intrinsic membrane properties, and rotation-evoked responses of trochlear motoneurons in the turtle. J Neurophysiol 99:1187–1200

    Article  PubMed  Google Scholar 

  • Juranek J, Currie SN (2000) Electrically evoked fictive swimming in the low-spinal immobilized turtle. J Neurophysiol 83:146–155

    CAS  PubMed  Google Scholar 

  • Land MF (1972) Stepping movements made by jumping spiders during turns mediated by the lateral eyes. J Exp Biol 57:15–40

    CAS  PubMed  Google Scholar 

  • Lennard PR, Stein PSG (1977) Swimming movements elicited by electrical stimulation of the turtle spinal cord. I. Low-spinal and intact preparations. J Neurophysiol 40:768–778

    CAS  PubMed  Google Scholar 

  • Lohmann KJ, Swartz AW, Lohmann CMF (1995) Perception of ocean wave direction by sea turtles. J Exp Biol 198:1079–1085

    PubMed  Google Scholar 

  • Marcus LC (1981) Veterinary biology and medicine of captive amphibians and reptiles. Lea and Febiger, Philadelphia

    Google Scholar 

  • Mardia KV, Jupp PE (2000) Directional statistics, 2nd edn. Wiley, New York

    Google Scholar 

  • McClellan AD (1984) Descending control and sensory gating of ‘fictive’ swimming and turning responses elicited in an in vitro preparation of the lamprey brainstem/spinal cord. Brain Res 302:151–162

    Article  CAS  PubMed  Google Scholar 

  • McClellan AD, Grillner S (1983) Initiation and sensory gating of ‘fictive’ swimming and withdrawal responses in an in vitro preparation of the lamprey spinal cord. Brain Res 269:237–250

    Article  CAS  PubMed  Google Scholar 

  • McClellan AD, Hagevik A (1997) Descending control of turning locomotor activity in larval lamprey: neurophysiology and computer modeling. J Neurophysiol 78:214–228

    CAS  PubMed  Google Scholar 

  • Mu L, Ritzmann RE (2005) Kinematics and motor activity during tethered walking and turning in the cockroach, Blaberus discoidalis. J Comp Physiol A 191:1037–1054

    Article  Google Scholar 

  • Pace CM, Blob RW, Westneat MW (2001) Comparative kinematics of the forelimb during swimming in red-eared slider (Trachemys scripta) and spiny softshell (Apalone spinifera) turtles. J Exp Biol 204:3261–3271

    CAS  PubMed  Google Scholar 

  • Renous S, Bels V (1993) Comparison between aquatic and terrestrial locomotion of the leatherback sea turtle (Dermochelys coriacea). J Zool Lond 230:357–378

    Article  Google Scholar 

  • Rivera ARV, Blob RW (2010) Forelimb kinematics and motor patterns of the slider turtle (Trachemys scripta) during swimming and walking: shared and novel strategies for meeting locomotor demands of water and land. J Exp Biol 213:3515–3526

    Article  PubMed Central  PubMed  Google Scholar 

  • Rivera G, Rivera ARV, Dougherty EE, Blob RW (2006) Aquatic turning performance of painted turtles (Chrysemys picta) and functional consequences of rigid body design. J Exp Biol 209:4203–4213

    Article  PubMed  Google Scholar 

  • Saitoh K, Menard A, Grillner S (2007) Tectal control of locomotion, steering, and eye movements in lamprey. J Neurophysiol 97:3093–3108

    Article  PubMed  Google Scholar 

  • Samara RF, Currie SN (2007) Crossed commissural pathways in the spinal hindlimb enlargement are not necessary for right-left hindlimb alternation during turtle swimming. J Neurophysiol 98:2223–2231

    Article  PubMed  Google Scholar 

  • Samara RF, Currie SN (2008a) Electrically evoked locomotor activity in the turtle spinal cord hemi-enlargement preparation. Neurosci Lett 441:105–109

    Article  CAS  PubMed  Google Scholar 

  • Samara RF, Currie SN (2008b) Location of spinal cord pathways that control hindlimb movement amplitude and interlimb coordination during voluntary swimming in turtles. J Neurophysiol 99:1953–1968

    Article  PubMed  Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Stein PSG (1978) Swimming movements elicited by electrical stimulation of the turtle spinal cord: the high spinal preparation. J Comp Physiol A 124:203–210

    Article  Google Scholar 

  • Strauß R, Heisenberg M (1990) Coordination of legs during straight walking and turning in Drosophila melanogaster. J Comp Physiol A 167:403–412

    Article  PubMed  Google Scholar 

  • Walker WF (1971a) A structural and functional analysis of walking in the turtle, Chrysemys picta marginata. J Morph 134:195–214

    Article  PubMed  Google Scholar 

  • Walker WF (1971b) Swimming in sea turtles of the family cheloniidae. Copeia 1971(2):229–233

    Article  Google Scholar 

  • Walker WF (1973) The locomotor apparatus of testudines. In: Gans C, Parsons TS (eds) Biology of the reptilia: morphology, vol 4. Academic Press, London, pp 1–100

    Google Scholar 

  • Welch DB (2011) Sensory-motor integration and control. Ph.D. thesis, University of California

  • Wyneken J (1996) Sea turtle locomotion: mechanisms, behavior, and energetics. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, New York, pp 165–198

    Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Zelenin PV (2005) Activity of individual reticulospinal neurons during different forms of locomotion in the lamprey. Eur J Neurosci 22:2271–2282

    Article  PubMed  Google Scholar 

  • Zelenin PV (2011) Reticulospinal neurons controlling forward and backward swimming in the lamprey. J Neurophysiol 105:1361–1371

    Article  CAS  PubMed  Google Scholar 

  • Zollikofer CPE (1994) Stepping pattern in ants. I. Influence of speed and curvature. J Exp Biol 192:95–106

    PubMed  Google Scholar 

  • Zolotov V, Frantsevich L, Falk E-M (1975) Kinematik der phototaktischen drehung bei der honigbiene Apis mellifera L. J Comp Physiol 97:339–353

    Article  Google Scholar 

Download references

Acknowledgments

We thank Basilio Haro and Clifford Jung Hun Kye for assistance with video digitization. All procedures were performed according to protocols approved by the UC Riverside Institutional Animal Care and Use Committee in accordance with federal guidelines. This research was supported by U.C.R. Academic Senate grants to S.N.C.

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Authors and Affiliations

  1. Department of Growth Development and Structure, Southern Illinois University, School of Dental Medicine, Alton, IL, 62002, USA

    Dan B. Welch

  2. Department of Cell Biology and Neuroscience, University of California, Riverside, CA, 92521, USA

    Scott N. Currie

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  1. Dan B. Welch
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  2. Scott N. Currie
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Correspondence to Scott N. Currie.

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Welch, D.B., Currie, S.N. Sensory-evoked turning locomotion in red-eared turtles: kinematic analysis and electromyography. J Comp Physiol A 200, 641–656 (2014). https://doi.org/10.1007/s00359-014-0908-0

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  • DOI: https://doi.org/10.1007/s00359-014-0908-0

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