Central Circuits Controlling Locomotion in Young Frog Tadpoles
ALAN ROBERTS
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Search for more papers by this authorS. R. SOFFE
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Search for more papers by this authorE. S. WOLF
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Present addresses:Department of Anatomy, Medical University, Debrecen, Hungary.
Search for more papers by this authorM. YOSHIDA
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Present addresses:Applied Biological Science, Hiroshima University, Higashi-Hiroshima, Japan.
Search for more papers by this authorF.-Y. ZHAO
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Search for more papers by this authorALAN ROBERTS
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Search for more papers by this authorS. R. SOFFE
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Search for more papers by this authorE. S. WOLF
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Present addresses:Department of Anatomy, Medical University, Debrecen, Hungary.
Search for more papers by this authorM. YOSHIDA
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Present addresses:Applied Biological Science, Hiroshima University, Higashi-Hiroshima, Japan.
Search for more papers by this authorF.-Y. ZHAO
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom
Search for more papers by this authorAbstract
Abstract: The young Xenopus tadpole is a very simple vertebrate that can swim. We have examined its behavior and neuroanatomy, and used immobilized tadpoles to study the initiation, production, coordination, and termination of the swimming motor pattern. We will outline the sensory pathways that control swimming behavior and the mainly spinal circuits that produce the underlying motor output. Our recent work has analyzed the glycinergic, glutamatergic, cholinergic, and electrotonic synaptic input to spinal neurons during swimming. This has led us to study the nonlinear summation of excitatory synaptic inputs to small neurons. We then analyzed the different components of excitation during swimming to ask which components control frequency, and to map the longitudinal distribution of the components along the spinal cord. The central axonal projection patterns of spinal interneurons and motoneurons have been defined in order to try to account for the longitudinal distribution of synaptic drive during swimming.
REFERENCES
- 1
Roberts, A.
1990. How does a nervous system produce behaviour? A case study in neurobiology.
Sci. Prog.
74: 1–51.
- 2
Roberts A. & J. D. W. Clarke.
1982. The neuroanatomy of an amphibian embryo spinal cord.
Philos. Trans. R. Soc. Lond. B
296: 195–212.
- 3
Soffe, S. R.
1991. Triggering and gating of motor responses by sensory stimulation: Behavioural selection in Xenopus embryos.
Proc. R. Soc. Lond. B
246: 197–203.
- 4
Roberts, A. & R. Perrins.
1996. Positive feedback as a general mechanism for sustaining rhythmic and non-rhythmic activity.
J. Physiol. (Paris)
89: 241–248.
- 5
Roberts, A. & K. T. Sillar.
1990. Characterisation and function of spinal excitatory interneurons with commissural projections in Xenopus laevis embryos.
Eur. J. Neurosci.
2: 1051–1062.
- 6
Zhao, F.-Y., B. G., Burton, E. S. Wolf & A. Roberts.
1998. Asymmetries in sensory pathways from skin to motoneurons on each side of the body determine the direction of an avoidance response in hatchling Xenopus tadpoles.
J. Physiol.
506: 471–487.
- 7
Dale, N., A. Roberts, O. P. Ottersen & J. Storm-Mathisen.
1987. The morphology and distribution of “Kolmer-Agduhr cells” a class of cerebrospinal fluid-contacting neurons revealed in the frog spinal cord by GABA immunocytochemistry.
Proc. R. Soc. Lond. B
232: 193–203.
- 8
Jamieson, D.
1997a. Synaptic transmission in the pineal eye of young Xenopus laevis tadpoles: A role for NMDA and non-NMDA glutamate and non-glutaminergic receptors.
J. Comp. Physiol. A
181: 177–186.
- 9
Jamieson, D. A. 1997b. The pineal eye of Xenopus laevis tadpoles: A behavioural, anatomical and physiological study of an extraretinal photosensory system. Ph.D. thesis, University of Bristol, Bristol, UK.
- 10
Roberts, A.
1996. Trigeminal pathway for the skin impulse to initiate swimming in hatchling Xenopus embryos.
J. Physiol.
493P: 40–41P.
- 11
Boothby, K. M. & A. Roberts.
1992. The stopping response of Xenopus laevis embryos: Pharmacology and intracellular physiology of rhythmic spinal neurons and hindbrain neurons.
J. Exp. Biol.
169: 65–86.
- 12
Woolston, A.-M., J. F. S. Wedderburn & K. T. Sillar.
1994. Descending serotonergic spinal projections and modulation of locomotor rhythmicity in Rana temporaria embryos.
Proc. R. Soc. Lond. B
255: 73–79.
- 13
Dale, N.
1995a. Kinetic characterization of the voltage-gated currents possessed by Xenopus embryo spinal neurons.
J. Physiol.
489: 473–488.
- 14
Scrymgeour-Wedderburn, J. F., C. A. Reith & K. T. Sillar.
1997. Voltage oscillations in Xenopus spinal neurons: Developmental onset and dependence on co-activation of NMDA and 5HT receptors.
Eur. J. Neurosci.
9: 1473–1482.
- 15
Roberts, A., S. R. Soffe & R. Perrins. 1997. Spinal networks controlling swimming in hatchling Xenopus tadpoles. In Neurons, Networks and Motor Behaviour. P. S. G. Stein, S. Grillner, A. I. Selverston & D. G. Stuart, Eds.: 83-89. MIT Press. Boston, MA.
- 16
Arshavsky, Yu., G. N. Orlovsky, Yu. V. Panchin, A. Roberts & S. R. Soffe.
1993. Neuronal control of swimming locomotion: Analysis of the pteropod mollusc Clione and embryos of the amphibian Xenopus.
Trends Neurosci.
16: 227–233.
- 17
Soffe, S. R.
1989. Roles of glycinergic inhibition and N-methyl-d-aspartate receptor-mediated excitation in the locomotor rhythmicity of one half of the Xenopus embryo CNS.
Eur. J. Neurosci.
1: 561–571.
- 18
Roberts, A. & M. J. Tunstall.
1990. Mutual-reexcitation with post-inhibitory rebound: A simulation study on the mechanisms for locomotor rhythm generation in the spinal cord of Xenopus embryos.
Eur. J. Neurosci.
2: 11–23.
- 19
Roberts, A., M. J. Tunstall & E. W. Wolf.
1995. Properties of networks controlling locomotion in a simple vertebrate and significance of voltage-dependency of NMDA channels: A simulation study of rhythm generation sustained by positive feedback.
J. Neurophysiol.
73: 485–496.
- 20
Dale, N.
1995b. Experimentally derived model for the locomotor pattern generator in the Xenopus embryo.
J. Physiol.
489: 489–510.
- 21
Dale, N. & F. M. Kuenzi.
1997. Ion channels and the control of swimming in the Xenopus embryo.
Prog. Neurobiol.
53: 729–756.
- 22
Perrins, R. & A. Roberts.
1995a. Cholinergic and electrical motoneuron-to-motoneuron synapses contribute to on-cycle excitation during swimming in Xenopus embryos.
J. Neurophysiol.
73: 1013–1019.
- 23
Perrins, R. & A. Roberts.
1995b. Cholinergic contribution to excitation in a spinal locomotor central pattern generator in Xenopus embryos.
J. Neurophysiol.
73: 1005–1012.
- 24
Perrins, R. & A. Roberts.
1995c. Cholinergic and electrical synapses between synergistic spinal motoneurones in the Xenopus laevis embryo.
J. Physiol.
485: 135–144.
- 25
Dale, N. & D. Gilday.
1996. Regulation of rhythmic movements by purinergic neurotransmitters in frog embryos.
Nature
383: 259–263.
- 26
Sillar, K.T. & A. Roberts.
1993. Control of frequency during swimming in Xenopus embryos: A study on interneuronal recruitment in a spinal rhythm generator.
J. Physiol.
472: 557–572.
- 27
Burke, R. E. 1981. Motor units: Anatomy, physiology and functional organization. In Handbook of Physiology, Section 1. The Nervous System, Vol. 2. Motor Control. V. Brooks, Ed.: 345-422. American Physiological Society. Waverly Press. Bethesda, MD.
- 28
Kernell, D. 1983. Functional properties of spinal motoneurons and gradation of muscle force. In Advances in Neurology 39, Motor Control in Health and Disease. J. E. Desmedt, Ed.: 213-26. Raven Press. New York.
- 29
Zhao, F.-Y. & A. Roberts. 1996. Antagonists unmask components of excitatory synaptic drive to motoneurons during swimming in Xenopus tadpoles. Abstract for 26th Annual Meeting of Society for Neuroscience, Washington, DC.
- 30
Tunstall, M. J. & A. Roberts.
1991. Longitudinal coordination of motor output during swimming in Xenopus embryos.
Proc. R. Soc. Lond. B
244: 27–32.
- 31
Tunstall, M. J. & K. T. Sillar.
1993. Physiological and developmental aspects of intersegmental coordination in Xenopus embryos and tadpoles.
Semin. Neurosci.
5: 29–40.
- 32
Roberts, A. & M. J. Tunstall.
1994. Longitudinal gradients in the spinal cord of Xenopus embryos and their possible role in coordination of swimming.
Eur. J. Morphol.
32: 176–184.
- 33
Tunstall, M. J. & A. Roberts.
1994. A longitudinal gradient of synaptic drive in the spinal cord of Xenopus embryos and its role in coordination of swimming.
J. Physiol.
474: 393–405.
- 34
Perrins, R. & S. R. Soffe.
1996. Composition of the excitatory drive for swimming in two amphibian embryos: Rana and Bufo.
J. Comp. Physiol.
179: 563–573.
- 35
Wolf, E., F.-Y. Zhao & A. Roberts.
1997. A simple model predicts the non-linearity in summation of postsynaptic potentials and the chemical synaptic and gap junctional conductances in spinal motoneurons of young Xenopus tadpoles.
J. Physiol.
505P: 182–183P.
- 36
Zhao, F.-Y., E. Wolf & A. Roberts.
1997. Non-linear summation of chemically mediated post-synaptic potentials in the motoneurons of Xenopus tadpoles.
J. Physiol.
505P: 182P.
- 37
Roberts, A. & A. Walford.
1996. Central synapses of spinal motoneurons innervating the trunk swimming muscles of Xenopus laevis embryos.
Acta Biol. Hungarica
47: 371–384.
- 38
Roberts, A., N. Dale, O. P. Ottersen & J. Storm-Mathisen.
1988. Development and characterization of commissural interneurons in the spinal cord of Xenopus laevis embryos revealed by antibodies to glycine.
Development
103: 447–461.
- 39
Yoshida, M., A. Roberts & S. R. Soffe.
1997. Axon projections of reciprocal inhibitory interneurons in the spinal cord of young Xenopus tadpoles and implications for the pattern of inhibition during swimming.
J. Physiol.
505P: 117P.
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