Reconfiguration of a vertebrate motor network: Specific neuron recruitment and context-dependent synaptic plasticity

Journal of Neuroscience

Volumn 27, Issue 45, 2007, Pages 12267-12276

  Li, Wen Chang ^a   Sautois, Bart ^b   Roberts, Alan ^a   Soffe, Stephen R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Inhibition; Interneurons; Modeling; Switching; Synaptic depression; Xenopus

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HYPOTHESIS; INTERNEURON; LIMB MOVEMENT; MOTONEURON; MOTOR COORDINATION; MOTOR NERVE; MOTOR PERFORMANCE; MUSCULOSKELETAL SYSTEM; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; SENSORIMOTOR FUNCTION; SKIN STIMULATION; SPINAL CORD; SWIMMING; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; TADPOLE; VERTEBRATE; XENOPUS;

ANIMALS; MOTOR NEURONS; NERVE NET; NEURONAL PLASTICITY; NEURONS; RECRUITMENT, NEUROPHYSIOLOGICAL; SYNAPSES; XENOPUS;

EID: 36048989924     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3694-07.2007     Document Type: Article

References (58)

1. Aiken SP, Kuenzi FM, Dale N (2003) Xenopus embryonic spinal neurons recorded in situ with patch-clamp electrodes - conditional oscillators after all? Eur J Neurosci 18:333-343.
2. Bekoff A, Nusbaum MP, Sabichi AL, Clifford M (1987) Neural control of limb coordination. I. Comparison of hatching and walking motor output patterns in normal and deafferented chicks. J Neurosci 7:2320-2330.
3. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390-393.
4. Berkinblit MB, Deliagina TG, Feldman AG, Gelfand IM, Orlovsky GN (1978) Generation of scratching. II. Nonregular regimes of generation. J Neurophysiol 41:1058-1069.
5. Berkowitz A (2002) Both shared and specialized spinal circuitry for scratching and swimming in turtles. J Comp Physiol 188:225-234.
6. Berkowitz A (2005) Physiology and morphology indicate that individual spinal interneurons contribute to diverse limb movements. J Neurophysiol 94:4455-4470.
7. Berkowitz A (2007) Spinal interneurons that are selectively activated during fictive flexion reflex. J Neurosci 27:4634-4641.
8. Bhatt DH, McLean DL, Hale ME, Fetcho JR (2007) Grading movement strength by changes in firing intensity versus recruitment of spinal interneurons. Neuron 53:91-102.
9. Briggman KL, Kristan Jr WB (2006) Imaging dedicated and multifunctional neural circuits generating distinct behaviors. J Neurosci 26:10925-10933.
10. Brown TG (1911) The intrinsic factor in the act of progression of the mammal. Proc R Soc Lond B Biol Sci 84:308-319.
11. Brown TG (1914) On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J Physiol (Lond) 48:18-46.
12. Buchanan JT (1999) The roles of spinal interneurons and motoneurons in the lamprey locomotor network. Prog Brain Res 123:311-321.
13. Buchanan JT, Grillner S (1987) Newly identified "glutamate interneurons" and their role in locomotion in the lamprey spinal cord. Science 236:312-314.
14. Budick SA, O'Malley DM (2000) Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. J Exp Biol 203:2565-2579.
15. Carter MC, Smith JL (1986) Simultaneous control of two rhythmical behaviors. I. Locomotion with paw-shake response in normal cat. J Neurophysiol 56:171-183.
16. Clarke JDW, Hayes BP, Hunt SP, Roberts A (1984) Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis. J Physiol (Lond) 348:511-525.
17. Currie SN, Stein PS (1989) Interruptions of fictive scratch motor rhythms by activation of cutaneous flexion reflex afferents in the turtle. J Neurosci 9:488-496.
18. Dale N (1985) Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. J Physiol (Lond) 363:61-70.
19. el Manira A, Tegner J, Grillner S (1994) Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72:1852-1861.
20. Feldman JL, Del Negro CA (2006) Looking for inspiration: new perspectives on respiratory rhythm. Nature Revs Neurosci 7:232-242.
21. Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185-204.
22. Getting PA, Dekin MS (1985) Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator. J Neurophysiol 53:466-480.
23. Grillner S, Wallen P, Brodin L, Lansner A (1991) Neuronal network generating locomotor behavior in lamprey: circuitry, transmitters, membrane properties, and simulation. Ann Rev Neurosci 14:169-199.
24. Hellgren J, Grillner S, Lansner (1992) A computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol Cybern 68:1-13.
25. Jing J, Weiss KR (2002) Interneuronal basis of the generation of related but distinct motor programs in Aplysia: implications for current neuronal models of vertebrate intralimb coordination. J Neurosci 22:6228-6238.
26. Kahn JA, Roberts A (1982) The neuromuscular basis of rhythmic struggling movements in embryos of Xenopus laevis. J Exp Biol 99:197-205.
27. Kahn JA, Roberts A, Kashin SM (1982) The neuromuscular basis of swimming movements in embryos of the amphibian Xenopus laevis. J Exp Biol 99:175-184.
28. Kimura Y, Okamura Y, Higashijima S (2006) alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J Neurosci 26:5684-5697.
29. Kosmidis EK, Pierrefiche O, Vibert JF (2004) Respiratory-like rhythmic activity can be produced by an excitatory network of non-pacemaker neuron models. J Neurophysiol 92:686-699.
30. Li WC, Perrins R, Soffe SR, Yoshida M, Walford A, Roberts A (2001) Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles. J Comp Neurol 441:248-265.
31. Li WC, Soffe SR, Roberts A (2002) Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J Neurosci 22:10924-10934.
32. Li WC, Soffe SR, Roberts A (2003) The spinal interneurons and properties of glutamatergic synapses in a primitive vertebrate cutaneous flexion reflex. J Neurosci 23:9068-9077.
33. Li WC, Soffe SR, Roberts A (2004a) Dorsal spinal interneurons forming a primitive, cutaneous sensory pathway. J Neurophysiol 92:895-904.
34. Li WC, Soffe SR, Roberts A (2004b) Glutamate and acetylcholine corelease at developing synapses. Proc Natl Acad Sci USA 101:15488-15493.
35. Li WC, Soffe SR, Roberts A (2004c) A direct comparison of whole cell patch and sharp electrodes by simultaneous recording from single spinal neurons in frog tadpoles. J Neurophysiol 92:380-386.
36. Li WC, Higashijima S, Parry DM, Roberts A, Soffe SR (2004d) Primitive roles for inhibitory interneurons in developing frog spinal cord. J Neurosci 24:5840-5848.
37. Li WC, Soffe SR, Wolf E, Roberts A (2006) Persistent responses to brief stimuli: feedback excitation among brainstem neurons. J Neurosci 26:4026-4035.
38. Lieske SP, Thoby-Brisson M, Telgkamp P, Ramirez JM (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps [see comment]. Nat Neurosci 3:600-607.
39. Marder E, Bucher D, Schulz DJ, Taylor AL (2005) Invertebrate central pattern generation moves along. Curr Biol 15:R685-R698.
40. McLean DL, Fan J, Higashijima S, Hale ME, Fetcho JR (2007) A topographic map of recruitment in spinal cord. Nature 446:71-75.
41. Meyrand P, Simmers J, Moulins M (1991) Construction of a pattern-generating circuit with neurons of different networks. Nature 351:60-63.
42. Mortin LI, Stein PS (1989) Spinal cord segments containing key elements of the central pattern generators for three forms of scratch reflex in the turtle. J Neurosci 9:2285-2296.
43. Popescu IR, Frost WN (2002) Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22:1985-1993.
44. Ritter DA, Bhatt DH, Fetcho JR (2001) In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J Neurosci 21:8956-8965.
45. Roberts A, Walford A, Soffe SR, Yoshida M (1999) Motoneurons of the axial swimming muscles in hatchling Xenopus tadpoles: features, distribution, and central synapses. J Comp Neurol 411:472-486.
46. Sautois B, Soffe SR, Li W-C, Roberts A (2007) Role of type-specific neuron properties in a spinal cord motor network. J Comput Neurosci 23:59-77.
47. Sillar KT, Wedderburn JF, Simmers AJ (1991) The development of swimming rhythmicity in post-embryonic Xenopus laevis. Proc R Soc Lond B Biol Sci 246:147-153.
48. Sillar KT, Wedderburn JF, Simmers AJ (1992) Modulation of swimming rhythmicity by 5-hydroxytryptamine during post-embryonic development in Xenopus laevis. Proc R Soc Lond B Biol Sci 250:107-114.
49. Soffe SR (1990) Active and passive membrane properties of spinal cord neurons that are rhythmically active during swimming in Xenopus embryos. Eur J Neurosci 2:1-10.
50. Soffe SR (1991) Triggering and gating of motor responses by sensory stimulation: behavioural selection in Xenopus embryos. Proc R Soc Lond B Biol Sci 246:197-203.
51. Soffe SR (1993) Two distinct rhythmic motor patterns are driven by common premotor and motor neurons in a simple vertebrate spinal cord. J Neurosci 13:4456-4469.
52. Soffe SR (1996) Motor patterns for two distinct rhythmic behaviors evoked by excitatory amino acid agonists in the Xenopus embryo spinal cord. J Neurophysiol 75:1815-1825.
53. Soffe SR (1997) The pattern of sensory discharge can determine the motor response in young Xenopus tadpoles. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 180:711-715.
54. Stein PSG (2005) Neuronal control of turtle hindlimb motor rhythms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:213-229.
55. 2+ currents by 5-HT1A and 5-HT1D receptors in spinal neurons of Xenopus larvae. J Physiol (Lond) 510:103-120.
56. Taylor AL, Cottrell GW, Kristan WB (2002) Analysis of oscillations in a reciprocally inhibitory network with synaptic depression. Neural Comput 14:561-581.
57. Tunstall MJ, Roberts A, Soffe SR (2002) Modelling inter-segmental coordination of neuronal oscillators: synaptic mechanisms for uni-directional coupling during swimming in Xenopus tadpoles. J Comput Neurosci 13:143-158.
58. + current that plays a role in termination of swimming in Xenopus embryos. J Physiol (Lond) 487:557-572.