Roles for inhibition: Studies on networks controlling swimming in young frog tadpoles

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 194, Issue 2, 2008, Pages 185-193

  Roberts, Alan ^a   Li, Wen Chang ^a   Soffe, S R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

GABA; Glycine; Reticulospinal; Spinal cord; Xenopus

Indexed keywords

ANIMAL; CENTRAL NERVOUS SYSTEM; FROGS AND TOADS; LARVA; NERVE CELL; NERVE CELL INHIBITION; NERVE CELL NETWORK; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; SWIMMING;

ANIMALS; ANURA; CENTRAL NERVOUS SYSTEM; LARVA; NERVE NET; NEURAL INHIBITION; NEURONS; SWIMMING;

EID: 38849158682     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-007-0273-3     Document Type: Review

References (52)

1. Binor E, Heathcote RD (2001) Development of GABA-immunoreactive neuron patterning in the spinal cord. J Comp Neurol 438:1-11
2. Boothby KM, Roberts A (1992) The stopping response of Xenopus laevis embryos: pharmacology and intracellular physiology of rhythmic spinal neurones and hindbrain neurones. J Exp Biol 169:65-86
3. Boothby KM, Roberts A (1995) Effects of site and strength of tactile stimulation on the swimming responses of Xenopus laevis embryos. J Zool (Lond) 235:113-125
4. Cangiano L, Grillner S (2005) Mechanisms of rhythm generation in a spinal locomotor network deprived of crossed connections: the lamprey hemicord. J Neurosci 25:923-935
5. Dale N (1985) Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. J Physiol (Lond) 363:61-70
6. Dale N (1995) Experimentally derived model for the locomotor pattern generator in the Xenopus embryo. J Physiol (Lond) 489:489-510
7. Dale N (2003) Coordinated motor activity in simulated spinal networks emerges from simple biologically plausible rules of connectivity. J Comput Neurosci 14:55-70
8. Dale N, Ottersen OP, Roberts A, Storm-Mathisen J (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255-257
9. Dale N, Roberts A, Ottersen OP, Storm-Mathisen J (1987) The morphology and distribution of ''Kolmer-Agduhr cells,'' a class of cerebrospinal-fluid- contacting neurons revealed in the frog embryo spinal cord by GABA immunocytochemistry. Proc R Soc B 232:193-203
10. Green CS, Soffe SR (1998) Roles of ascending inhibition during two rhythmic motor patterns in Xenopus tadpoles. J Neurophysiol 79:2316-2328
11. Higashijima S, Masino MA, Mandel G, Fetcho JR (2004) Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 24:5827-5839
12. Jamieson D, Roberts A (2000) Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. J Exp Biol 203(Pt 12):1857-1867
13. Kahn JA, Roberts A (1982) The neuromuscular basis of rhythmic struggling movements in embryos of Xenopus laevis. J Exp Biol 99:197-205
14. 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
15. Lambert TD, Li WC, Soffe SR, Roberts A (2004a) Brainstem control of activity and responsiveness in resting frog tadpoles: tonic inhibition. J Comp Physiol A 190:331-342
16. Lambert TD, Howard J, Plant A, Soffe S, Roberts A (2004b) Mechanisms and significance of reduced activity and responsiveness in resting frog tadpoles. J Exp Biol 207:1113-1125
17. 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
18. 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
19. Li WC, Soffe SR, Roberts A (2003a) The spinal interneurons and properties of glutamatergic synapses in a primitive vertebrate cutaneous flexion reflex. J Neurosci 23:9068-9077
20. Li WC, Perrins R, Walford A, Roberts A (2003b) The neuronal targets for GABAergic reticulospinal inhibition that stops swimming in hatchling frog tadpoles. J Comp Physiol A 189:29-37
21. Li W-C, Soffe SR, Roberts A (2004a) Dorsal spinal interneurons forming a primitive, cutaneous sensory pathway. J Neurophysiol 92:895-904
22. Li WC, Higashijima S, Parry DM, Roberts A, Soffe SR (2004b) Primitive roles for inhibitory interneurons in developing frog spinal cord. J Neurosci 24:5840-5848
23. Li W-C, Soffe SR, Wolf E, Roberts A (2006) Persistent pesponses to brief stimuli: feedback excitation among brainstem neurons. J Neurosci 26:4026-4035
24. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H (2004) Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7:17-23
25. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16:265-297
26. Perkel DH, Mulloney B (1974) Motor pattern production in reciprocally inhibitory neurons exhibiting post-inhibitory rebound. Science 185:181-183
27. Perrins R, Walford A, Roberts A (2002) Sensory activation and role of inhibitory reticulospinal neurons that stop swimming in hatchling frog tadpoles. J Neurosci 22:4229-4240
28. Poulet JFA, Hedwig B (2007) New insights into corollary discharges mediated by identified neural pathways. Trends Neurosci 30:14
29. Renshaw B (1946) Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 9:191-204
30. Roberts A (1980) The function and role of two types of mechanoreceptive 'free' nerve endings in the head skin of amphibian embryos. J Comp Physiol A 135:341-348
31. Roberts A (2000) Early functional organization of spinal neurons in developing lower vertebrates. Brain Res Bull 53:585-593
32. Roberts A, Blight AR (1975) Anatomy, physiology and behavioural role of sensory nerve endings in the cement gland of embryonic Xenopus. Proc R Soc B 192:111-127
33. Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian embryo spinal cord. Phil Trans R Soc 296:195-212
34. Roberts A, Tunstall MJ (1990) Mutual re-excitation 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
35. Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J Comp Neurol 261:435-449
36. Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1988) Development and characterization of commissural interneurones in the spinal cord of Xenopus laevis embryos revealed by antibodies to glycine. Development 103:447-461
37. Satterlie RA (1985) Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generator. Science 229:402-404
38. 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
39. Seki K, Perlmutter SI, Fetz EE (2003) Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309-1316
40. Sherrington CS (1906) The integrative action of the nervous system, Yale University Press, New Haven
41. Sillar KT, Roberts A (1988) A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331:262-265
42. Sillar KT, Roberts A (1992) The role of premotor interneurons in phase-dependent modulation of a cutaneous reflex during swimming in Xenopus laevis embryos. J Neurosci 12:1647-1657
43. Sillar KT, Wedderburn JF, Simmers AJ (1991) The development of swimming rhythmicity in post-embryonic Xenopus laevis. Proc R Soc B 246:147-153
44. Soffe SR (1989) Roles of glycinergic inhibition and N-methyl-d-aspartate receptor mediated excitation in the locomotor rhythmicity of one half of the Xenopus embryo central nervous system. Eur J Neurosci 1:561-571
45. 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
46. Soffe SR (1991) Triggering and gating of motor responses by sensory stimulation: behavioural selection in Xenopus embryos. Proc R Soc Lond B 246:197-203
47. 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
48. Soffe SR, Clarke JD, Roberts A (1984) Activity of commissural interneurons in spinal cord of Xenopus embryos. J Neurophysiol 51:1257-1267
49. Soffe SR, Zhao FY, Roberts A (2001) Functional projection distances of spinal interneurons mediating reciprocal inhibition during swimming in Xenopus tadpoles. Europ J Neurosci 13:617-627
50. Vu ET, Krasne FB (1993) Crayfish tonic inhibition: prolonged modulation of behavioral excitability by classical GABAergic inhibition. J Neurosci 13:4394-4402
51. Wu LG, Saggau P (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20:204-212
52. Yoshida M, Roberts A, Soffe SR (1998) Axon projections of reciprocal inhibitory interneurons in the spinal cord of young Xenopus tadpoles and implications for the pattern of inhibition during swimming and struggling. J Comp Neurol 400:504-518