Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord

Overview

Journal J Neurosci

Specialty Neurology

Date 2004 Jun 25

PMID 15215306

Citations 61

Authors

W-C Li

Shin-Ichi Higashijima

D M Parry

Alan Roberts

S R Soffe

Affiliations

Soon will be listed here.

Abstract

Understanding the neuronal networks in the mammal spinal cord is hampered by the diversity of neurons and their connections. The simpler networks in developing lower vertebrates may offer insights into basic organization. To investigate the function of spinal inhibitory interneurons in Xenopus tadpoles, paired whole-cell recordings were used. We show directly that one class of interneuron, with distinctive anatomy, produces glycinergic, negative feedback inhibition that can limit firing in motoneurons and interneurons of the central pattern generator during swimming. These same neurons also produce inhibitory gating of sensory pathways during swimming. This discovery raises the possibility that some classes of interneuron, with distinct functions later in development, may differentiate from an earlier class in which these functions are shared. Preliminary evidence suggests that these inhibitory interneurons express the transcription factor engrailed, supporting a probable homology with interneurons in developing zebrafish that also express engrailed and have very similar anatomy and functions.

Citing Articles

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References

SAUERESSIG H, Burrill J, Goulding M . Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development. 1999; 126(19):4201-12. DOI: 10.1242/dev.126.19.4201. View

Rudomin P, Schmidt R . Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res. 1999; 129(1):1-37. DOI: 10.1007/s002210050933. View

Lim R, Alvarez F, Walmsley B . GABA mediates presynaptic inhibition at glycinergic synapses in a rat auditory brainstem nucleus. J Physiol. 2000; 525 Pt 2:447-59. PMC: 2269953. DOI: 10.1111/j.1469-7793.2000.t01-1-00447.x. View

Parker D, Grillner S . The activity-dependent plasticity of segmental and intersegmental synaptic connections in the lamprey spinal cord. Eur J Neurosci. 2000; 12(6):2135-46. DOI: 10.1046/j.1460-9568.2000.00095.x. View

Wenner P, ODonovan M, Matise M . Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J Neurophysiol. 2000; 84(5):2651-7. DOI: 10.1152/jn.2000.84.5.2651. View

Buchanan J . Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurobiol. 2001; 63(4):441-66. DOI: 10.1016/s0301-0082(00)00050-2. View

Roberts A . Early functional organization of spinal neurons in developing lower vertebrates. Brain Res Bull. 2001; 53(5):585-93. DOI: 10.1016/s0361-9230(00)00392-0. View

Jankowska E . Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol. 2001; 533(Pt 1):31-40. PMC: 2278593. DOI: 10.1111/j.1469-7793.2001.0031b.x. View

Coen L, Du Pasquier D, Le Mevel S, Brown S, Tata J, MAZABRAUD A . Xenopus Bcl-X(L) selectively protects Rohon-Beard neurons from metamorphic degeneration. Proc Natl Acad Sci U S A. 2001; 98(14):7869-74. PMC: 35434. DOI: 10.1073/pnas.141226798. View

10.

Hale M, Ritter D, Fetcho J . A confocal study of spinal interneurons in living larval zebrafish. J Comp Neurol. 2001; 437(1):1-16. DOI: 10.1002/cne.1266. View

11.

Drapeau P . Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron. 2001; 31(6):1035-46. DOI: 10.1016/s0896-6273(01)00416-0. View

12.

Lee S, Pfaff S . Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat Neurosci. 2001; 4 Suppl:1183-91. DOI: 10.1038/nn750. View

13.

Li W, Perrins R, Soffe S, Yoshida M, WALFORD A, Roberts A . Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles. J Comp Neurol. 2001; 441(3):248-65. DOI: 10.1002/cne.1410. View

14.

Soffe S . 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. 1989; 1(6):561-571. DOI: 10.1111/j.1460-9568.1989.tb00363.x. View

15.

Sillar K, Roberts A . Phase-dependent Modulation of a Cutaneous Sensory Pathway by Glycinergic Inhibition from the Locomotor Rhythm Generator in Xenopus Embryos. Eur J Neurosci. 1992; 4(11):1022-1034. DOI: 10.1111/j.1460-9568.1992.tb00129.x. View

16.

Goulding M, Lanuza G, Sapir T, Narayan S . The formation of sensorimotor circuits. Curr Opin Neurobiol. 2002; 12(5):508-15. DOI: 10.1016/s0959-4388(02)00371-9. View

17.

Nakayama K, Nishimaru H, Kudo N . Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci. 2002; 22(23):10388-98. PMC: 6758765. View

18.

Li W, Soffe S, Roberts A . Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J Neurosci. 2002; 22(24):10924-34. PMC: 6758443. View

19.

Helms A, Johnson J . Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol. 2003; 13(1):42-9. DOI: 10.1016/s0959-4388(03)00010-2. View

20.

Aiken S, Kuenzi F, Dale N . Xenopus embryonic spinal neurons recorded in situ with patch-clamp electrodes--conditional oscillators after all?. Eur J Neurosci. 2003; 18(2):333-43. DOI: 10.1046/j.1460-9568.2003.02755.x. View