Excitatory and inhibitory intermediate zone interneurons in pathways from feline group I and II afferents: Differences in axonal projections and input

Journal of Physiology

Volumn 587, Issue 2, 2009, Pages 379-399

  Bannatyne, B A ^a   Liu, T T ^a   Hammar, I ^b   Stecina, K ^b   Jankowska, E ^b   Maxwell, D J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE RECEPTOR; GLYCINE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAT; CELL LABELING; CONTROLLED STUDY; DENDRITE; ELECTROPHYSIOLOGY; GRAY MATTER; IMMUNOCYTOCHEMISTRY; INTERNEURON; LUMBAR SPINE; MORPHOLOGY; MOTONEURON NUCLEUS; MUSCLE SPINDLE AFFERENT NERVE; NERVE ENDING; NERVE FIBER; NONHUMAN; PERIKARYON; PHENOTYPE; POSTSYNAPTIC INHIBITION; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RETICULOSPINAL TRACT; SYNAPTIC TRANSMISSION; ADULT; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE PROJECTION; YOUNG ADULT;

AFFERENT PATHWAYS; ANIMALS; AXONS; CARRIER PROTEINS; CATS; CHOLINE O-ACETYLTRANSFERASE; DENDRITES; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMATE DECARBOXYLASE; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MEMBRANE PROTEINS; MOTOR NEURONS; MUSCLE, SKELETAL; PERIPHERAL NERVES; REFLEX; SPINAL CORD; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 58349092087     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.159129     Document Type: Article

References (60)

1. Aggelopoulos NC, Burton MJ, Clarke RW & Edgley SA (1996). Characterization of a descending system that enables crossed group II inhibitory reflex pathways in the cat spinal cord. J Neurosci 16, 723-729.
2. Aggelopoulos NC & Edgley SA (1995). Segmental localisation of the relays mediating crossed inhibition of hindlimb motoneurons from group II afferents in the anaesthetized cat spinal cord. Neurosci Lett 185, 60-64.
3. Alstermark B & Kummel H (1986). Transneuronal labelling of neurones projecting to forelimb motoneurones in cats performing different movements. Brain Res 376, 387-391.
4. Alvarez FJ, Dewey DE, Harrington DA & Fyffe REW (1997). Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J Comp Neurol 379, 150-170.
5. Angel MJ, Guertin P, Jimenez T & McCrea DA (1996). Group I extensor afferents evoke disynaptic EPSPs in cat hindlimb extensor motorneurones during fictive locomotion. J Physiol 494, 851-861.
6. Angel MJ, Jankowska E & McCrea DA (2005). Candidate interneurones mediating group I disynaptic EPSPs in extensor motoneurones during fictive locomotion in the cat. J Physiol 563, 597-610.
7. Arya T, Bajwa S & Edgley SA (1991). Crossed reflex actions from group II muscle afferents in the lumbar spinal cord of the anaesthetized cat. J Physiol 444, 117-131.
8. Bannatyne BA, Edgley SA, Hammar I, Jankowska E & Maxwell DJ (2003). Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur J Neurosci 18, 2273-2284.
9. Bannatyne BA, Edgley SA, Hammar I, Jankowska E & Maxwell DJ (2006). Differential projections of excitatory and inhibitory dorsal horn interneurons relaying information from group II muscle afferents in the cat spinal cord. J Neurosci 26, 2871-2880.
10. Biro Z, Hill RH & Grillner S (2008). The activity of spinal commissural interneurons during fictive locomotion in the lamprey. J Neurophysiol 100, 716-722.
11. Bras H, Cavallari P, Janowska E & Kubin L (1989). Morphology of midlumbar interneurons relaying information from group II muscle afferents in the cat spinal cord. J Comp Neurol 290, 1-15.
12. Brink E, Harrison PJ, Jankowska E, McCrea DA & Skoog B (1983). Post-synaptic potentials in a population of motoneurones following activity of single interneurones in the cat. J Physiol 343, 341-359.
13. Brink E, Jankowska E, McCrea D & Skoog B (1981). Use of sucrose gap for recording postsynaptic population potentials evoked by single interneurones in spinal motoneurones. Brain Res 223, 165-169.
14. Butt SJ, Harris-Warrick RM & Kiehn O (2002). Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 22, 9961-9971.
15. Butt SJ & Kiehn O (2003). Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38, 953-963.
16. Cavallari P, Edgley SA & Jankowska E (1987). Post-synaptic actions of midlumbar interneurones on motoneurones of hind-limb muscles in the cat. J Physiol 389, 675-689.
17. Czarkowska J, Jankowska E & Sybirska E (1976). Axonal projections of spinal interneurones excited by group I afferents in the cat, revealed by intracellular staining with horseradish peroxidase. Brain Res 118, 115-118.
18. Eccles JC, Magni F & Willis WD (1962). Depolarization of central terminals of Group I afferent fibres from muscle. J Physiol 160, 62-93.
19. Edgley SA & Jankowska E (1987a). Field potentials generated by group II muscle afferents in the middle lumbar segments of the cat spinal cord. J Physiol 385, 393-413.
20. Edgley SA & Jankowska E (1987b). An interneuronal relay for group I and II muscle afferents in the midlumbar segments of the cat spinal cord. J Physiol 389, 647-674.
21. Fetz EE, Jankowska E, Johannisson T & Lipski J (1979). Autogenetic inhibition of motoneurones by impulses in group Ia muscle spindle afferents. J Physiol 293, 173-195.
22. Flatman JA, Engberg I & Lambert JD (1982). Reversibility of Ia EPSP investigated with intracellularly iontophoresed QX-222. J Neurophysiol 48, 419-430.
23. Gonzalez-Forero D, Pastor AM, Geiman EJ, Benítez-Temiño B & Alvarez FJ (2005). Regulation of gephyrin cluster size and inhibitory synaptic currents on Renshaw cells by motor axon excitatory inputs. J Neurosci 25, 417-429.
24. Gossard JP, Brownstone RM, Barajon I & Hultborn H (1994). Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp Brain Res 98, 213-228.
25. Harrison PJ, Jankowska E & Zytnicki D (1986). Lamina VIII interneurones interposed in crossed reflex pathways in the cat. J Physiol 371, 147-166.
26. Holmqvist B & Lundberg A (1959). On the organization of the supraspinal inhibitory control of interneurones of various spinal reflex arcs. Arch Ital Biol 97, 340-356.
27. Holmqvist B & Lundberg A (1961). Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurones. Acta Physiol Scand Suppl 186, 1-15.
28. Hoover JE & Durkovic RG (1992). Retrograde labeling of lumbosacral interneurons following injections of red and green fluorescent microspheres into hindlimb motor nuclei of the cat. Somatosens Mot Res 9, 211-226.
29. Hughes DI, Mackie M, Nagy GG, Riddell JS, Maxwell DJ, Szabo G, Erdelyi F, Veress G, Szucs P, Antal M & Todd AJ (2005). P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase-65 and originate from cells in deep medial dorsal horn. Proc Natl Acad Sci U S A 102, 9038-9043.
30. Jankowska E (1992). Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38, 335-378.
31. Jankowska E, Bannatyne BA, Liu TT, Cabaj A, Stecina K, Hammar I & Maxwell DJ (2009). Commissural interneurones with input from muscle afferents in midlumbar segments in the cat; axonal projections, transmitter content and target cells. J Physiol 587, 401-418.
32. Jankowska E, Edgley SA, Krutki P & Hammar I (2005). Functional differentiation and organization of feline midlumbar commissural interneurones. J Physiol 565, 645-658.
33. Jankowska E, Hammar I, Chojnicka B & Heden CH (2000). Effects of monoamines on interneurons in four spinal reflex pathways from group I and/or group II muscle afferents. Eur J Neurosci 12, 701-714.
34. Jankowska E, Hammar I, Slawinska U, Maleszak K & Edgley SA (2003). Neuronal basis of crossed actions from the reticular formation upon feline hindlimb motoneurons. J Neurosci 23, 1867-1878.
35. Jankowska E & Skoog B (1986). Labelling of midlumbar neurones projecting to cat hindlimb motoneurones by transneuronal transport of a horseradish peroxidase conjugate. Neurosci Lett 71, 163-168.
36. Jordan L, Liu J, Hedlund P, Akay T & Pearson K (2008). Descending command systems for the initiation of locomotion in mammals. Brain Res Rev 57, 183-191.
37. Kiehn O (2006). Locomotor circuits in the mammalian spinal cord. Ann Rev Neurosci 29, 279-306.
38. Kiehn O & Butt SJ (2003). Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog Neurobiol 70, 347-361.
39. Li WC, Cooke T, Sautois B, Soffe SR, Borisyuk R & Roberts A (2007). Axon and dendrite geography predict the specificity of synaptic connections in a functioning spinal cord network. Neural Develop 2, 17.
40. Lundberg A (1982). Inhibitory control from the brain stem of transmission from primary afferents to motoneurones, primary afferent terminals and ascending pathways. In Brain Stem Control of Spinal Mechnisms, ed. Sjölund B & Björklund A, pp. 179-225. Elsevier Biomedical Press, Amsterdam.
41. Lundberg A, Malmgren K & Schomburg ED (1987). Reflex pathways form group II muscle afferent. 3. Secondary spindle afferents and the FRA: A new hypothesis. Exp Brain Res 65, 294-306.
42. Maxwell DJ & Riddell JS (1999). Axoaxonic synapses on terminals of group II muscle spindle afferent axons in the spinal cord of the cat. Eur J Neurosci 11, 2151-2159.
43. McCrea DA & Rybak IA (2007). Modeling the mammalian locomotor CPG: insights from mistakes and perturbations. Prog Brain Res 165, 235-253.
44. McCrea DA & Rybak IA (2008). Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57, 134-146.
45. McCrea DA, Shefchyk SJ, Stephens MJ & Pearson KG (1995). Disynaptic group I excitation of synergist ankle extensor motoneurones during fictive locomotion in the cat. J Physiol 487, 527-539.
46. Olave MJ, Puri N, Kerr R & Maxwell DJ (2002). Myelinated and unmyelinated primary afferent axons form contacts with cholinergic interneurons in the spinal dorsal horn. Exp Brain Res 145, 448-456.
47. Perreault MC, Angel MJ, Guertin P & McCrea DA (1995). Effects of stimulation of hindlimb flexor group II afferents during fictive locomotion in the cat. J Physiol 487, 211-220.
48. Perreault MC, Shefchyk SJ, Jimenez I & McCrea DA (1999). Depression of muscle and cutaneous afferent-evoked monosynaptic field potentials during fictive locomotion in the cat. J Physiol 521, 691-703.
49. Quevedo J, Fedirchuk B, Gosgnach S & McCrea DA (2000). Group I disynaptic excitation of cat hindlimb flexor and bifunctional motoneurones during fictive locomotion. J Physiol 525, 549-564.
50. Quinlan KA & Kiehn O (2007). Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J Neurosci 27, 6521-6530.
51. 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.
52. Rudomin P & Schmidt RF (1999). Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129, 1-37.
53. Rybak IA, Shevtsova NA, Lafreniere-Roula M & McCrea DA (2006a). Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 577, 617-639.
54. Rybak IA, Stecina K, Shevtsova NA & McCrea DA (2006 b). Modelling spinal circuitry involved in locomotor pattern generation: Insights from the effects of afferent stimulation. J Physiol 577, 641-658.
55. Stecina K, Jankowska E, Cabaj A, Pettersson L-G, Bannatyne BA & Maxwell DJ (2008). Premotor interneurones contributing to actions of feline pyramidal tract neurones on ipsilateral hindlimb motoneurones. J Physiol 586, 557-574.
56. Todd AJ, Hughes DI, Polgár E, Nagy GG, Mackie M, Ottersen OP & Maxwell DJ (2003). The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17, 13-27.
57. Todd AJ & Spike RC (1993). The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog Neurobiol 41, 609-638.
58. Todd AJ, Spike RC, Chong D & Neilson M (1995). The relationship between glycine and gephyrin in synapses of the rat spinal cord. Eur J Neurosci 7, 1-11.
59. i transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22, 142-155.
60. Watson AHD & Bazzaz AA (2001). GABA and glycine-like immunoreactivity at axoaxonic synapses on 1a muscle afferent terminals in the spinal cord of the rat. J Comp Neurol 433, 335-348.