Properties of axon terminals contacting intermediate zone excitatory and inhibitory premotor interneurons with monosynaptic input from group I and II muscle afferents

Journal of Physiology

Volumn 588, Issue 21, 2010, Pages 4217-4233

  Liu, Ting Ting ^a   Bannatyne, B Anne ^a   Jankowska, Elzbieta ^b   Maxwell, David J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CONTROLLED STUDY; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MONOSYNAPTIC POTENTIAL; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL STIMULATION; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PREMOTOR CORTEX; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SENSORY SYSTEM ELECTROPHYSIOLOGY; SPINAL CORD NERVE CELL;

ANIMALS; CATS; CELL COMMUNICATION; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MODELS, ANIMAL; MUSCLE, SKELETAL; NEURONS, AFFERENT; PRESYNAPTIC TERMINALS; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 78049452080     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.192211     Document Type: Article

References (49)

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. 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.
3. 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.
4. 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.
5. Bannatyne BA, Liu TT, Hammar I, Stecina K, Jankowska E & Maxwell DJ (2009). Excitatory and inhibitory intermediate zone interneurons in pathways from feline group I and II afferents: differences in axonal projections and input. J Physiol 587, 379-399.
6. Bennett DJ, Hultborn H, Fedirchuk B & Gorassini M (1998). Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80, 2023-2037.
7. Brink E, Jankowska E, McCrea DA & Skoog B (1983). Inhibitory interactions between interneurones in reflex pathways from group Ia and group Ib afferents in the cat. J Physiol 343, 361-373.
8. Cai YL, Ma WL, Wang JQ, Li YQ & Li M (2008). Excitatory pathways from the vestibular nuclei to the NTS and the PBN and indirect vestibulo-cardiovascular pathway from the vestibular nuclei to the RVLM relayed by the NTS. Brain Res 1240, 96-104.
9. 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.
10. Davies HE & Edgley SA (1994). Inputs to group II-activated midlumbar interneurones from descending motor pathways in the cat. J Physiol 479, 463-473.
11. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
12. Duenas SH & Rudomin P (1988). Excitability changes of ankle extensor group Ia and Ib fibers during fictive locomotion in the cat. Exp Brain Res 70, 15-25.
13. Edgley SA & Gallimore CM (1988). The morphology and projections of dorsal horn spinocerebellar tract neurones in the cat. J Physiol 397, 99-111.
14. 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.
15. 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.
16. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J & Edwards RH (2001). The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31, 247-260.
17. Grillner S & Hongo T (1972). Vestibulospinal effects on motoneurones and interneurones in the lumbosacral cord. Prog Brain Res 37, 243-262.
18. Harrison PJ & Jankowska E (1985). Sources of input to interneurones mediating group I non-reciprocal inhibition of motoneurones in the cat. J Physiol 361, 379-401.
19. Holmquist B & Lundberg A (1961). Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurons. Acta Physiol Scand 54, 1-51.
20. Hongo T, Jankowska E & Lundberg A (1972). The rubrospinal tract. IV. Effects on interneurones. Exp Brain Res 15, 54-78.
21. 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.
22. Hultborn H, Brownstone RB, Toth TI & Gossard JP (2004). Key mechanisms for setting the input-output gain across the motoneuron pool. Prog Brain Res 143, 77-95.
23. Jankowska E (1992). Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38, 335-378.
24. Jankowska E (2001). Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol 533, 31-40.
25. Jankowska E (2008). Spinal interneuronal networks in the cat: elementary components. Brain Res Rev 57, 46-55.
26. Jankowska E, Bannatyne BA, Stecina K, Hammar I, Cabaj A & Maxwell DJ (2009). Commissural interneurons with input from group I and II muscle afferents in feline lumbar segments: neurotransmitters, projections and target cells. J Physiol 587, 401-418.
27. Jankowska E & Edgley SA (2010). Functional subdivision of feline spinal interneurons in reflex pathways from group Ib and II muscle afferents; an update. Eur J Neurosci 32, 881-893.
28. Jankowska E, Edgley SA, Krutki P & Hammar I (2005). Functional differentiation and organization of feline midlumbar commissural interneurones. J Physiol 565, 645-658.
29. Jankowska E & Hammar I (2002). Spinal interneurons; how can studies in animals contribute to the understanding of spinal interneuronal systems in man? Brain Res Rev 40, 19-28.
30. Jankowska E, Slawinska U & Hammar I (2002). Differential presynaptic inhibition of actions of group II afferents in di- and polysynaptic pathways to feline motoneurones. J Physiol 542, 287-299.
31. Kullander K, Butt SJ, Lebret JM, Lundfald L, Restrepo CE, Rydstrom A, Klein R & Kiehn O (2003). Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299, 1889-1892.
32. McCrea DA & Rybak IA (2008). Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57, 134-146.
33. 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.
34. Maxwell DJ, Kerr R, Jankowska E & Riddell JS (1997). Synaptic connections of dorsal horn group II spinal interneurons: synapses formed with the interneurons and by their axon collaterals. J Comp Neurol 380, 51-69.
35. 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.
36. Nielsen JB, Crone C & Hultborn H (2007). The spinal pathophysiology of spasticity - from a basic science point of view. Acta Physiol (Oxf) 189, 171-180.
37. Olave MJ & Maxwell DJ (2003). Neurokinin-1 projection cells in the rat dorsal horn receive synaptic contacts from axons that possess α2C-adrenergic receptors. J Neurosci 23, 6837-6846.
38. Oliveira AL, Hydling F, Olsson E, Shi T, Edwards RH, Fujiyama F, Kaneko T, Hokfelt T, Cullheim S & Meister B (2003). Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50, 117-129.
39. 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.
40. Riddell JS, Jankowska E & Huber J (1995). Organization of neuronal systems mediating presynaptic inhibition of group II muscle afferents in the cat. J Physiol 483, 443-460.
41. Rudomin P & Schmidt RF (1999). Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129, 1-37.
42. Stecina K, Jankowska E, Cabaj A, Pettersson L-G, Bannatyne BA & Maxwell DJ (2008a). Premotor interneurones contributing to actions of feline pyramidal tract neurones on ipsilateral hindlimb motoneurones. J Physiol 586, 557-574.
43. Stecina K, Quevedo J & McCrea DA (2005). Parallel reflex pathways from flexor muscle afferents evoking resetting and flexion enhancement during fictive locomotion and scratch in the cat. J Physiol 569, 275-290.
44. Stecina K, Slawinska U & Jankowska E (2008b). Ipsilateral actions of feline rubrospinal tract neurones on hindlimb motoneurones. J Physiol 586, 5865-5884.
45. Todd AJ, Hughes DI, Polgar 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.
46. +/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22, 142-155.
47. Watson AH & 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.
48. Yakovenko S, McCrea DA, Stecina K & Prochazka A (2005). Control of locomotor cycle durations. J Neurophysiol 94, 1057-1065.
49. Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM & Miles GB (2009). A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64, 645-662.