Abstract
Although stimulation of cutaneous limb afferents has been shown to evoke crossed extension reflexes in unanaesthetised decerebrate or spinalised animals, here we show that stimulation of cutaneous nerves evokes crossed inhibition rather than excitation of contralateral extensor motoneurones in anaesthetised, spinal cord intact cats. Single pulse stimuli delivered to the saphenous, sural or superficial peroneal nerves evoked IPSPs in a high proportion of contralateral motoneurones including those of knee and ankle extensors. These IPSPs had thresholds of less than 1.5 times the threshold of the most excitable fibres and so large myelinated afferents contributed to them. The relative latencies of IPSPs evoked by stimulation of the contralateral superficial peroneal and sural nerves were longer than those evoked via ipsilateral pathways by approximately 1 ms, suggesting that there are at least three synaptic relays in the crossed reflexes. The IPSPs evoked by stimulation of both ipsilateral and contralateral saphenous nerves had minimal latencies suggesting at least three synaptic delays. Like IPSPs evoked by group II afferents, the frequencies of occurrence of crossed IPSPs evoked by stimulation of cutaneous afferents were significantly reduced after spinal transection and the IPSPs recorded after spinalisation were significantly smaller. These findings are consistent with the recent proposal that dorsal horn neurones, which receive input from cutaneous afferents and contact premotor commissural interneurones may mediate the crossed inhibition.
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References
Aggelopoulos NC, Edgley SA (1995) Segmental localisation of the relays mediating crossed inhibition of hindlimb motoneurones from group II afferents in the anaesthetized cat spinal cord. Neurosci Lett 185:60–64
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
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
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
Bouyer LJ, Rossignol S (2003) Contribution of cutaneous inputs from the hindpaw to the control of locomotion. I. Intact cats. J Neurophysiol 90:3625–3639
Bras H, Cavallari P, Jankowska E, Kubin L (1989) Morphology of midlumbar interneurones relaying information from group II muscle afferents in the cat spinal cord. J Comp Neurol 290:1–15
Bras H, Jankowska E, Noga B, Skoog B (1990) Comparison of effects of various types of NA and 5-HT agonists on transmission from group II muscle afferents in the cat. Eur J Neurosci 2:1029–1039
Brown AG (1981) Organisation in the spinal cord. Springer, Berlin Heidelberg New York, pp 13–69
Burke RE (1999) The use of state-dependent modulation of spinal reflexes as a tool to investigate the organization of spinal interneurons. Exp Brain Res 128:263–277
Burke RE, Degtyarenko AM, Simon ES (2001) Patterns of locomotor drive to motoneurons and last-order interneurons: clues to the structure of the CPG. J Neurophysiol 86:447–462
Edgley, Wallace (1989) A short-latency crossed pathway from cutaneous afferents to rat hindlimb motoneurones. J Physiol 411:469–480
Edgley SA, Jankowska E, Krutki P, Hammar I (2003) Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from feline group II muscle afferents. J Physiol 552:961–974
Forssberg H (1979) Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. J Neurophysiol 42:936–953
Forssberg H, Grillner S, Rossignol S (1977) Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Res 132:121–139
Gauthier L, Rossignol S (1981) Contralateral hindlimb responses to cutaneous stimulation during locomotion in high decerebrate cats. Brain Res 207:303–320
Hammar I, Bannatyne BA, Maxwell DJ, Edgley SA, Jankowska E (2004) The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord. Eur J Neurosci 19:1305–1316
Harrison PJ, Jankowska E, Zytnicki D (1986) Lamina VIII interneurones interposed in crossed reflex pathways in the cat. J Physiol (Lond) 371:147–166
Holmquist B, Lundberg A (1959) The organisation of the supraspinal inhibitory control of interneurons of various spinal reflex arcs. Arch Ital Biol 97:340–356
Jankowska E, Noga BR (1990) Contralaterally projecting lamina VIII interneurones in middle lumbar segments in the cat. Brain Res 535:327–330
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
Lundberg A (1979) Multisensory control of spinal reflex pathways. Prog Brain Res 50:11–28
Lundberg A (1982) Inhibitory control from the brainstem of transmission from primary afferents to motoneurones, primary afferent terminals and ascending pathways. In: Sjolund B, Bjorklund A (eds) Brain stem control of spinal mechanisms. Elsevier, Amsterdam, pp 179–224 (Sherrington (1910))
Lundberg A, Malmgren K, Schomburg ED (1987) Reflex pathways from group II muscle afferents. 3. Secondary spindle afferents and the FRA: a new hypothesis. Exp Brain Res 65:294–306
Petko M, Veress G, Vereb G, Storm-Mathisen J, Antal M (2004) Commissural propriospinal connections between the lateral aspects of laminae III–IV in the lumbar spinal cord of rats. J Comp Neurol 480:364–377
Quevedo J, Stecina K, Gosgnach S, McCrea DA (2005a) Stumbling corrective reaction during fictive locomotion in the cat. J Neurophysiol 94:2045–2052
Quevedo J, Stecina K, McCrea DA (2005b) Intracellular analysis of reflex pathways underlying the stumbling corrective reaction during fictive locomotion in the cat. J Neurophysiol 94:2053–2062
Wand P, Prochazka A, Sontag KH (1980) Neuromuscular responses to gait perturbations in freely moving cats. Exp Brain Res 38:109–114
Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347–361
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This work was supported by a grant from the Welcome Trust.
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Edgley, S., Aggelopoulos, N. Short latency crossed inhibitory reflex actions evoked from cutaneous afferents. Exp Brain Res 171, 541–550 (2006). https://doi.org/10.1007/s00221-005-0302-9
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DOI: https://doi.org/10.1007/s00221-005-0302-9