STIMULATION OF THE SPINAL CORD OF DECEREBRATED RAT WITH DOUBLE PULSES
PDF (Русский)

Keywords

decerebrated rat
epidural stimulation
transvertebral stimulation
evoked potential
paired pulse facilitation

Abstract

Analysis of responses on electrical stimulation is one of the experimental paradigms to study the excitability of the nervous system. In particular, the technique of recording muscle responses evoked by electrical epidural stimulation (ES) of the spinal cord (SC) in humans and animals is widely used. In rats decerebrated at the precollicular level, responses of mm. tibialis anterior (TA) and gastrocnemius medialis (GM) on ES of the L2, L4, L6 spinal segments and transvertebral stimulation (TS) of the VL2, VL4, VL6 vertebrae with single and double pulses were analyzed. The currents at which the amplitude of the sensory component of the response for a single pulse and one of the pulses of the pair was maximum were determined. At the minimum of these currents, the ratio of the amplitudes of the sensory component of the response to the first and second pulses to the amplitude of the sensory component of the response to a single pulse was analyzed. For both muscles, a weakening of the response to both pulses of the pair was obtained with TS VL2 and VL4, while when stimulating VL2, the TA response to the second pulse was lower than to the first. On the contrary, with ES of all segments of interest, a facilitation of the response to the second pulse was obtained for both muscles. A similar facilitation was qualitatively observed for two other muscles, mm. iliacus and vastus lateralis. Thus, the use of double pulses during stimulation made it possible to identify the dependence of the response of SC neural networks on the method of their activation (TS or ES). The facilitation of the response to the second pulse during ES is presumably explained by a decrease in presynaptic inhibition due to decerebration.

https://doi.org/10.31857/S0044452924020051
PDF (Русский)

References

McLeod JG, Van der Meulen JP (1967) Effect of cerebellar ablation on the H reflex in the cat. Arch Neurol. 16: 421–432. https://doi.org/10.1001/archneur.1967.00470220085010

Lavrov I, Gerasimenko YP, Ichiyama RM, Courtine G, Zhong H, Roy RR, Edgerton VR (2006) Plasticity of spinal cord reflexes after a complete transection in adult rats: relationship to stepping ability. J Neurophysiol. 96: 1699–1710. https://doi.org/10.1152/jn.00325.2006

Hofstoetter US, Freundl B, Binder H, Minassian K (2019) Recovery cycles of posterior root-muscle reflexes evoked by transcutaneous spinal cord stimulation and of the H reflex in individuals with intact and injured spinal cord. PLoS One. 14: e0227057. https://doi.org/10.1371/journal.pone.0227057

Sharma P, Shah PK (2021) In vivo electrophysiological mechanisms underlying cervical epidural stimulation in adult rats. J Physiol. 599: 3121–3150. https://doi.org/10.1113/JP281146

Gerasimenko YP, Lavrov IA, Courtine G, Ichiyama RM, Dy CJ, Zhong H, Roy RR, Edgerton VR (2006) Spinal cord reflexes induced by epidural spinal cord stimulation in normal awake rats. J Neurosci Methods. 157: 253–263. https://doi.org/10.1016/j.jneumeth.2006.05.004

Courtine G, Harkema SJ, Dy CJ, Gerasimenko YP, Dyhre-Poulsen P (2007) Modulation of multisegmental monosynaptic responses in a variety of leg muscles during walking and running in humans. J Physiol. 582(Pt 3): 1125–1139. https://doi.org/10.1113/jphysiol.2007.128447

Roy FD, Gibson G, Stein RB (2012) Effect of percutaneous stimulation at different spinal levels on the activation of sensory and motor roots. Exp Brain Res. 223: 281–289. https://doi.org/10.1007/s00221-012-3258-6

Verma R, Virdi JK, Singh N, Jaggi AS (2019) Animals models of spinal cord contusion injury. Korean J Pain. 32: 12–21. https://doi.org/10.3344/kjp.2019.32.1.12

Павлова НВ, Богачева ИН, Баженова ЕЮ, Горский ОВ, Мошонкина ТР, Герасименко ЮП (2019) Восстановление двигательных функций у спинализированных крыс при электрической стимуляции спинного мозга и локомоторной тренировкe. Российский физиологический журнал им. И.М. Сеченова. 105: 565–577. [Pavlova NV, Bogacheva IN, Bazhenova EJu, Gorskiy OV, Moshonkina TR, Gerasimenko YuP (2019) Vosstanovleniye dvigatel'nykh funktsiy u spinalizirovannykh krys pri elektricheskoy stimulyatsii spinnogo mozga i lokomotornoy trenirovke [Restoration of motor functions in spinal rats by electrical stimulation of the spinal cord and locomotor training] Ross Fiziol Zh Im I M Sechenova 105: 565–577. (In Russ)] https://doi.org/10.1134/S086981391905008X

Malloy DC, Knikou M, Côté M-P (2022) Adapting human-based transcutaneous spinal cord stimulation to develop a clinically relevant animal model. J. of Clinical Medicine. 11: 2023. https://doi.org/10.3390/jcm11072023

Shkorbatova P, Lyakhovetskii V, Pavlova N, Popov A, Bazhenova E, Kalinina D, Gorskii O, Musienko P (2020) Mapping of the spinal sensorimotor network by transvertebral and transcutaneous spinal cord stimulation. Frontiers in systems neuroscience. 14: 555593. https://doi.org/10.3389/fnsys.2020.555593

Nicolopoulos-Stournaras S, Iles JF (1984) Hindlimb muscle activity during locomotion in the rat (Rattus norvegicus) (Rodentia: Muridae). J. Zool. Lond. 203: 427–440. https://doi.org/10.1111/j.1469-7998.1984.tb02342.x

Nakanishi ST, Whelan PJ (2012) A decerebrate adult mouse model for examining the sensorimotor control of locomotion. J Neurophysiol. 107: 500–515. https://doi.org/10.1152/jn.00699.2011

Skinner RD, Garcia-Rill E (1984) The mesencephalic locomotor region (MLR) in the rat. Brain Res. 323: 385–389. https://doi.org/10.1016/0006-8993(84)90319-6

Шкорбатова ПЮ, Ляховецкий ВА, Горский ОВ, Павлова НВ, Баженова ЕЮ, Калинина ДС, Мусиенко ПЕ, Меркульева НС (2023) Электрическая эпидуральная стимуляция спинного мозга децеребрированной крысы. Российский физиологический журнал им. И.М. Сеченова. 109: 798–816. [Shkorbatova PYu, Lyakhovetskii VA, Gorskiy OV, Pavlova NV, Bazhenova EJu, Kalinina DS, Musienko PE, Merkulyeva NS (2023) Elektricheskaya epidural'naya stimulyatsiya spinnogo mozga detserebrirovannoy krysy [Electric epidural stimulation of the spinal cord of the decerebrated rat] Ross Fiziol Zh Im I M Sechenova 109: 798–816. (In Russ)] https://doi.org/10.31857/S0869813923060092

Capogrosso M, Wenger N, Raspopovic S, Musienko P, Beauparlant J, Bassi Luciani L, Courtine G, Micera S (2013) A computational model for epidural electrical stimulation of spinal sensorimotor circuits. J Neurosci. 33: 19326–19340. https://doi.org/10.1523/JNEUROSCI.1688-13.2013

Ghali GZ, Ghali MGZ (2020) Microneurosurgical techniques and perioperative strategies utilized to optimize experimental supracollicular decerebration in rats. J of integrative neuroscience. 19: 137–177. https://doi.org/10.31083/j.jin.2020.01.1153

Gilerovich EG, Moshonkina TR, Fedorova EA, Shishko TT, Pavlova NV, Gerasimenko YP, Otellin VA (2008) Morphofunctional characteristics of the lumbar enlargement of the spinal cord in rats. Neurosci Behav Physiol. 38: 855–860. https://doi.org/10.1007/s11055-008-9056-8

Wenger N, Moraud EM, Gandar J, Musienko P, Capogrosso M, Baud L, Le Goff CG, Barraud Q, Pavlova N, Dominici N, Minev IR, Asboth L, Hirsch A, Duis S, Kreider J, Mortera A, Haverbeck O, Kraus S, Schmitz F, DiGiovanna J, van den Brand R, Bloch J, Detemple P, Lacour SP, Bézard E, Micera S, Courtine G. (2016) Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury. Nat Med. 22: 138–145. https://doi.org/10.1038/nm.4025

Curtis DR, Eccles JC (1960) Synaptic action during and after repetitive stimulation. J Physiol. 150: 374–398. https://doi.org/10.1113/jphysiol.1960.sp006393

Granit R (1950) Reflex self-regulation of muscle contraction and autogenetic inhibition. J Neurophysiol. 13: 351–372. https://doi.org/10.1152/jn.1950.13.5.351

Lloyd DP, Wilson VJ (1957) Reflex depression in rhythmically active monosynaptic reflex pathways. J Gen Physiol. 40: 409–426. https://doi.org/10.1085/jgp.40.3.409

Minassian K, Jilge B, Rattay F, Pinter MM, Binder H, Gerstenbrand F, Dimitrijevic MR (2004) Stepping-like movements in humans with complete spinal cord injury induced by epidural stimulation of the lumbar cord: electromyographic study of compound muscle action potentials. Spinal Cord. 42:401–416. https://doi.org/10.1038/sj.sc.3101615

Dideriksen JL, Muceli S, Dosen S, Laine CM, Farina D (2015) Physiological recruitment of motor units by high-frequency electrical stimulation of afferent pathways. J Appl Physiol (1985). 118: 365–376. https://doi.org/10.1152/japplphysiol.00327.2014

Jaumard NV, Leung J, Gokhale AJ, Guarino BB, Welch WC, Winkelstein BA (2015) Relevant anatomic and morphological measurements of the rat spine. Spine 40: E1084–E1092. https://doi.org/10.1097/BRS.0000000000001021

Mohan R, Tosolini AP, Morris R (2015) Segmental distribution of the motor neuron columns that supply the rat hindlimb: A muscle/motor neuron tract-tracing analysis targeting the motor end plates. Neuroscience. 307: 98–108. https://doi.org/10.1016/j.neuroscience.2015.08.030

Wilson VJ, Talbot WH, Diecke FP (1960) Distribution of recurrent facilitation and inhibition in cat spinal cord. J Neurophysiol. 23: 144–153.

Tanabe M, Kaneko T (1996) Paired pulse facilitation of GABAergic IPSCs in ventral horn neurons in neonatal rat spinal cord. Brain Res. 716:101–106. https://doi.org/10.1016/0006-8993(96)00051-0

Meinck HM (1976). Occurrence of the H reflex and the F wave in the rat. Electroencephalogr Clin Neurophysiol. 41: 530–533. https://doi.org/10.1016/0013-4694(76)90064-x

Calancie B, Broton JG, Klose KJ, Traad M, Difini J, Ayyar DR (1993) Evidence that alterations in presynaptic inhibition contribute to segmental hypo- and hyperexcitability after spinal cord injury in man. Electroencephalogr Clin Neurophysiol. 89: 177–186. https://doi.org/10.1016/0168-5597(93)90131-8

Andrews JC, Roy FD, Ba F, Sankar T (2020). Intraoperative changes in the H-reflex pathway during deep brain stimulation surgery for Parkinson's disease: A potential biomarker for optimal electrode placement. Brain Stimul. 13: 1765–1773. https://doi.org/10.1016/j.brs.2020.09.024

Ho SM, Waite PM (2002) Effects of different anesthetics on the paired-pulse depression of the h reflex in adult rat. Exp Neurol. 177: 494–502. https://doi.org/10.1006/exnr.2002.8013

Guiho T, Baker SN, Jackson A (2021) Epidural and transcutaneous spinal cord stimulation facilitates descending inputs to upper-limb motoneurons in monkeys. J Neural Eng. 18: 046011. https://doi.org/10.1088/1741-2552/abe358

Taylor BA, Fennelly ME, Taylor A, Farrell J (1993) Temporal summation - the key to motor evoked potential spinal cord monitoring in humans. J Neurol Neurosurg Psychiatry. 56: 104–106.

Zhang W, Schneider SP (2011). Short-term modulation at synapses between neurons in laminae II-V of the rodent spinal dorsal horn. J Neurophysiol. 105:2920–2930. https://doi.org/10.1152/jn.00684.2010

Floeter MK, Lev-Tov A (1993) Excitation of lumbar motoneurons by the medial longitudinal fasciculus in the in vitro brain stem spinal cord preparation of the neonatal rat. J Neurophysiol. 70: 2241–2250. https://doi.org/10.1152/jn.1993.70.6.2241

Lyakhovetskii V, Shkorbatova P, Gorskii O, Musienko P. (2022) Forward stepping evoked by transvertebral stimulation in the decerebrate cat. Neuromodulation. S1094-7159(22)01373-3.