Russian Journal of PhysiologyRussian Journal of PhysiologyРоссийский физиологический журнал им. И.М. Сеченова0869-81392658-655XThe Russian Academy of Sciences65156210.31857/S0869813923060092WHJWUMEXPERIMENTAL ARTICLESЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИElectric Epidural Stimulation of the Spinal Cord of the Decerebrated RatЭлектрическая эпидуральная стимуляция спинного мозга децеребрированной крысыShkorbatovaP. Yu.ШкорбатоваП. Ю.mer-natalia@yandex.ruLyakhovetskiiV. A.ЛяховецкийВ. А.mer-natalia@yandex.ruGorskyO. V.ГорскийО. В.mer-natalia@yandex.ruPavlovaaN. V.ПавловаН. В.mer-natalia@yandex.ruBazhenovaE. Yu.БаженоваЕ. Ю.mer-natalia@yandex.ruKalininaD. S.КалининаД. С.mer-natalia@yandex.ruMusienkoP. E.МусиенкоП. Е.mer-natalia@yandex.ruMerkulyevaaN. S.МеркульеваН. С.mer-natalia@yandex.ruPavlov Institute of Physiology of the Russian Academy of SciencesИнститут физиологии им. И.П. Павлова РАНSaint-Petersburg State UniversityСанкт-Петербургский Государственный УниверситетSirius Science and Technology UniversityНаучно-технологический университет “Сириус”01062023109679881601022025Copyright ©; 2023, П.Ю. Шкорбатова, В.А. Ляховецкий, О.В. Горский, Н.В. Павлова, Е.Ю. Баженова, Д.С. Калинина, П.Е. Мусиенко, Н.С. МеркульеваCopyright ©; 2023, П.Ю. Шкорбатова, В.А. Ляховецкий, О.В. Горский, Н.В. Павлова, Е.Ю. Баженова, Д.С. Калинина, П.Е. Мусиенко, Н.С. Меркульева2023П.Ю. Шкорбатова, В.А. Ляховецкий, О.В. Горский, Н.В. Павлова, Е.Ю. Баженова, Д.С. Калинина, П.Е. Мусиенко, Н.С. МеркульеваП.Ю. Шкорбатова, В.А. Ляховецкий, О.В. Горский, Н.В. Павлова, Е.Ю. Баженова, Д.С. Калинина, П.Е. Мусиенко, Н.С. Меркульеваhttps://journals.eco-vector.com/0869-8139/article/view/651562

Decerebrated animals are often used in experimental neurophysiology to study multilevel physiological processes. The model of a decerebrated cat is traditionally used to study locomotion in acute experiments. We wondered if it would be possible to replace it with electrical epidural stimulation of the spinal cord with a decerebrated rat model. On an acute preparation of 16 Wistar rats decerebrated at the precollicular level, the tonic muscles activity, muscles evoked potentials and the possibility of inducing locomotion during electrical epidural stimulation of the spinal cord, were studied. Histological control of the level of decerebration was performed in 10 rats. Quadrupedal walking was induced in five animals, bipedal hindlimb walking – in one animal; the parameters of the evoked locomotion do not depend on the substantia nigra degree of damage. The tonic activity and the amplitude of the sensory component of the evoked potential of the hindlimb muscles (mm. tibialis anterior and gastrocnemius medialis) depend on the rostrocaudal level of decerebration – they are higher when the substantia nigra is damaged. Thus, the model under consideration makes it possible to successfully study muscle tonic activity and evoked muscle potentials; however, the use of this model in the study of controlled locomotion requires additional research.

Децеребрированные препараты часто используются в экспериментальной нейрофизиологии для изучения многоуровневых физиологических процессов. Для исследования локомоции в острых опытах традиционно используется модель децеребрированной кошки. Мы задались вопросом, возможно ли заменить ее при электрической эпидуральной стимуляции спинного мозга на модель децеребрированной крысы. На остром препарате 16-ти децеребрированных на преколликулярном уровне крыс линии Вистар изучены возможность вызова локомоции, а также тоническая активность мышц и мышечные вызванные потенциалы. У 10 проводили гистологический контроль уровня децеребрации. Квадрипедальную ходьбу удалось вызвать у пяти животных, бипедальную ходьбу задними конечностями – у одного животного; при этом параметры вызванной локомоции не зависят от степени повреждения substantia nigra. Тоническая активность и амплитуда сенсорного компонента вызванных потенциалов мышц задних конечностей (mm. tibialis anterior и gastrocnemius medialis) зависят от рострокаудального уровня децеребрации животных – они выше при повреждении черной субстанции (substantia nigra). Таким образом, рассматриваемая модель позволяет успешно исследовать тоническую активность мышц и вызванные мышечные потенциалы, однако использование этой модели при изучении контролируемой локомоции требует проведения дополнительных исследований.

decerebrated ratepidural stimulationtonic activitylocomotionevoked potentialдецеребрированная крысаэпидуральная стимуляциятоническая активностьлокомоциявызванный потенциалStahnisch FW (2010) Chapter 11: on the use of animal experimentation in the history of neurology. Handb Clin Neurol 95: 129–148. https://doi.org/10.1016/S0072-9752(08)02111-8Whelan PJ (1996) Control of locomotion in the decerebrate cat. Prog Neurobiol 49: 481–515.Domínguez-Rodríguez LE, Stecina K, García-Ramírez DL, Mena-Avila E, Milla-Cruz JJ, Martínez-Silva L, Zhang M, Hultborn H, Quevedo JN (2020) Candidate interneurons mediating the resetting of the locomotor rhythm by extensor group I afferents in the cat. Neuroscience 450: 96–112. https://doi.org/10.1016/j.neuroscience.2020.09.017Aguilar Garcia IG, Dueñas-Jiménez JM, Castillo L, Osuna-Carrasco LP, De La Torre Valdovinos B, Castañeda-Arellano R, López-Ruiz JR, Toro-Castillo C, Treviño M, Mendizabal-Ruiz G, Duenas-Jimenez SH (2020) Fictive scratching patterns in brain cortex-ablated, midcollicular decerebrate, and spinal cats. Front Neural Circuits 27: 14. https://doi.org/10.3389/fncir.2020.00001Silverman J., Garnett NL., Giszter SF, Heckman CJ, Kulpa-Eddy JA, Lemay MA, Perry CK, Pinter M (2005) Decerebrate mammalian preparations: unalleviated or fully alleviated pain? A review and opinion. Contempor Topics Lab Animal Sci 44: 34–36.Sapru HN, Krieger AJ (1979) Cardiovascular and respiratory effects of some anesthetics in the decerebrate rat. Eur J Pharmacol 53: 151–158. https://doi.org/10.1016/0014-2999(79)90160-2Ho 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.2002.8013Thiele FH (1905) On the efferent relationship of the optic thalamus and Deiter’s nucleus to the spinal cord, with special reference to the cerebellar influx of Dr Hughlings Jackson and the genesis of the decerebrate rigidity of Ord and Sherrington. J Physiol 32: 358–384. https://doi.org/10.1113/jphysiol.1905.sp001089Sherrington CS (1910) Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40: 28–121. https://doi.org/10.1113/jphysiol.1910.sp001362Frigon A (2020) Fundamental contributions of the cat model to the neural control of locomotion. In The Neural Control of Movement (P. 315–348). Academic Press.https://doi.org/10.1016/B978-0-12-816477-8.00013-2Мусиенко ПЕ, Горский ОВ, Килимник ВА, Козловская ИБ, Courtine G, Edgerton VR, Герасименко ЮП (2013) Регуляция позы и локомоции у децеребрированных и спинализированных животных. Рос физиол журн им ИМ Сеченова 99: 392–405. [Musienko PE, Gorskii OV, Kilimnik VA, Kozlovskaia IB, Courtine G, Edgerton VR, Gerasimenko YuP (2013) Neuronal control of posture and locomotion in decerebrated and spinalized animals. Ross Fiziol Zh Im I M Sechenova 99: 392–405. (In Russ)].Макарова МН (2021) Кошки в лабораторных исследованиях. Обзор литературы. Лабораторные животные для научных исследований. 1: 86–104. [Makarova MN (2021) Cats in laboratory studies. Literature review Laboratornyye Zhivotnyye Dlya Nauchnykh Issledovaniy. 1: 86–104. (In Russ)]. https://doi.org/10.29296/2618723X-2021-01-09Harnie J, Audet J, Klishko AN, Doelman A, Prilutsky BI, Frigon A (2021) The spinal control of backward locomotion. J Neurosci 41: 630–647. https://doi.org/10.1523/JNEUROSCI.0816-20.2020Fathi Y, Erfanian A (2022) Decoding bilateral hindlimb kinematics from cat spinal signals using three-dimensional convolutional neural network. Front Neurosci 16: 801818. https://doi.org/10.3389/fnins.2022.801818Roussel M, Lemieux M, Bretzner F (2020) Using mouse genetics to investigate supraspinal pathways of the brain important to locomotion. In The Neural Control of Movement (P. 269–313). Academic Press. https://doi.org/10.1016/B978-0-12-816477-8.00012-0Hofstoetter US, Freundl B, Binder H, Minassian K (2018) Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: Elicitation of posterior root-muscle reflexes. PloS One 13: e0192013. https://doi.org/10.1371/journal.pone.0192013Ichiyama RM, Gerasimenko YP, Zhong H, Roy RR, Edgerton VR (2005) Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci Lett 383: 339–344. https://doi.org/10.1016/j.neulet.2005.04.049Capogrosso 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.1688-13.2013Wang S, Zhang LC, Fu HT, Deng JH, Xu GX, Li T, Ji XR, Tang PF (2021) Epidural electrical stimulation effectively restores locomotion function in rats with complete spinal cord injury. Neural Regen Res 16: 573–579. https://doi.org/10.4103/1673-5374.290905Gerasimenko Y, Preston C, Zhong H, Roy RR, Edgerton VR, Shah PK (2019) Rostral lumbar segments are the key controllers of hindlimb locomotor rhythmicity in the adult spinal rat. J Neurophysiol 122: 585–600. https://doi.org/10.1152/jn.00810.2018Nicolopoulos-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.xSkinner 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)90319-6Garcia-Rill E, Kinjo N, Atsuta Y, Ishikawa Y, Webber M, Skinner RD (1990) Posterior midbrain-induced locomotion. Brain Res Bull 24: 499–508. https://doi.org/10.1016/0361-9230(90)90103-7Yang CT, Vaca L, Roy RR, Zhong H, Edgerton VR, Judy JW (2005) Neural-Ensemble activity of spinal cord L1/L2 during stepping in a decerebrate rat preparation. Conference Proceedings. 2nd Internat IEEE EMBS Conf Neural Engineer 66–69. https://doi.org/10.1109/CNE.2005.1419554Grillner S, Shik ML (1973) On the descending control of the lumbosacral spinal cord from the “mesencephalic locomotor region”. Acta Physiol Scand 87: 320–333. https://doi.org/10.1111/j.1748-1716.1973.tb05396.xIvanenko YP, Gurfinkel VS, Selionov VA, Solopova IA, Sylos-Labini F, Guertin PA, Lacquaniti F (2017) Tonic and rhythmic spinal activity underlying locomotion. Curr Pharm Des 23: 1753–1763. https://doi.org/10.2174/1381612823666170125152246Vargas Luna JL, Brown J, Krenn MJ, McKay B, Mayr W, Rothwell JC, Dimitrijevic MR (2021) Neurophysiology of epidurally evoked spinal cord reflexes in clinically motor-complete posttraumatic spinal cord injury. Exp Brain Res 239: 2605–2620. https://doi.org/10.1007/s00221-021-06153-1Dobson KL, Harris J (2012) A detailed surgical method for mechanical decerebration of the rat. Exp Physiol 97: 693–698. https://doi.org/10.1113/expphysiol.2012.064840Ghali GZ, Ghali MGZ (2020) Microneurosurgical techniques and perioperative strategies utilized to optimize experimental supracollicular decerebration in rats. J Integ Neurosci 19: 137–177. https://doi.org/10.31083/j.jin.2020.01.1153Gilerovich 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/s11055-008-9056-8Wenger 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.4025Merkulyeva N, Veshchitskii A, Gorsky O, Pavlova N, Zelenin PV, Gerasimenko Y, Deliagina TG, Musienko P (2018) Distribution of spinal neuronal networks controlling forward and backward locomotion. J Neurosci 38: 4695–4707. https://doi.org/10.1523/JNEUROSCI.2951-17.2018Merkulyeva N, Lyakhovetskii V, Gorskii O, Musienko P (2022) Differences in backward and forward treadmill locomotion in decerebrated cats. J Exp Biol 225: jeb244210. https://doi.org/10.1242/jeb.244210Darling RA, Ritter S (2009) 2-Deoxy-D-glucose, but not mercaptoacetate, increases food intake in decerebrate rats. Am J Physiol Regul Integr Comp Physiol 297: R382–R386. https://doi.org/10.1152/ajpregu.90827.2008Zhou D, Huang Q, Fung ML, Li A, Darnall RA, Nattie EE, St John WM (1996) Phrenic response to hypercapnia in the unanesthetized, decerebrate, newborn rat. Respir Physiol 104: 11–22. https://doi.org/10.1016/0034-5687(95)00098-4Bedford TG, Loi PK, Crandall CC (1985) A model of dynamic exercise: the decerebrate rat locomotor preparation. J Appl Physiol 72: 121–127. https://doi.org/10.1152/jappl.1992.72.1.121Ghali MGZ (2021) Dynamic changes in arterial pressure following high cervical transection in the decerebrate rat. J Spinal Cord Med 44: 399–410. https://doi.org/10.1080/10790268.2019.1639974Yoshiyama M, Roppolo JR, Takeda M, de Groat WC (2013) Effects of urethane on reflex activity of lower urinary tract in decerebrate unanesthetized rats. Am J Physiol Renal Physiol 304: F390–F396. https://doi.org/10.1152/ajprenal.00574.2012Asanome M, Matsuyama K, Mori S (1998) Augmentation of postural muscle tone induced by the stimulation of the descending fibers in the midline area of the cerebellar white matter in the acute decerebrate cat. Neurosci Res 30: 257–269.Musienko P, Courtine G, Tibbs JE, Kilimnik V, Savochin A, Garfinkel A, Roy RR, Edgerton VR, Gerasimenko Y (2012) Somatosensory control of balance during locomotion in decerebrated cat. J Neurophysiol 107: 2072–2082. https://doi.org/10.1152/jn.00730.2011Musienko PE, Zelenin PV, Lyalka VF, Gerasimenko YP, Orlovsky GN, Deliagina TG (2012) Spinal and supraspinal control of the direction of stepping during locomotion. J Neurosci 32: 17442–17453. https://doi.org/10.1523/JNEUROSCI.3757-12.2012Musienko PE, Deliagina TG, Gerasimenko YP, Orlovsky GN, Zelenin PV (2014) Limb and trunk mechanisms for balance control during locomotion. J Neurosci 2014. 34: 5704–5716. https://doi.org/10.1523/JNEUROSCI.4663-13.2014Pickering AE, Paton JF (2006) A decerebrate, artificially-perfused in situ preparation of rat: utility for the study of autonomic and nociceptive processing. J Neurosci Meth 155: 260–271. https://doi.org/10.1016/j.jneumeth.2006.01.011Grill HJ, Norgren R (1978) Neurological tests and behavioral deficits in chronic thalamic and chronic decerebrate rats. Brain Res 14: 299–312. https://doi.org/10.1016/0006-8993(78)90570-xШик МЛ, Северин ФВ, Орловский ГН (1966) Управление ходьбой и бегом посредством электрической стимуляции среднего мозга. Биофизика XI: 659–666. [Shik ML, Severin FV, Orlovsky GN (1966) Control of walking and running by means of electric stimulation of the midbrain. Biophyzica XI: 659–666. (In Russ)].Fouad K, Pearson KG (1997) Effects of extensor muscle afferents on the timing of locomotor activity during walking in adult rats. Brain Res 749: 320–328. https://doi.org/10.1016/S0006-8993(96)01328-5Shkorbatova 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. Front Systems Neurosci 14: 555593. https://doi.org/10.3389/fnsys.2020.555593Ishii K, Asahara R, Komine H, Liang N, Matsukawa K (2020) Pivotal role of the ventral tegmental area in spontaneous motor activity and concomitant cardiovascular responses in decerebrate rats. Brain Res 1729: 146616. https://doi.org/10.1016/j.brainres.2019.146616Orlovsky GN (1972) Activity of rubrospinal neurons during locomotion. Brain Res 46: 99–112. https://doi.org/10.1016/0006-8993(72)90008-xBasile GA, Quartu M, Bertino S, Serra MP, Boi M, Bramanti A, Anastasi GP, Milardi D, Cacciola A (2021) Red nucleus structure and function: from anatomy to clinical neurosciences. Brain Struct Funct 226: 69–91. https://doi.org/10.1007/s00429-020-02171-xNicolopoulos-Stournaras S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217: 75–85. https://doi.org/10.1002/cne.902170107Vanderhorst VG, Holstege G (1997) Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat. J Comp Neurol 382: 46–76. https://doi.org/10.1002/(sici)1096-9861(19970526)Lavrov I, Musienko PE, Selionov VA, Zdunowski S, Roy RR, Edgerton VR, Gerasimenko Y (2015) Activation of spinal locomotor circuits in the decerebrated cat by spinal epidural and/or intraspinal electrical stimulation. Brain Res 1600: 84–92. https://doi.org/10.1016/j.brainres.2014.11.003Iwahara T, Atsuta Y, Garcia-Rill E, Skinner RD (1992) Spinal cord stimulation-induced locomotion in the adult cat. Brain Res Bull 28: 99–105. https://doi.org/10.1016/0361-9230(92)90235-pBogacheva IN, Musienko PE, Shcherbakova NA, Moshonkina TR, Savokhin AA, Gerasimenko YuP (2014) Analysis of locomotor activity in decerebrate cats using electromagnetic and epidural electrical stimulation of the spinal cord. Neurosci Behav Physi 44: 552–559. https://doi.org/10.1007/s11055-014-9950-1Waller WH (1940) Progression movements elicited by subthalamic stimulation. J Neurophysiol 3: 300–307.Garcia-Rill E, Skinner RD, Fitzgerald JA (1983) Activity in the mesencephalic locomotor region during locomotion. Exp Neurol 82: 609–622. https://doi.org/10.1016/0014-4886(83)90084-5Орловский ГН (1969) Спонтанная и вызванная локомоция таламической кошки. Биофизика XIV: 1095–1102. [Orlovsky GN (1969) Spontaneous and evoked locomotion of the thalamic cat. Biophyzica XIVI: 1095–1102. (In Russ)].Будакова НН, Шик МЛ (1974) Шагательные движения передних конечностей и феномен Шиффа–Шеррингтона. Бюлл экспер биол мед 77: 6–10. [Budakova NN, Shik ML (1974) Stepping movements of the forelimbs and Shiff-Sherrington phenomen. Byull eksper biol med 77: 6–10. (In Russ)].Yamaguchi T (1992) Muscle activity during forelimb stepping in decerebrate cats. Jpn J Physiol 42: 489–399. https://doi.org/10.2170/jjphysiol.42.489Juvin L, Simmers J, Morin D (2005) Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 25: 6025–6035. https://doi.org/10.1523/JNEUROSCI.0696-05.2005Reed WR, Shum-Siu A, Onifer SM, Magnuson DSK (2006) Inter-enlargement pathways in the ventrolateral funiculus of the adult rat spinal cord. Neuroscience 142: 1195–1207. https://doi.org/10.1016/j.neuroscience.2006.07.017Miller S, Reitsma DJ, van der Meché FG (1973) Functional organization of long ascending propriospinal pathways linking lumbo-sacral and cervical segments in the cat. Brain Res 62: 169–188. https://doi.org/10.1016/0006-8993(73)90626-4Barthélemy D, Leblond H, Provencher J, Rossignol S (2006) Non-locomotor and locomotor hindlimb responses evoked by electrical microstimulation of the lumbar cord in spinalized cats. J Neurophysiol 96: 3273–3292. https://doi.org/10.1152/jn.00203.2006Barthélemy D, Leblond H, Rossignol S (2007) Characteristics and mechanisms of locomotion induced by intraspinal microstimulation and dorsal root stimulation in spinal cats. J Neurophysiol 97: 1986–2000. https://doi.org/10.1152/jn.00818.2006Будакова НН (1971) Шагательные движения, вызываемые у мезэнцефалической кошки ритмическим раздражением дорсального корешка. Физиол журн СССР им ИМ Сеченова LVII: 1632–1640. [Budakova NN (1971) Stepping movements evoked by a rhythmic stimulation of a dorsal root in mesencephalic cat. Fiziol zhurnal SSSR im IM Sechenova LVII: 1632–1640. (In Russ)].Lyakhovetskii V, Merkulyeva N, Gorskii O, Musienko P (2021) Simultaneous bidirectional hindlimb locomotion in decerebrate cats. Sci Rep 11: 3252. https://doi.org/10.1038/s41598-021-82722-2Thota AK, Watson SC, Knapp E, Thompson B, Jung R (2005) Neuromechanical control of locomotion in the rat. J Neurotrauma 22: 442–465. https://doi.org/10.1089/neu.2005.22.442Walker C, Vierck CJ Jr, Ritz LA (1998) Balance in the cat: role of the tail and effects of sacrocaudal transection. Behav Brain Res 91: 41–47. https://doi.org/10.1016/s0166-4328(97)00101-0Wada N, Hori H, Tokuriki M (1993) Electromyographic and kinematic studies of tail movements in dogs during treadmill locomotion. J Morphol 217: 105–113. https://doi.org/10.1002/jmor.1052170109Takakusaki K (2013) Neurophysiology of gait: from the spinal cord to the frontal lobe. Mov Disord 28: 1483–1491. https://doi.org/10.1002/mds.25669de Vrind VAJ, van 't Sant LJ, Rozeboom A, Luijendijk-Berg MCM, Omrani A, Adan RAH (2021) Leptin receptor expressing neurons in the substantia nigra regulate locomotion, and in the ventral tegmental area motivation and feeding. Front Endocrinol 12: 680494. https://doi.org/10.3389/fendo.2021.680494Double KL, Crocker AD (1993) Quantitative electromyographic changes following modification of central dopaminergic transmission. Brain Res 604(1–2): 342–344. https://doi.org/10.1016/0006-8993(93)90388-4Wolfarth S, Konieczny J, Smiałowska M, Schulze G, Ossowska K (1996) Influence of 6-hydroxydopamine lesion of the dopaminergic nigrostriatal pathway on the muscle tone and electromyographic activity measured during passive movements. Neuroscience 74: 985–996. https://doi.org/10.1016/0306-4522(96)00418-6