Abstract
After hindlimb unloading (HU), the adaptive changing of the rat step cycle duration, kinematics of the ankle and knee joints, and duration of one-joint ankle extensor m. soleus (SOL) activity are detected. However, how the activity of their synergist gastrocnemius medialis muscle (GM) changes in locomotion after HU remains unknown. GM is a two-joint muscle that produces both extension and flexion torques at the ankle and knee, respectively, regardless of the step cycle phase. The aim of our study was to assess changes in the flexor and extensor activity of GM and their influence on hindlimb kinematics after HU. The hindlimb kinematics, activity of GM, and SOL were evaluated, and semitendinosus muscle (ST) activity was registered in six Wistar rats in treadmill locomotion before and after HU. The mean EMG of the GM activity, which was co-active with ST burst activity, significantly increased after HU. The mean EMG of the GM activity, which was co-active with SOL activity, was unchanged after HU, but both SOL and GM bursts had a tendency to increase in duration. Hyperextension of the knee joint and the tendency to overextension of the ankle joint in the late of the stance phase were revealed after HU. The results show that the absence of weight bearing leads to an increase only in the flexor activity of GM and does not affect the extensor GM activity. Possible mechanisms of changes in GM activity and joint kinematics after HU are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data will be made available from the corresponding author on reasonable request.
References
Aarts E, Verhage M, Veenvliet JV, Dolan CV, Van Der Sluis S (2014) A solution to dependency: using multilevel analysis to accommodate nested data. Nat Neurosci 17:491–496. https://doi.org/10.1038/nn.3648
Alford EK, Roy RR, Hodgson JA, Edgerton VR (1987) Electromyography of rat soleus, medial gastrocnemius, and tibialis anterior during hind limb suspension. Exp Neurol 96(3):635–649. https://doi.org/10.1016/0014-4886(87)90225-1
Ashley-Ross MA (1995) Patterns of hind limb motor output during walking in the salamander Dicamptodon tenebrosus, with comparisons to other tetrapods. J Comp Physiol A 177:273–285
Canu MH, Falempin M (1996) Effect of hindlimb unloading on locomotor strategy during treadmill locomotion in the rat. Eur J Appl Physiol Occup Physiol 74(4):297–304. https://doi.org/10.1007/bf02226924
Canu MH, Falempin M (1997) Effect of hindlimb unloading on two hindlimb muscles during treadmill locomotion in rats. Eur J Appl Physiol Occup Physiol 75(4):283–288. https://doi.org/10.1007/s004210050162
Canu MH, Garnier C (2009) A 3D analysis of fore- and hindlimb motion during overground and ladder walking: comparison of control and unloaded rats. Exp Neurol 218(1):98–108. https://doi.org/10.1016/j.expneurol.2009.04.009
Canu MH, Falempin M, Orsal D (2001) Fictive motor activity in rat after 14 days of hindlimb unloading. Exp Brain Res 139(1):30–38. https://doi.org/10.1007/s002210100734
Canu MH, Garnier C, Lepoutre FX, Falempin M (2005) A 3D analysis of hindlimb motion during treadmill locomotion in rats after a 14-day episode of simulated microgravity. Behav Brain Res 157(2):309–321. https://doi.org/10.1016/j.bbr.2004.07.009
Capogrosso M, Wagner FB, Gandar J, Moraud EM, Wenger N, Milekovic T et al (2018) Configuration of electrical spinal cord stimulation through real-time processing of gait kinematics. Nat Protoc 13:2031–2061. https://doi.org/10.1038/s41596-018-0030-9
Diogo R, Bello-Hellegouarch G, Kohlsdorf T, Esteve-Altava B, Molnar JL (2016) Comparative myology and evolution of marsupials and other vertebrates, with notes on complexity, bauplan, and “scala naturae.” Anat Rec (Hoboken) 299(9):1224–1255. https://doi.org/10.1002/ar.23390
Duysens J, Pearson KG (1980) Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187(2):321–332. https://doi.org/10.1016/0006-8993(80)90206-1
English AW, Weeks OI (1987) An anatomical and functional analysis of cat biceps femoris and semitendinosus muscles. J Morphol 191(2):161–175. https://doi.org/10.1002/jmor.1051910207
Goudard I, Orsal D, Cabelguen JM (1992) An electromyographic study of the hindlimb locomotor movements in the acute thalamic rat. Eur J Neurosci 4(11):1130–1139. https://doi.org/10.1111/j.1460-9568.1992.tb00140.x
Higham TE, Jayne BC (2004) In vivo muscle activity in the hindlimb of the arboreal lizard, Chamaeleo calyptratus: general patterns and the effects of incline. J Exp Biol 207(Pt 2):249–261. https://doi.org/10.1242/jeb.00745
Hodgson JA (1983) The relationship between soleus and gastrocnemius muscle activity in conscious cats–a model for motor unit recruitment? J Physiol 337:553–562. https://doi.org/10.1113/jphysiol.1983.sp014641
Hutchison DL, Roy RR, Hodgson JA, Edgerton VR (1989) EMG amplitude relationships between the rat soleus and medial gastrocnemius during various motor tasks. Brain Res 502(2):233–244. https://doi.org/10.1016/0006-8993(89)90618-5
Jayne BC, Irschick DJ (1999) Effects of incline and speed on the three-dimensional hindlimb kinematics of a generalized iguanian lizard (Dipsosaurus dorsalis). J Exp Biol 202:143–159
Kaya M, Leonard T, Herzog W (2003) Coordination of medial gastrocnemius and soleus forces during cat locomotion. J Exp Biol 206(Pt 20):3645–3655. https://doi.org/10.1242/jeb.00544
Lauber B, Lichtwark GA, Cresswell AG (2014) Reciprocal activation of gastrocnemius and soleus motor units is associated with fascicle length change during knee flexion. Physiol Rep. https://doi.org/10.14814/phy2.12044
Lawrence JH 3rd, Nichols TR, English AW (1993) Cat hindlimb muscles exert substantial torques outside the sagittal plane. J Neurophysiol 69(1):282–285. https://doi.org/10.1152/jn.1993.69.1.282
Macpherson JM (1988) Strategies that simplify the control of quadrupedal stance. I. Forces at the ground. J Neurophysiol 60(1):204–217. https://doi.org/10.1152/jn.1988.60.1.204
Molnar JL, Diogo R, Hutchinson JR, Pierce SE (2020) Evolution of hindlimb muscle anatomy across the tetrapod water-to-land transition, including comparisons with forelimb anatomy. Anat Rec (Hoboken) 303(2):218–234. https://doi.org/10.1002/ar.23997
Morey-Holton ER, Globus RK (2002) Hindlimb unloading rodent model: technical aspects. J Appl Physiol (1985) 92(4):1367–1377. https://doi.org/10.1152/japplphysiol.00969.2001
Musienko P, van den Brand R, Märzendorfe O, Roy RR, Gerasimenko Y, Edgerton VR, Courtine G (2011) Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. J Neurosci 31:9264–9278
Ohira Y, Nomura T, Kawano F, Sato Y, Ishihara A, Nonaka I (2002) Effects of nine weeks of unloading on neuromuscular activities in adult rats. J Gravit Physiol 9(2):49–59
Pearson KG, Ramirez JM, Jiang W (1992) Entrainment of the locomotor rhythm by group Ib afferents from ankle extensor muscles in spinal cats. Exp Brain Res 90(3):557–566. https://doi.org/10.1007/BF00230939
Philippson M (1905) L’autonomie et la centralisation dans le syst`eme nerveux des animaux. Trav Lab Physio Inst Solvay (Bruxelles) 7:1–208
Popov A, Lyakhovetskii V, Bazhenova E, Gorskii O, Kalinina D, Merkulyeva N, Musienko P (2021) The role of the load-dependent sensory input in control of balance during gait. J Exp Biol. jeb.242138: https://doi.org/10.1242/jeb.242138
Roy RR, Hutchison DL, Pierotti DJ, Hodgson JA, Edgerton VR (1991) EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming. J Appl Physiol 70(6):2522–2529. https://doi.org/10.1152/jappl.1991.70.6.2522
Smith JL, Betts B, Edgerton VR, Zernicke RF (1980) Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. J Neurophysiol 43(3):612–620. https://doi.org/10.1152/jn.1980.43.3.612
Suzuki T, Chino K, Fukashiro S (2014) Gastrocnemius and soleus are selectively activated when adding knee extensor activity to plantar flexion. Hum Mov Sci 36:35–45. https://doi.org/10.1016/j.humov.2014.04.009
Tachibana A, McVea DA, Donelan JM, Pearson KG (2006) Recruitment of gastrocnemius muscles during the swing phase of stepping following partial denervation of knee flexor muscles in the cat. Exp Brain Res 169(4):449–460. https://doi.org/10.1007/s00221-005-0160-5
Tajino J, Ito A, Nagai M, Zhang X, Yamaguchi S, Iijima H, Aoyama T, Kuroki H (2015) Intermittent application of hypergravity by centrifugation attenuates disruption of rat gait induced by 2 weeks of simulated microgravity. Behav Brain Res 287:276–284. https://doi.org/10.1016/j.bbr.2015.03.030
Templeton GH, Padalino M, Manton J, Glasberg M, Silver CJ, Silver P, DeMartino G, Leconey T, Klug G, Hagler H et al (1984) Influence of suspension hypokinesia on rat soleus muscle. J Appl Physiol Respir Environ Exerc Physiol 56(2):278–286. https://doi.org/10.1152/jappl.1984.56.2.278
Walmsley B, Hodgson JA, Burke RE (1978) Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. J Neurophysiol 41(5):1203–1216. https://doi.org/10.1152/jn.1978.41.5.1203
Winiarski AM, Roy RR, Alford EK, Chiang PC, Edgerton VR (1987) Mechanical properties of rat skeletal muscle after hind limb suspension. Exp Neurol 96(3):650–660
Acknowledgements
This work was performed within project ID: 73025408 of the St. Petersburg State University, St. Petersburg, Russia (for N.M.), supported by the Russian Foundation for Basic Research grant №17-29-01034_ofi_m (for electrophysiological testing), Grant № 20-015-00568 (for the data analysis). We thank the following people for their help and expertise: O.V. Gorskii (technical support for experimental setup), E.Y. Bazhenova (care and technical assistance with the animals), Olga Ptitsyna (design and layout of figures).
Author information
Authors and Affiliations
Contributions
AP and PM conceived and designed the experiments; AP and PM performed the research; AP and VL analyzed the data; AP wrote the first draft of the paper; AP, VL, NM and PM revised and approved the final manuscript PM supervised the study.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Communicated by Winston D. Byblow.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Alexander, P., Vsevolod, L., Natalia, M. et al. Effect of hindlimb unloading on recruitment of gastrocnemius medialis muscle during treadmill locomotion in rats. Exp Brain Res 239, 2793–2801 (2021). https://doi.org/10.1007/s00221-021-06167-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-021-06167-9