Volume 44 Issue 3
May  2023
Turn off MathJax
Article Contents
Paola Salmas, Vincent C. K Cheung. Gradient descent decomposition of force-field motor primitives optogenetically elicited for motor mapping of the murine lumbosacral spinal cord. Zoological Research, 2023, 44(3): 604-619. doi: 10.24272/j.issn.2095-8137.2022.276
Citation: Paola Salmas, Vincent C. K Cheung. Gradient descent decomposition of force-field motor primitives optogenetically elicited for motor mapping of the murine lumbosacral spinal cord. Zoological Research, 2023, 44(3): 604-619. doi: 10.24272/j.issn.2095-8137.2022.276

Gradient descent decomposition of force-field motor primitives optogenetically elicited for motor mapping of the murine lumbosacral spinal cord

doi: 10.24272/j.issn.2095-8137.2022.276
The authors declare that they have no competing interests.
P.S. conceived and designed the study, collected and analyzed the data, and wrote the paper. V.C.K.C. conceived and designed the study and wrote the paper. All authors read and approved the final version of the manuscript.
Funds:  This work was supported by the CUHK Faculty of Medicine Faculty Innovation Award FIA2016/A/04 (to V.C.K.C.), Group Research Scheme NL/JW/rc/grs1819/0426/19hc (to V.C.K.C.), and The Hong Kong Research Grants Council 24115318, CUHK-R4022-18, 14114721, and 14119022 (to V.C.K.C)
More Information
  • Corresponding author: E-mail: vckc@cuhk.edu.hk
  • Received Date: 2022-11-22
  • Accepted Date: 2023-01-19
  • Published Online: 2023-01-20
  • Publish Date: 2023-05-18
  • Generating diverse motor behaviors critical for survival is a challenge that confronts the central nervous system (CNS) of all animals. During movement execution, the CNS performs complex calculations to control a large number of neuromusculoskeletal elements. The theory of modular motor control proposes that spinal interneurons are organized in discrete modules that can be linearly combined to generate a variety of behavioral patterns. These modules have been previously represented as stimulus-evoked force fields (FFs) comprising isometric limb-endpoint forces across workspace locations. Here, we ask whether FFs elicited by different stimulations indeed represent the most elementary units of motor control or are themselves the combination of a limited number of even more fundamental motor modules. To probe for potentially more elementary modules, we optogenetically stimulated the lumbosacral spinal cord of intact and spinalized Thy1-ChR2 transgenic mice (n=21), eliciting FFs from as many single stimulation loci as possible (20–70 loci per mouse) at minimally necessary power. We found that the resulting varieties of FFs defied simple categorization with just a few clusters. We used gradient descent to further decompose the FFs into their underlying basic force fields (BFFs), whose linear combination explained FF variability. Across mice, we identified 4–5 BFFs with partially localizable but overlapping representations along the spinal cord. The BFFs were structured and topographically distributed in such a way that a rostral-to-caudal traveling wave of activity across the lumbosacral spinal cord may generate a swing-to-stance gait cycle. These BFFs may represent more rudimentary submodules that can be flexibly merged to produce a library of motor modules for building different motor behaviors.
  • The authors declare that they have no competing interests.
    P.S. conceived and designed the study, collected and analyzed the data, and wrote the paper. V.C.K.C. conceived and designed the study and wrote the paper. All authors read and approved the final version of the manuscript.
  • loading
  • [1]
    Aoyagi Y, Stein RB, Mushahwar VK, et al. 2004. The role of neuromuscular properties in determining the end-point of a movement. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 12(1): 12−23. doi: 10.1109/TNSRE.2003.823265
    [2]
    Bizzi E, Ajemian R. 2015. A hard scientific quest: understanding voluntary movements. Daedalus, 144(1): 83−95. doi: 10.1162/DAED_a_00324
    [3]
    Bizzi E, Cheung VCK. 2013. The neural origin of muscle synergies. Frontiers in Computational Neuroscience, 7: 51.
    [4]
    Bizzi E, Giszter SF, Loeb E, et al. 1995. Modular organization of motor behavior in the frog’s spinal cord. Trends in Neurosciences, 18(10): 442−446. doi: 10.1016/0166-2236(95)94494-P
    [5]
    Bizzi E, Hogan N, Mussa-Ivaldi FA, et al. 1992. Does the nervous system use equilibrium-point control to guide single and multiple joint movements?. Behavioral and Brain Sciences, 15(4): 603−613. doi: 10.1017/S0140525X00072538
    [6]
    Bizzi E, Mussa-Ivaldi FA, Giszter S. 1991. Computations underlying the execution of movement: a biological perspective. Science, 253(5017): 287−291. doi: 10.1126/science.1857964
    [7]
    Caggiano V, Cheung VCK, Bizzi E. 2016. An optogenetic demonstration of motor modularity in the mammalian spinal cord. Scientific Reports, 6: 35185. doi: 10.1038/srep35185
    [8]
    Cheung VCK, Cheung BMF, Zhang JH, et al. 2020. Plasticity of muscle synergies through fractionation and merging during development and training of human runners. Nature Communications, 11(1): 4356. doi: 10.1038/s41467-020-18210-4
    [9]
    Cheung VCK, d’Avella A, Tresch MC, et al. 2005. Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. Journal of Neuroscience, 25(27): 6419−6434. doi: 10.1523/JNEUROSCI.4904-04.2005
    [10]
    Cheung VCK, Seki K. 2021. Approaches to revealing the neural basis of muscle synergies: a review and a critique. Journal of Neurophysiology, 125(5): 1580−1597. doi: 10.1152/jn.00625.2019
    [11]
    Cheung VCK, Turolla A, Agostini M, et al. 2012. Muscle synergy patterns as physiological markers of motor cortical damage. Proceedings of the National Academy of Sciences of the United States of America, 109(36): 14652−14656. doi: 10.1073/pnas.1212056109
    [12]
    Clark DJ, Ting LH, Zajac FE, et al. 2010. Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. Journal of Neurophysiology, 103(2): 844−857. doi: 10.1152/jn.00825.2009
    [13]
    d’Avella A, Bizzi E. 1998. Low dimensionality of supraspinally induced force fields. Proceedings of the National Academy of Sciences of the United States of America, 95(13): 7711−7714. doi: 10.1073/pnas.95.13.7711
    [14]
    Devarajan K, Cheung VCK. 2014. On nonnegative matrix factorization algorithms for signal-dependent noise with application to electromyography data. Neural Computation, 26(6): 1128−1168. doi: 10.1162/NECO_a_00576
    [15]
    Ethier C, Brizzi L, Darling WG, et al. 2006. Linear summation of cat motor cortex outputs. Journal of Neuroscience, 26(20): 5574−5581. doi: 10.1523/JNEUROSCI.5332-05.2006
    [16]
    Feldman AG. 1986. Once more on the equilibrium-point hypothesis (λ model) for motor control. Journal of Motor Behavior, 18(1): 17−54. doi: 10.1080/00222895.1986.10735369
    [17]
    Giszter S, Kargo W. 2000. Movement organization in the frog spinal cord: prerational intelligence?. In: Cruse H, Dean J, Ritter H. Prerational Intelligence: Adaptive Behavior and Intelligent Systems Without Symbols and Logic, Volume 1, Volume 2 Prerational Intelligence: Interdisciplinary Perspectives on the Behavior of Natural and Artificial Systems, Volume 3. Dordrecht: Springer, 323–341.
    [18]
    Giszter SF, Bizzi E, Mussa-Ivaldi FA. 1992. Motor organization in the frog’s spinal cord. In: Eeckman FH. Analysis and Modeling of Neural Systems. Boston: Springer, 377–392.
    [19]
    Giszter SF, Mussa-Ivaldi FA, Bizzi E. 1993. Convergent force fields organized in the frog’s spinal cord. Journal of Neuroscience, 13(2): 467−491. doi: 10.1523/JNEUROSCI.13-02-00467.1993
    [20]
    Harrison M, O'Brien A, Adams L, et al. 2013. Vertebral landmarks for the identification of spinal cord segments in the mouse. NeuroImage, 68: 22−29. doi: 10.1016/j.neuroimage.2012.11.048
    [21]
    Lee DD, Seung HS. 1999. Learning the parts of objects by non-negative matrix factorization. Nature, 401(6755): 788−791. doi: 10.1038/44565
    [22]
    Lemay MA, Calagan JE, Hogan N, et al. 2001. Modulation and vectorial summation of the spinalized frog’s hindlimb end-point force produced by intraspinal electrical stimulation of the cord. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 9(1): 12−23. doi: 10.1109/7333.918272
    [23]
    Lemay MA, McConnell GC, Kao T, et al. 2002. Endpoint forces obtained during intraspinal microstimulation of the cat lumbar spinal cord - experimental and biomechanical model results. In: Proceedings of the IEEE 28th Annual Northeast Bioengineering Conference (IEEE Cat. No. 02CH37342). Philadelphia: IEEE, 113–114.
    [24]
    Lemay MA, Grill WM. 2004. Modularity of motor output evoked by intraspinal microstimulation in cats. Journal of Neurophysiology, 91(1): 502−514. doi: 10.1152/jn.00235.2003
    [25]
    Levine AJ, Hinckley CA, Hilde KL, et al. 2014. Identification of a cellular node for motor control pathways. Nature Neuroscience, 17(4): 586−593. doi: 10.1038/nn.3675
    [26]
    Liu K, Lu Y, Lee JK, Samara R, et al. 2010. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nature Neuroscience, 13(9): 1075−1081. doi: 10.1038/nn.2603
    [27]
    Loeb EP, Giszter SF, Borghesani P, et al. 1993. Effects of dorsal root cut on the forces evoked by spinal microstimulation in the spinalized frog. Somatosensory & Motor Research, 10(1): 81−95.
    [28]
    Loeb EP, Giszter SF, Saltiel P, et al. 2000. Output units of motor behavior: an experimental and modeling study. Journal of Cognitive Neuroscience, 12(1): 78−97. doi: 10.1162/08989290051137611
    [29]
    Mattis J, Tye KM, Ferenczi EA, et al. 2012. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nature Methods, 9(2): 159−172. doi: 10.1038/nmeth.1808
    [30]
    Mondello SE, Sunshine MD, Fischedick AE, et al. 2018. Optogenetic surface stimulation of the rat cervical spinal cord. Journal of Neurophysiology, 120(2): 795−811. doi: 10.1152/jn.00461.2017
    [31]
    Mussa-Ivaldi FA. 1992. From basis functions to basis fields: vector field approximation from sparse data. Biological Cybernetics, 67(6): 479−489. doi: 10.1007/BF00198755
    [32]
    Mussa-Ivaldi FA, Giszter SF. 1992. Vector field approximation: a computational paradigm for motor control and learning. Biological Cybernetics, 67(6): 491−500. doi: 10.1007/BF00198756
    [33]
    Mussa-Ivaldi FA, Giszter SF, Bizzi E. 1994. Linear combinations of primitives in vertebrate motor control. Proceedings of the National Academy of Sciences of the United States of America, 91(16): 7534−7538. doi: 10.1073/pnas.91.16.7534
    [34]
    Overduin SA, d’Avella A, Carmena JM, et al. 2012. Microstimulation activates a handful of muscle synergies. Neuron, 76(6): 1071−1077. doi: 10.1016/j.neuron.2012.10.018
    [35]
    Ozden I, Wang J, Lu Y, et al. 2013. A coaxial optrode as multifunction write-read probe for optogenetic studies in non-human primates. Journal of Neuroscience Methods, 219(1): 142−154. doi: 10.1016/j.jneumeth.2013.06.011
    [36]
    Rana M, Yani MS, Asavasopon S, et al. 2015. Brain connectivity associated with muscle synergies in humans. Journal of Neuroscience, 35(44): 14708−14716. doi: 10.1523/JNEUROSCI.1971-15.2015
    [37]
    Rathelot JA, Strick PL. 2006. Muscle representation in the macaque motor cortex: an anatomical perspective. Proceedings of the National Academy of Sciences of the United States of America, 103(21): 8257−8262. doi: 10.1073/pnas.0602933103
    [38]
    Saltiel P, D'Avella A, Tresch MC, et al. 2017. Critical points and traveling wave in locomotion: experimental evidence and some theoretical considerations. Frontiers in Neural Circuits, 11: 98. doi: 10.3389/fncir.2017.00098
    [39]
    Saltiel P, D'Avella A, Wyler-Duda K, et al. 2016. Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion. Brain Structure and Function, 221(8): 3869−3890. doi: 10.1007/s00429-015-1133-5
    [40]
    Saltiel P, Wyler-Duda K, D'Avella A, et al. 2005. Localization and connectivity in spinal interneuronal networks: the adduction–caudal extension–flexion rhythm in the frog. Journal of Neurophysiology, 94(3): 2120−2138. doi: 10.1152/jn.00117.2005
    [41]
    Saltiel P, Wyler-Duda K, D'Avella A, et al. 2001. Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. Journal of Neurophysiology, 85(2): 605−619. doi: 10.1152/jn.2001.85.2.605
    [42]
    Savage N. 2019. How AI and neuroscience drive each other forwards. Nature, 571(7766): S15−S17.
    [43]
    Sylos-Labini F, La Scaleia V, Cappellini G, et al. 2020. Distinct locomotor precursors in newborn babies. Proceedings of the National Academy of Sciences of the United States of America, 117(17): 9604−9612.
    [44]
    Takei T, Confais J, Tomatsu S, et al. 2017. Neural basis for hand muscle synergies in the primate spinal cord. Proceedings of the National Academy of Sciences of the United States of America, 114(32): 8643−8648.
    [45]
    Ting LH, Chiel HJ, Trumbower RD, et al. 2015. Neuromechanical principles underlying movement modularity and their implications for rehabilitation. Neuron, 86(1): 38−54.
    [46]
    Tresch MC, Bizzi E. 1999. Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation. Experimental Brain Research, 129(3): 401−416.
    [47]
    Tresch MC, Saltiel P, Bizzi E. 1999. The construction of movement by the spinal cord. Nature Neuroscience, 2(2): 162−167.
    [48]
    Vogt N. 2018. Machine learning in neuroscience. Nature Methods, 15(1): 33.
    [49]
    Yaron A, Kowalski D, Yaguchi H, et al. 2020. Forelimb force direction and magnitude independently controlled by spinal modules in the macaque. Proceedings of the National Academy of Sciences, 117(44): 27655−27666.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(8)  / Tables(2)

    Article Metrics

    Article views (1064) PDF downloads(207) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return