Abstract
Flexible motor control is essential for navigating complex, unpredictable environments. Although movement execution is often associated with stereotyped patterns of neural and muscular activation, the degree to which these patterns are conserved versus flexibly reorganized to meet task demands across diverse contextual changes has not been well characterized. Here we recorded head and body kinematics alongside muscle activity in rhesus monkeys during head stabilization—crucial for maintaining gaze and balance—while walking on a treadmill at various speeds, and during overground locomotion in the presence or absence of enhanced autonomic arousal. Dimensionality reduction analyses revealed a flexible control strategy during treadmill walking: a stable activation structure that scaled with speed. In contrast, overground walking evoked heightened muscle engagement and more substantial changes in organization. This pattern largely persisted even during elevated arousal, with larger pupil size linked to stronger but structurally preserved muscle recruitment. Together these findings demonstrate that the brain dynamically adapts motor coordination to context even for automatic behaviors, underscoring the need to examine control strategies in a wide range of conditions.
Similar content being viewed by others
Data availability
All data supporting the findings of this study are available within the paper and its Supplementary Information. Additional raw data are available from the corresponding author upon reasonable request.
Code availability
Custom MATLAB scripts used to generate the figures are available from the corresponding author upon reasonable request, no original code report.
References
Keshner, F. A. & Peterson, B. W. Mechanisms controlling human head stabilization: I. Head-neck dynamics during random rotations in the horizontal plane. J. Neurophysiol. 73, 2293–2301 (1995).
Cromwell, R. L., Aadland-Monahan, T. K., Nelson, A. T., Stern-Sylvestre, S. M. & Seder, B. Sagittal plane analysis of head, neck, and trunk kinematics and electromyographic activity during locomotion. J. Orthop. Sports Phys. Ther. 31, 255–262 (2001).
Zubair, H. N., Beloozerova, I. N., Sun, H. & Marlinski, V. Head movement during walking in the cat. Neuroscience 332, 101–120 (2016).
Zubair, H. N., Chu, K. M. I., Johnson, J. L., Rivers, T. J. & Beloozerova, I. N. Gaze coordination with strides during walking in the cat. J. Physiol. 597, 5195–5229 (2019).
Dunbar, D. C., Macpherson, J. M., Simmons, R. W. & Zarcades, A. Stabilization and mobility of the head, neck and trunk in horses during overground locomotion: comparisons with humans and other primates. J. Exp. Biol. 211, 3889–3907 (2008).
Zsoldos, R. R., Kotschwar, A. B., Groesel, M., Licka, T. & Peham, C. Electromyography activity of the equine splenius muscle and neck kinematics during walk and trot on the treadmill. Equine Vet. J. Suppl. 42, 455–461 (2010).
Dunbar, D. C. Stabilization and mobility of the head and trunk in vervet monkeys (Cercopithecus aethiops) during treadmill walks and gallops. J. Exp. Biol. 207, 4427–4438 (2004).
Dunbar, D. C., Badam, G. L., Hallgrímsson, B. & Vieilledent, S. Stabilization and mobility of the head and trunk in wild monkeys during terrestrial and flat-surface walks and gallops. J. Exp. Biol. 207, 1027–1042 (2004).
Xiang, Y., Yakushin, S. B., Kunin, M., Raphan, T. & Cohen, B. Head stabilization by vestibulocollic reflexes during quadrupedal locomotion in monkey. J. Neurophysiol. 100, 763–780 (2008).
Imai, T., Moore, S. T., Raphan, T. & Cohen, B. Interaction of the body, head, and eyes during walking and turning. Exp. Brain Res. 136, 1–18 (2001).
Pozzo, T., Berthoz, A. & Lefort, L. Head stabilization during various locomotor tasks in humans. I. normal subjects. Exp. Brain Res. 82, 97–106 (1990).
Kavanagh, J., Barrett, R. & Morrison, S. The role of the neck and trunk in facilitating head stability during walking. Exp. Brain Res. 172, 454–462 (2006).
Cromwell, R., Schurter, J., Shelton, S. & Vora, S. Head stabilization strategies in the sagittal plane during locomotor tasks. Physiother. Res. Int. 9, 33–42 (2004).
Aryan, R., Zobeiri, O. A., Millar, J. L., Schubert, M. C. & Cullen, K. E. Effect of vestibular loss on head-on-trunk stability in individuals with vestibular schwannoma. Sci. Rep. 14, 3512 (2024).
Zobeiri, O. A., Mischler, G. M., King, S. A., Lewis, R. F. & Cullen, K. E. Effects of vestibular neurectomy and neural compensation on head movements in patients undergoing vestibular schwannoma resection. Sci. Rep. 11, 517 (2021).
Zobeiri, O. A., Wang, L., Millar, J. L., Schubert, M. C. & Cullen, K. E. Head movement kinematics are altered during balance stability exercises in individuals with vestibular schwannoma. J. Neuroeng. Rehabil. 19, 120 (2022).
Tokuriki, M. et al. EMG activity of the muscles of the neck and forelimbs during different forms of locomotion. Equine Vet. J. 31, 231–234 (1999).
Tokuriki, M. et al. Effects of trotting speed on muscle activity and kinematics in saddlehorses. Equine Vet. J. 34, 295–301 (2002).
Oliveira, A. S., Gizzi, L., Kersting, U. G. & Farina, D. Modular organization of balance control following perturbations during walking. J. Neurophysiol. 108, 1895–1906 (2012).
Boynton, A. M. & Carrier, D. R. The human neck is part of the musculoskeletal core: cervical muscles help stabilize the pelvis during running and jumping. Integr. Org. Biol. 4, ob021 (2022).
Olree, K. S. & Vaughan, C. L. Fundamental patterns of bilateral muscle activity in human locomotion. Biol. Cyber. 73, 409–414 (1995).
Ivanenko, Y. P., Poppele, R. E. & Lacquaniti, F. Five basic muscle activation patterns account for muscle activity during human locomotion. J. Physiol. 556, 267–282 (2004).
Ivanenko, Y. P., Cappellini, G., Dominici, N., Poppele, R. E. & Lacquaniti, F. Coordination of locomotion with voluntary movements in humans. J. Neurosci. 25, 7238–7253 (2005).
Mileti, I. et al. Muscle activation patterns are more constrained and regular in treadmill than in overground human locomotion. Front. Bioeng. Biotechnol. 8, 581619 (2020).
Marino, G. et al. Influence of backpack carriage and walking speed on muscle synergies in healthy children. Bioengineering 11, 173 (2024).
Cheung, V. C. K. et al. Plasticity of muscle synergies through fractionation and merging during development and training of human runners. Nat. Commun. 11, 4356 (2020).
Torres-Oviedo, G. & Ting, L. H. Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts. J. Neurophysiol. 103, 3084–3098 (2010).
Oliveira, A. S., Gizzi, L., Ketabi, S., Farina, D. & Kersting, U. G. Modular control of treadmill vs overground running. PLoS One 11, e0153307 (2016).
Higurashi, Y. et al. Locomotor kinematics and EMG activity during quadrupedal versus bipedal gait in the Japanese macaque. J. Neurophysiol. 122, 398–412 (2019).
Druelle, F. et al. A comparative study of muscle activity and synergies during walking in baboons and humans. J. Hum. Evol. 189, 103513 (2024).
Goto, R., Larson, S., Shitara, T., Hashiguchi, Y. & Nakano, Y. Muscle synergy in several locomotor modes in chimpanzees and Japanese macaques, and its implications for the evolutionary origin of bipedalism through shared muscle synergies. Sci. Rep. 14, 31134 (2024).
Raffegeau, T. E. et al. Walking (and talking) the plank: dual-task performance costs in a virtual balance-threatening environment. Exp. Brain Res. 242, 1237–1250 (2024).
Nóbrega-Sousa, P. et al. Usual walking and obstacle avoidance are influenced by depressive and anxiety symptoms in patients with Parkinson’s disease. Geriatr. Gerontol. Int. 19, 868–873 (2019).
Mildren, R. L. & Cullen, K. E. Vestibular contributions to primate neck postural muscle activity during natural motion. J. Neurosci. 43, 2326–2337 (2023).
Gallego, J. A., Perich, M. G., Miller, L. E. & Solla, S. A. Neural manifolds for the control of movement. Neuron 94, 978–984 (2017).
Churchland, M. M. et al. Neural population dynamics during reaching. Nature 487, 51–56 (2012).
Russo, A. A. et al. Motor cortex embeds muscle-like commands in an untangled population response. Neuron 97, 953–966 (2018).
Russo, A. A. et al. Neural trajectories in the supplementary motor area and motor cortex exhibit distinct geometries, compatible with different classes of computation. Neuron 107, 745–58.e6 (2020).
Gallego, J. A. et al. Cortical population activity within a preserved neural manifold underlies multiple motor behaviors. Nat. Commun. 9, 4233 (2018).
Perich, M. G., Narain, D. & Gallego, J. A. A neural manifold view of the brain. Nat. Neurosci. 28, 1582–1597 (2025).
Wank, V., Frick, U. & Schmidtbleicher, D. Kinematics and electromyography of lower limb muscles in overground and treadmill running. Int. J. Sports Med. 19, 455–461 (1998).
Riley, P. O., Paolini, G., Della Croce, U., Paylo, K. W. & Kerrigan, D. C. A kinematic and kinetic comparison of overground and treadmill walking in healthy subjects. Gait Posture 26, 17–24 (2007).
Sinclair, J. et al. Three-dimensional kinematic comparison of treadmill and overground running. Sports Biomech. 12, 272–282 (2013).
Matthis, J. S., Yates, J. L. & Hayhoe, M. M. Gaze and the control of foot placement when walking in natural terrain. Curr. Biol. 28, 1224–1233.e5 (2018).
Corneil, B. D., Olivier, E., Richmond, F. J., Loeb, G. E. & Munoz, D. P. Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements. J. Neurophysiol. 86, 1729–1749 (2001).
Blouin, J. S., Siegmund, G. P., Carpenter, M. G. & Inglis, J. T. Neural control of superficial and deep neck muscles in humans. J. Neurophysiol. 98, 920–928 (2007).
Santuz, A. et al. Neuromotor dynamics of human locomotion in challenging settings. iScience 23, 100796 (2020).
Ting, L. H. et al. Neuromechanical principles underlying movement modularity and their implications for rehabilitation. Neuron 86, 38–54 (2015).
Lacquaniti, F., Ivanenko, Y. P. & Zago, M. Patterned control of human locomotion. J. Physiol. 590, 2189–2199 (2012).
Saxena, S., Russo, A. A., Cunningham, J. & Churchland, M. M. Motor cortex activity across movement speeds is predicted by network-level strategies for generating muscle activity. eLife 11, e67620 (2022).
Zaback, M., Adkin, A. L., Chua, R., Inglis, J. T. & Carpenter, M. G. Facilitation and habituation of cortical and subcortical control of standing balance following repeated exposure to a height-related postural threat. Neuroscience 487, 8–25 (2022).
Hodgson, D. D. et al. Visual feedback-dependent modulation of arousal, postural control, and muscle stretch reflexes assessed in real and virtual environments. Front. Hum. Neurosci. 17, 1128548 (2023).
Courtine, G. et al. Kinematic and EMG determinants in quadrupedal locomotion of a non-human primate (Rhesus). J. Neurophysiol. 93, 3127–3145 (2005).
Rosenzweig, E. S. et al. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat. Neurosci. 13, 1505–1510 (2010).
Wei, R. H. et al. Neuromuscular control pattern in rhesus monkeys during bipedal walking. Exp. Anim. 68, 341–349 (2019).
Mazaheri R. et al. The activation pattern of trunk and lower limb muscles in an electromyographic assessment; comparison between ground and treadmill walking. Asian J. Sports Med. 7, e33649 (2016).
Prosser, L., Stanley, C., Norman, T., Park, H. & Damiano, D. Comparison of elliptical training, stationary cycling, treadmill walking and overground walking: electromyographic patterns. Gait Posture 33, 244–250 (2011).
Di Nardo F, Fioretti S. EMG-based analysis of treadmill and ground walking in distal leg muscles. IFMBE Proc. 41, 575–578 (2014).
Safaie, M. et al. Preserved neural dynamics across animals performing similar behaviour. Nature 623, 765–771 (2023).
Vernooij, C. A. et al. Functional coordination of muscles underlying changes in behavioural dynamics. Sci. Rep. 6, 27759 (2016).
Yokoyama, H., Ogawa, T., Kawashima, N., Shinya, M. & Nakazawa, K. Distinct sets of locomotor modules control the speed and modes of human locomotion. Sci. Rep. 6, 36275 (2016).
Winner, T. S., Rosenberg, M. C., Berman, G. J., Kesar, T. M. & Ting, L. H. Gait signature changes with walking speed are similar among able-bodied young adults despite persistent individual-specific differences. Sci. Rep. 14, 19730 (2024).
Kirk, E. A. et al. An output-null signature of inertial load in motor cortex. Nat. Commun. 15, 7309 (2024).
Miri, A. et al. Behaviorally selective engagement of short-latency effector pathways by motor cortex. Neuron 95, 683–96, e11 (2017).
Mante, V., Sussillo, D., Shenoy, K. V. & Newsome, W. T. Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 503, 78–84 (2013).
Fallahtafti, F., Mohammadzadeh Gonabadi, A., Samson, K. & Yentes, J. M. Margin of stability may be larger and less variable during treadmill walking versus overground. Biomechanics 1, 118–130 (2021).
Bernstein, N. A. The Co-ordination and Regulation of Movements. (Pergamon Press, 1967).
Turvey, M. T., Fitch, H. L. & Tuller, B. The Bernstein perspective: I. The problems of degrees of freedom and context-conditioned variability. In Human Motor Behavior (eds. Kelso, J. A. S.) 239–252 (Psychology Press, 2014).
Semaan, M. B. et al. Is treadmill walking biomechanically comparable to overground walking? A systematic review. Gait Posture 92, 249–257 (2022).
Vickery-Howe, D. M. et al. Physiological, perceptual, and biomechanical differences between treadmill and overground walking in healthy adults: a systematic review and meta-analysis. J. Sports Sci. 41, 2088–2120 (2023).
Sain, M. K. & Yurkovich, S. Controller scheduling: a possible algebraic viewpoint. In Proc. Am. Control Conf. 261–269 (1982).
Rugh, J. Design of nonlinear compensators for nonlinear systems by an extended linearization technique. In Proc. IEEE Conf. Decision Control 69–73 (IEEE, 1984).
Baumann, W. & Rugh, W. Feedback control of nonlinear systems by extended linearization. IEEE Trans. Autom. Control 31, 40–46 (1986).
Zobeiri, O. A. & Cullen, K. E. Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum. eLife 11, e75018 (2022).
Mathis, A. et al. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289 (2018).
Wei, R. H. et al. Influence of walking speed on gait parameters of bipedal locomotion in rhesus monkeys. J. Med. Primatol. 45, 304–311 (2016).
Wei, R. H. et al. The kinematic recovery process of rhesus monkeys after spinal cord injury. Exp. Anim. 67, 431–440 (2018).
Vagvolgyi, B. P., Jayakumar, R. P., Madhav, M. S., Knierim, J. J. & Cowan, N. J. Wide-angle, monocular head tracking using passive markers. J. Neurosci. Methods 368, 109453 (2022).
Lee, D. D. & Seung, H. S. Algorithms for non-negative matrix factorization. Adv. Neural Inf. Process. Syst. 13, 556–562 (2001).
Joshi, S., Li, Y., Kalwani, R. M. & Gold, J. I. Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron 89, 221–234 (2016).
Maness, E. B. et al. Role of the locus coeruleus and basal forebrain in arousal and attention. Brain Res. Bull. 188, 47–58 (2022).
Turner, K. L., Gheres, K. W. & Drew, P. J. Relating pupil diameter and blinking to cortical activity and hemodynamics across arousal states. J. Neurosci. 43, 949–964 (2023).
Boisgontier, M. P. & Cheval, B. The anova to mixed model transition. Neurosci. Biobehav. Rev. 68, 1004–1005 (2016).
Acknowledgements
We would like to thank Dale Roberts for his technical support, Balazs Vagvolgyies for his technical support of head and body motion tracking and Pum Wiboonsaksakul, Olivia Leavitt Brown, Dr. Lex Gómez, Dr. Robyn Mildren, Skyler Thomas, Chenhao Bao, and Eva Yezerets for their comments. This research was supported by grants R01DC002390 & R01DC018061 from the National Institute of Health (K.E.C.), as well as a Postdoctoral Research Accelerator Award and the Kavli Neuroscience Discovery Institute Distinguished Postdoctoral Fellowship (R.H.W.).
Author information
Authors and Affiliations
Contributions
R.H.W. and K.E.C. conceived of and designed the overall experiments. R.H.W. and O.R.S. conducted experiments and collected related data. R.H.W. analyzed the data and made the figures. All authors discussed the results. RHW wrote the original draft of the paper with valuable revisions by K.E.C., O.R.S., and A.S.C. K.E.C. secured funding and provided oversight of the project.
Corresponding author
Ethics declarations
Competing interests
All authors declare no competing interests.
Peer review
Peer review information
Communications Biology thanks Arthur Dewolf, Narae Shin and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editors: Shenbing Kuang and Jasmine Pan.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Wei, RH., Stanley, O.R., Charles, A.S. et al. Locomotion engages context-dependent motor strategies for head stabilization in primates. Commun Biol (2026). https://doi.org/10.1038/s42003-026-09512-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s42003-026-09512-2
