Neural coordination of bilateral hand movements: evidence for an involvement of brainstem motor centres.
bimanual movement
brainstem
hand coordination
neural coupling
reticulospinal control
reticulospinal system
startle
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
04 Jan 2024
04 Jan 2024
Historique:
received:
30
07
2023
accepted:
20
12
2023
medline:
5
1
2024
pubmed:
5
1
2024
entrez:
5
1
2024
Statut:
aheadofprint
Résumé
Bilateral hand movements are assumed to be coordinated by a neural coupling mechanism. Neural coupling is experimentally reflected in complex electromyographic (EMG) responses in the forearm muscles of both sides to unilateral electrical arm nerve stimulation (ES). The aim of this study was to examine a potential involvement of the reticulospinal system in neural coupling by the application of loud acoustic stimuli (LAS) known to activate neurons of this system. LAS, ES and combined LAS/ES were applied to healthy subjects during visually guided bilateral hand flexion-extension movements. Muscle responses to the different stimuli were evaluated by electrophysiological recordings. Unilateral electrical ulnar nerve stimulation resulted in neural coupling responses in the forearm extensors (FE) of both sides. Interestingly, LAS evoked bilateral EMG responses that were similar in their configuration to those induced by ES. The presence of startles was associated with a shift of the onset and enhanced amplitude of LAS-induced coupling-like responses. Upon combined LAS/ES application, ES facilitated ipsilateral startles and coupling-like responses. Modulation of coupling-like responses by startles, the similarity of the responses to ES and LAS, and their interaction following combined stimulation suggests that both responses are mediated by the reticulospinal system. Our findings provide novel indirect evidence that the reticulospinal system is involved in the neural coupling of hand movements. This becomes clinically relevant in subjects with a damaged corticospinal system where a dominant reticulospinal system leads to involuntary limb coupling, referred to as associated movements. KEY POINTS: Automatic coordination of hand movements is assumed to be mediated by a neural coupling mechanism reflected by bilateral reflex responses in forearm muscles to unilateral electrical arm nerve stimulation (ES). Loud acoustic stimuli (LAS) were applied to assess a potential involvement of the reticulospinal system in the neural coupling mechanism. LAS evoked a bilateral reflex response in the forearm extensors that was similar to the neural coupling response to ES, and which could be separated from the acoustic startle response. Combined application of LAS and ES resulted in a facilitation of startle and coupling-like responses ipsilateral to ES, thus indicating an interaction of afferences from both stimuli. These novel findings provide indirect evidence that the reticulospinal system is a key motor structure for the coupling of bilateral hand movements.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Swiss National Science Foundation
ID : 32003B_208 110
Pays : Switzerland
Informations de copyright
© 2024 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Ashford, A., Huang, J., Zhang, C., Wei, W., Mustain, W., Eby, T., Zhu, H., & Zhou, W.u (2016) The cervical vestibular-evoked myogenic potentials (cVEMPs) recorded along the sternocleidomastoid muscles during head rotation and flexion in normal human subjects. Journal of the Association for Research in Otolaryngology, 17(4), 303-311.
Baker, S. N. (2011) The primate reticulospinal tract, hand function and functional recovery. The Journal of Physiology, 589(23), 5603-5612.
Balter, J. E., & Zehr, E. P. (2007) Neural coupling between the arms and legs during rhythmic locomotor-like cycling movement. Journal of Neurophysiology, 97(2), 1809-1818.
Brocard, F., Ryczko, D., Fénelon, K., Hatem, R., Gonzales, D., Auclair, F., & Dubuc, R. (2010) The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. Journal of Neuroscience, 30(2), 523-533.
Brown, P., Rothwell, J. C., Thompson, P. D., Britton, T. C., Day, B. L., & Marsden, C. D. (1991) New observations on the normal auditory startle reflex in man. Brain, 114 (Pt 4), 1891-1902.
Carson, R. G., Riek, S., Mackey, D. C., Meichenbaum, D. P., Willms, K., Forner, M., & Byblow, W. D. (2004) Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb. The Journal of Physiology, 560(3), 929-940.
Chen, Y.-T., Li, S., Zhou, P., & Li, S. (2016) Different effects of startling acoustic stimuli (SAS) on TMS-induced responses at rest and during sustained voluntary contraction. Frontiers in Human Neuroscience, 10, 396.
Colebatch, J. G., Rosengren, S. M., & Welgampola, M. S. (2016) Vestibular-evoked myogenic potentials. Handbook of Clinical Neurology, 137, 133-155.
Connolly, K., & Stratton, P. (1968) Developmental changes in associated movements. Developmental Medicine and Child Neurology, 10(1), 49-56.
Davidson, A. G., & Buford, J. A. (2004) Motor outputs from the primate reticular formation to shoulder muscles as revealed by stimulus-triggered averaging. Journal of Neurophysiology, 92(1), 83-95.
Davidson, A. G., & Buford, J. A. (2006) Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: Stimulus triggered averaging. Experimental Brain Research, 173(1), 25-39.
Davis, M., Gendelman, D.s, Tischler, M.d, & Gendelman, P.m (1982) A primary acoustic startle circuit: Lesion and stimulation studies. Journal of Neuroscience, 2(6), 791-805.
Dietz, V. (2002) Do human bipeds use quadrupedal coordination? Trends in Neuroscience (Tins), 25(9), 462-467.
Dietz, V., Macauda, G., Schrafl-Altermatt, M., Wirz, M., Kloter, E., & Michels, L. (2015) Neural coupling of cooperative hand movements: A reflex and fMRI study. Cerebral Cortex, 25(4), 948-958.
Drew, T., & Rossignol, S. (1990a) Functional organization within the medullary reticular formation of intact unanesthetized cat. I. Movements evoked by microstimulation. Journal of Neurophysiology, 64(3), 767-781.
Drew, T., & Rossignol, S. (1990b) Functional organization within the medullary reticular formation of intact unanesthetized cat. II. Electromyographic activity evoked by microstimulation. Journal of Neurophysiology, 64(3), 782-795.
Ejaz, N., Xu, J., Branscheidt, M., Hertler, B., Schambra, H., Widmer, M., Faria, A. V., Harran, M. D., Cortes, J. C., Kim, N., Celnik, P. A., Kitago, T., Luft, A. R., Krakauer, J. W., & Diedrichsen, J. (2018) Evidence for a subcortical origin of mirror movements after stroke: A longitudinal study. Brain, 141(3), 837-847.
Eliassen, J. C., Baynes, K., & Gazzaniga, M. S. (2000) Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers. Brain : A Journal of Neurology, 123 Pt 12, 2501-2511.
Fisher, K. M., Zaaimi, B., & Baker, S. N. (2012) Reticular formation responses to magnetic brain stimulation of primary motor cortex. The Journal of Physiology, 590(16), 4045-4060.
Franz, E. A., Eliassen, J. C., Ivry, R. B., & Gazzaniga, M. S. (1996) Dissociation of spatial and temporal coupling in the bimanual movements of callosotomy patients. Psychological Science, 7(5), 306-310.
Furubayashi, T., Ugawa, Y., Terao, Y., Hanajima, R., Sakai, K., Machii, K., Mochizuki, H., Shiio, Y., Uesugi, H., Enomoto, H., & Kanazawa, I. (2000) The human hand motor area is transiently suppressed by an unexpected auditory stimulus. Clinical Neurophysiology, 111(1), 178-183.
Germann, M., & Baker, S. N. (2021) Evidence for subcortical plasticity after paired stimulation from a wearable device. Journal of Neuroscience, 41(7), 1418-1428.
Germann, M., Maffitt, N. J., Poll, A., Raditya, M., Ting, J. S. K., & Baker, S. N. (2023) Pairing transcranial magnetic stimulation and loud sounds produces plastic changes in motor output. Journal of Neuroscience, 43(14), 2469-2481.
Honeycutt, C. F., Kharouta, M., & Perreault, E. J. (2013) Evidence for reticulospinal contributions to coordinated finger movements in humans. Journal of Neurophysiology, 110(7), 1476-1483.
Irvine, D. R., & Jackson, G. D. (1983) Auditory input to neurons in mesencephalic and rostral pontine reticular formation: An electrophysiological and horseradish peroxidase study in the cat. Journal of Neurophysiology, 49(6), 1319-1333.
Jeffreys, H. (1961) Theory of probability. Oxford: Clarendon Press.
Kennerley, S. W., Diedrichsen, J., Hazeltine, E., Semjen, A., & Ivry, R. B. (2002) Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements. Nature Neuroscience, 5(4), 376-381.
Keysers, C., Gazzola, V., & Wagenmakers, E.-J. (2020) Using Bayes factor hypothesis testing in neuroscience to establish evidence of absence. Nature Neuroscience, 23(7), 788-799.
Köchli, S., Scharfenberger, T., & Dietz, V. (2020) Coordination of bilateral synchronous and asynchronous hand movements. Neuroscience Letters, 720, 134757.
Koerte, I., Eftimov, L., Laubender, R. P., Esslinger, O., Schroeder, A. S., Ertl-Wagner, B., Wahllaender-Danek, U., Heinen, F., & Danek, A. (2010) Mirror movements in healthy humans across the lifespan: Effects of development and ageing. Developmental Medicine and Child Neurology, 52(12), 1106-1112.
Licari, M., & Larkin, D. (2008) Increased associated movements: Influence of attention deficits and movement difficulties. Human Movement Science, 27(2), 310-324.
Lingenhohl, K., & Friauf, E. (1994) Giant neurons in the rat reticular formation: A sensorimotor interface in the elementary acoustic startle circuit? Journal of Neuroscience, 14(3), 1176-1194.
Liuzzi, G., Horniss, V., Zimerman, M., Gerloff, C., & Hummel, F. C. (2011) Coordination of uncoupled bimanual movements by strictly timed interhemispheric connectivity. Journal of Neuroscience, 31(25), 9111-9117.
Maslovat, D., Carter, M. J., & Carlsen, A. N. (2017) Response preparation and execution during intentional bimanual pattern switching. Journal of Neurophysiology, 118(3), 1720-1731.
Maslovat, D., Teku, F., Smith, V., Drummond, N. M., & Carlsen, A. N. (2020) Bimanual but not unimanual finger movements are triggered by a startling acoustic stimulus: evidence for increased reticulospinal drive for bimanual responses. Journal of Neurophysiology, 124(6), 1832-1838.
Matsuyama, K., Takakusaki, K., Nakajima, K., & Mori, S. (1997) Multi-segmental innervation of single pontine reticulospinal axons in the cervico-thoracic region of the cat: Anterograde PHA-L tracing study. Journal of Comparative Neurology, 377(2), 234-250.
Mcpherson, J. G., Chen, A., Ellis, M. D., Yao, J., Heckman, C. J., & Dewald, J. P. A. (2018) Progressive recruitment of contralesional cortico-reticulospinal pathways drives motor impairment post stroke. The Journal of Physiology, 596(7), 1211-1225.
Meyer, B.-U., Röricht, S., Von Einsiedel, H. G., Kruggel, F., & Weindl, A. (1995) Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain, 118 (Pt 2), 429-440.
Morecraft, R. J., Ge, J., Stilwell-Morecraft, K. S., Mcneal, D. W., Pizzimenti, M. A., & Darling, W. G. (2013) Terminal distribution of the corticospinal projection from the hand/arm region of the primary motor cortex to the cervical enlargement in rhesus monkey. Journal of Comparative Neurology, 521(18), 4205-4235.
Naranjo, E. N., Allum, J. H. J., Inglis, J. T., & Carpenter, M. G. (2015) Increased gain of vestibulospinal potentials evoked in neck and leg muscles when standing under height-induced postural threat. Neuroscience, 293, 45-54.
Nonnekes, J., Carpenter, M. G., Inglis, J. T., Duysens, J., & Weerdesteyn, V. (2015) What startles tell us about control of posture and gait. Neuroscience and Biobehavioral Reviews, 53, 131-138.
Nonnekes, J., Oude Nijhuis, L. B., De Niet, M., De Bot, S. T., Pasman, J. W., Van De Warrenburg, B. P. C., Bloem, B. R., Weerdesteyn, V., & Geurts, A. C. (2014) StartReact restores reaction time in HSP: Evidence for subcortical release of a motor program. Journal of Neuroscience, 34(1), 275-281.
Ornitz, E. M., & Guthrie, D. (1989) Long-term habituation and sensitization of the acoustic startle response in the normal adult human. Psychophysiology, 26(2), 166-173.
Pataky, T. C. (2012) One-dimensional statistical parametric mapping in Python. Computer Methods in Biomechanics and Biomedical Engineering, 15(3), 295-301.
Pataky, T. C., Robinson, M. A., & Vanrenterghem, J. (2013) Vector field statistical analysis of kinematic and force trajectories. Journal of Biomechanics, 46(14), 2394-2401.
Riddle, C. N., Edgley, S. A., & Baker, S. N. (2009) Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. Journal of Neuroscience, 29(15), 4993-4999.
Rothwell, J. C. (2006) The startle reflex, voluntary movement, and the reticulospinal tract. Supplements to Clinical Neurophysiology, 58, 223-231.
Schrafl-Altermatt, M., & Dietz, V. (2016) Cooperative hand movements in post-stroke subjects: Neural reorganization. Clinical Neurophysiology, 127(1), 748-754.
Soska, K. C., Galeon, M. A., & Adolph, K. E. (2012) On the other hand: overflow movements of infants' hands and legs during unimanual object exploration. Developmental Psychobiology, 54(4), 372-382.
Tapia, J. A., Tohyama, T., Poll, A., & Baker, S. N. (2022) The existence of the startreact effect implies reticulospinal, not corticospinal, inputs dominate drive to motoneurons during voluntary movement. Journal of Neuroscience, 42(40), 7634-7647.
Tazoe, T., & Perez, M. A. (2017) Cortical and reticular contributions to human precision and power grip. The Journal of Physiology, 595(8), 2715-2730.
Thomas, F. A., Dietz, V., & Schrafl-Altermatt, M. (2018) Automatic gain control of neural coupling during cooperative hand movements. Scientific Reports, 8(1), 5959.
Valls-Sole, J. (2012) Assessment of excitability in brainstem circuits mediating the blink reflex and the startle reaction. Clinical Neurophysiology, 123(1), 13-20.
Valls-Solé, J., Kumru, H., & Kofler, M. (2008) Interaction between startle and voluntary reactions in humans. Experimental Brain Research, 187(4), 497-507.
Valls-Solé, J., Rothwell, J. C., Goulart, F., Cossu, G., & Muñoz, E. (1999) Patterned ballistic movements triggered by a startle in healthy humans. The Journal of Physiology, 516 (Pt 3), 931-938.
Yeomans, J. S., & Frankland, P. W. (1995) The acoustic startle reflex: Neurons and connections. Brain Research Brain Research Reviews, 21(3), 301-314.
Ziemann, U., Ishii, K., Borgheresi, A., Yaseen, Z., Battaglia, F., Hallett, M., Cincotta, M., & Wassermann, E. M. (1999) Dissociation of the pathways mediating ipsilateral and contralateral motor-evoked potentials in human hand and arm muscles. The Journal of Physiology, 518 (Pt 3), 895-906.