Academic Journal
Skeletal Motor Unit Recruitment During Periodic Auditory Cueing: A Simultaneous Behavioral and Motor Unit Magnetic Resonance Imaging (MUMRI) Study.
| Title: | Skeletal Motor Unit Recruitment During Periodic Auditory Cueing: A Simultaneous Behavioral and Motor Unit Magnetic Resonance Imaging (MUMRI) Study. |
|---|---|
| Authors: | Wang A; Newcastle University, Translational and Clinical Research Institute (NUTCRI), Newcastle University, Newcastle upon Tyne, UK., Schofield I; Newcastle University, Translational and Clinical Research Institute (NUTCRI), Newcastle University, Newcastle upon Tyne, UK., Birkbeck MG; Newcastle University, Translational and Clinical Research Institute (NUTCRI), Newcastle University, Newcastle upon Tyne, UK.; Northern Medical Physics and Clinical Engineering, Freeman Hospital, Newcastle Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK., Baxter-Beard D; Newcastle University, Translational and Clinical Research Institute (NUTCRI), Newcastle University, Newcastle upon Tyne, UK., Blamire AM; Newcastle University, Translational and Clinical Research Institute (NUTCRI), Newcastle University, Newcastle upon Tyne, UK., Whittaker RG; Newcastle University, Translational and Clinical Research Institute (NUTCRI), Newcastle University, Newcastle upon Tyne, UK. |
| Source: | NMR in biomedicine [NMR Biomed] 2026 Aug; Vol. 39 (8), pp. e70347. |
| Publication Type: | Journal Article |
| Language: | English |
| Journal Info: | Publisher: Wiley Country of Publication: England NLM ID: 8915233 Publication Model: Print Cited Medium: Internet ISSN: 1099-1492 (Electronic) Linking ISSN: 09523480 NLM ISO Abbreviation: NMR Biomed Subsets: MEDLINE |
| Imprint Name(s): | Publication: Chichester : Wiley Original Publication: London : Heyden & Son, 1988- |
| MeSH Terms: | Muscle, Skeletal*/physiology , Recruitment, Neurophysiological*/physiology , Motor Neurons*/physiology , Magnetic Resonance Imaging* , Cues* , Periodicity* , Behavior*, Muscle Contraction/physiology ; Humans ; Male ; Female ; Adult ; Reproducibility of Results ; Young Adult ; Acoustic Stimulation |
| Abstract: | Rhythmic motor paradigms are widely used to study sensorimotor timing, yet magnetic resonance imaging (MRI) research has largely focused on central processes, with limited insight into peripheral neuromuscular mechanisms. Motor unit MRI (MUMRI), a motion-sensitive technique in which muscle contraction induces intravoxel water redistribution and transient signal attenuation, enables in vivo visualization of muscle activity. In this study, we developed and validated a combined behavioral-MUMRI paradigm to characterize muscle recruitment during rhythmic foot tapping. Healthy participants performed an auditory-paced tapping task inside an MRI scanner while timing was recorded via an MRI-compatible force transducer and muscle activity was measured using single-slice MUMRI. A variable-latency cueing design systematically sampled the temporal relationship between auditory cues, motor execution, and image acquisition, allowing identification of the optimal latency window for detecting contraction-related signal changes. Fixed-latency acquisitions were then used to assess reproducibility. Behavioral results showed stable performance across conditions, with low variability in tapping accuracy (mean coefficient of variation [CoV] ≈0.078). Transient, localized signal reductions consistent with muscle contraction were observed in anterior lower leg muscles during dorsiflexion. Voxel-wise analyses demonstrated high within-condition reproducibility and latency-dependent spatial patterns, with the greatest average consistency when tapping aligned with scanner rhythm (r ≈0.68). These findings establish a robust framework for integrating rhythmic motor tasks with MUMRI, highlighting the importance of precise temporal alignment for reliable measurement of muscle activity. This approach provides a reproducible method for linking motor behavior to peripheral neuromuscular dynamics and offers potential for advancing both basic and clinical MRI research. (© 2026 The Author(s). NMR in Biomedicine published by John Wiley & Sons Ltd.) |
| References: | B. H. Repp, “Sensorimotor Synchronization: A Review of the Tapping Literature,” Psychonomic Bulletin & Review 12 (2005): 969–992. T. Fujioka, B. Ross, and L. J. Trainor, “Beta‐Band Oscillations Represent Auditory Beat and Its Metrical Hierarchy in Perception and Imagery,” Journal of Neuroscience 35 (2015): 15187–15198. J. A. Grahn and M. Brett, “Rhythm and Beat Perception in Motor Areas of the Brain,” Journal of Cognitive Neuroscience 19 (2007): 893–906. J. L. Chen, R. J. Zatorre, and V. B. Penhune, “Interactions Between Auditory and Dorsal Premotor Cortex During Synchronization to Musical Rhythms,” NeuroImage 32 (2006): 1771–1781. J. M. Ross and R. Balasubramaniam, “Physical and Neural Entrainment to Rhythm: Human Sensorimotor Coordination Across Tasks and Effector Systems,” Frontiers in Human Neuroscience 8 (2014): 576. M. H. Thaut and V. Hoemberg, Handbook of Neurologic Music Therapy, eds. M. H. Thaut and V. Hoemberg (Oxford University Press, 2014), 372. C. Nombela, L. E. Hughes, A. M. Owen, and J. A. Grahn, “Into the Groove: Can Rhythm Influence Parkinson's Disease?” Neuroscience and Biobehavioral Reviews 37 (2013): 2564–2570. M. Roerdink, C. J. Lamoth, J. van Kordelaar, et al., “Rhythm Perturbations in Acoustically Paced Treadmill Walking After Stroke,” Neurorehabilitation and Neural Repair 23 (2009): 668–678. R. L. Wright and M. T. Elliott, “Stepping to Phase‐Perturbed Metronome Cues: Multisensory Advantage in Movement Synchrony but Not Correction,” Frontiers in Human Neuroscience 8 (2014): 724. C. la Fougère, A. Zwergal, A. Rominger, et al., “Real Versus Imagined Locomotion: A [18F]‐FDG PET‐fMRI Comparison,” NeuroImage 50 (2010): 1589–1598. H. P. Sigurdsson, L. Alcock, M. Firbank, et al., “Developing a Novel Dual‐Injection FDG‐PET Imaging Methodology to Study the Functional Neuroanatomy of Gait,” NeuroImage 288 (2024): 120531. M. G. Birkbeck, L. Heskamp, I. S. Schofield, A. M. Blamire, and R. G. Whittaker, “Non‐Invasive Imaging of Single Human Motor Units,” Clinical Neurophysiology 131 (2020): 1399–1406. L. Heskamp, A. R. Miller, M. G. Birkbeck, et al., “In Vivo 3D Imaging of Human Motor Units in Upper and Lower Limb Muscles,” Clinical Neurophysiology 141 (2022): 91–100. L. Heskamp, M. G. Birkbeck, R. G. Whittaker, I. S. Schofield, and A. M. Blamire, “The Muscle Twitch Profile Assessed With Motor Unit Magnetic Resonance Imaging,” NMR in Biomedicine 34 (2021): e4466. C. Rorden, “MRIcroGL: Voxel‐Based Visualization for Neuroimaging,” Nature Methods 22 (2025): 1613–1614. E. C. Argentieri, E. T. Tan, J. S. Whang, et al., “Quantitative T(2) ‐Mapping Magnetic Resonance Imaging for Assessment of Muscle Motor Unit Recruitment Patterns,” Muscle & Nerve 63 (2021): 703–709. J. Schindelin, I. Arganda‐Carreras, E. Frise, et al., “Fiji: An Open‐Source Platform for Biological‐Image Analysis,” Nature Methods 9 (2012): 676–682. M. Pranjić, T. Braun Janzen, N. Vukšić, and M. Thaut, “From Sound to Movement: Mapping the Neural Mechanisms of Auditory‐Motor Entrainment and Synchronization,” Brain Sciences 14 (2024): 1063. D. Rose, L. Ott, S. M. R. Guérin, L. E. Annett, P. Lovatt, and Y. N. Delevoye‐Turrell, “A General Procedure to Measure the Pacing of Body Movements Timed to Music and Metronome in Younger and Older Adults,” Scientific Reports 11 (2021): 3264. D. Hammerschmidt and C. Wöllner, “Spontaneous Motor Tempo Over the Course of a Week: The Role of the Time of the Day, Chronotype, and Arousal,” Psychological Research 87 (2023): 327–338. D. Rose, D. J. Cameron, P. J. Lovatt, J. A. Grahn, and L. E. Annett, “Comparison of Spontaneous Motor Tempo During Finger Tapping, Toe Tapping and Stepping on the Spot in People With and Without Parkinson's Disease,” Journal of Movement Disorders 13 (2020): 47–56. A. Desbernats, E. Martin, and J. Tallet, “Which Factors Modulate Spontaneous Motor Tempo? A Systematic Review of the Literature,” Frontiers in Psychology 14 (2023): 1161052. B. H. Repp and Y. H. Su, “Sensorimotor Synchronization: A Review of Recent Research (2006‐2012),” Psychonomic Bulletin & Review 20 (2013): 403–452. W. Qi, T. Nakajima, M. Sakamoto, K. Kato, Y. Kawakami, and K. Kanosue, “Walking and Finger Tapping Can Be Done With Independent Rhythms,” Scientific Reports 9 (2019): 7620. M. G. Birkbeck, A. M. Blamire, R. G. Whittaker, A. A. Sayer, and R. M. Dodds, “The Role of Novel Motor Unit Magnetic Resonance Imaging to Investigate Motor Unit Activity in Ageing Skeletal Muscle,” Journal of Cachexia, Sarcopenia and Muscle 12 (2021): 17–29. D. K. Jones and M. Cercignani, “Twenty‐Five Pitfalls in the Analysis of Diffusion MRI Data,” NMR in Biomedicine 23 (2010): 803–820. R. A. Poldrack, J. A. Mumford, and T. E. Nichols, Handbook of Functional MRI Data Analysis (Cambridge University Press, 2011). N. Novitski, I. Anourova, S. Martinkauppi, H. J. Aronen, R. Näätänen, and S. Carlson, “Effects of Noise From Functional Magnetic Resonance Imaging on Auditory Event‐Related Potentials in Working Memory Task,” NeuroImage 20 (2003): 1320–1328. C. J. Scarff, J. C. Dort, J. J. Eggermont, and B. G. Goodyear, “The Effect of MR Scanner Noise on Auditory Cortex Activity Using fMRI,” Human Brain Mapping 22 (2004): 341–349. K. Tomyta, H. Ohira, and K. Katahira, “Asymmetric Error Correction in the Synchronization Tapping Task,” Timing & Time Perception 13 (2023): 25–34. J. Yang, F. Ouyang, L. Holm, et al., “A Mechanism of Timing Variability Underlying the Association Between the Mean and SD of Asynchrony,” Human Movement Science 67 (2019): 102500. M. de Carvalho, A. Turkman, and M. Swash, “Motor Unit Firing in Amyotrophic Lateral Sclerosis and Other Upper and Lower Motor Neurone Disorders,” Clinical Neurophysiology 123 (2012): 2312–2318. B. Emeryk‐Szajewska, J. Kopéc, and A. Karwanska, “The Reorganization of Motor Units in Motor Neuron Disease,” Muscle & Nerve 20 (1997): 306–315. |
| Grant Information: | 2023/MNDS/6300/740WHIT MND Scotland |
| Contributed Indexing: | Keywords: foot tapping; motor unit MRI; neuromuscular recruitment; rhythmic motor entrainment |
| Entry Date(s): | Date Created: 20260706 Date Completed: 20260706 Latest Revision: 20260726 |
| Update Code: | 20260726 |
| PubMed Central ID: | PMC13333902 |
| DOI: | 10.1002/nbm.70347 |
| PMID: | 42402730 |
| Database: | MEDLINE |
| ISSN: | 1099-1492 |
|---|---|
| DOI: | 10.1002/nbm.70347 |