Abstract
Inhibition is a key cognitive control mechanism humans use to enable goal-directed behavior. When rapidly exerted, inhibitory control has broad, nonselective motor effects, typically demonstrated using corticospinal excitability measurements (CSE) elicited by transcranial magnetic stimulation (TMS). For example, during rapid action-stopping, CSE is suppressed at both stopped and task-unrelated muscles. While such TMS-based CSE measurements have provided crucial insights into the fronto-basal ganglia circuitry underlying inhibitory control, they have several downsides. TMS is contraindicated in many populations (e.g., epilepsy or deep-brain stimulation patients), has limited temporal resolution, produces distracting auditory and haptic stimulation, is difficult to combine with other imaging methods, and necessitates expensive, immobile equipment. Here, we attempted to measure the nonselective motor effects of inhibitory control using a method unaffected by these shortcomings. Thirty male and female human participants exerted isometric force on a high-precision handheld force transducer while performing a foot-response stop-signal task. Indeed, when foot movements were successfully stopped, force output at the task-irrelevant hand was suppressed as well. Moreover, this nonselective reduction of isometric force was highly correlated with stop-signal performance and showed frequency dynamics similar to established inhibitory signatures typically found in neural and muscle recordings. Together, these findings demonstrate that isometric force recordings can reliably capture the nonselective effects of motor inhibition, opening the door to many applications that are hard or impossible to realize with TMS.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Code availability
References
Almuklass, A. M., Price, R. C., Gould, J. R., & Enoka, R. M. (2016). Force steadiness as a predictor of time to complete a pegboard test of dexterity in young men and women. Journal of Applied Physiology, 120(12), 1410–1417. https://doi.org/10.1152/japplphysiol.01051.2015
Androulidakis, A. G., Doyle, L. M. F., Yarrow, K., Litvak, V., Gilbertson, T. P., & Brown, P. (2007). Anticipatory changes in beta synchrony in the human corticospinal system and associated improvements in task performance. European Journal of Neuroscience, 25(12), 3758–3765. https://doi.org/10.1111/j.1460-9568.2007.05620.x
Aron, A. R., & Poldrack, R. A. (2006). Cortical and subcortical contributions to stop signal response inhibition: Role of the subthalamic nucleus. The Journal of Neuroscience, 26(9), 2424–2433. https://doi.org/10.1523/jneurosci.4682-05.2006
Badawy, R. A. B., Jackson, G. D., Berkovic, S. F., & MacDonell, R. A. L. (2013). Cortical excitability and refractory epilepsy: A three-year longitudinal transcranial magnetic stimulation study. International Journal of Neural Systems, 23(01), 1250030. https://doi.org/10.1142/s012906571250030x
Badry, R., Mima, T., Aso, T., Nakatsuka, M., Abe, M., Fathi, D., Foly, N., Nagiub, H., Nagamine, T., & Fukuyama, H. (2009). Suppression of human cortico-motoneuronal excitability during the stop-signal task. Clinical Neurophysiology, 120(9), 1717–1723. https://doi.org/10.1016/j.clinph.2009.06.027
Baker, S. N. (2007). Oscillatory interactions between sensorimotor cortex and the periphery. Current Opinion in Neurobiology, 17(6), 649–655. https://doi.org/10.1016/j.conb.2008.01.007
Bestmann, S., & Duque, J. (2016). Transcranial magnetic stimulation: Decomposing the processes underlying action preparation. The Neuroscientist, 22(4), 392–405. https://doi.org/10.1177/1073858415592594
Bonaiuto, J. J., Little, S., Neymotin, S. A., Jones, S. R., Barnes, G. R., & Bestmann, S. (2021). Laminar dynamics of high amplitude beta bursts in human motor cortex. NeuroImage, 242, 118479. https://doi.org/10.1016/j.neuroimage.2021.118479
Bourguignon, M., Piitulainen, H., Smeds, E., Zhou, G., Jousmäki, V., & Hari, R. (2017). MEG insight into the spectral dynamics underlying steady isometric muscle contraction. The Journal of Neuroscience, 37(43), 10421–10437. https://doi.org/10.1523/jneurosci.0447-17.2017
Bourguignon, M., Piitulainen, H., Tiège, X. D., Jousmäki, V., & Hari, R. (2015). Corticokinematic coherence mainly reflects movement-induced proprioceptive feedback. NeuroImage, 106, 382–390. https://doi.org/10.1016/j.neuroimage.2014.11.026
Bräcklein, M., Barsakcioglu, D. Y., Vecchio, A. D., Ibáñez, J., & Farina, D. (2022). Reading and modulating cortical β bursts from motor unit spiking activity. The Journal of Neuroscience, 42(17), 3611–3621. https://doi.org/10.1523/jneurosci.1885-21.2022
Brainard, D. H. (1997). The psychophysics toolbox. Spatial Vision, 10(4), 433–436. https://doi.org/10.1163/156856897x00357
Cavanagh, J. F., Sanguinetti, J. L., Allen, J. J. B., Sherman, S. J., & Frank, M. J. (2014). The subthalamic nucleus contributes to post-error slowing. Journal of Cognitive Neuroscience, 26(11), 2637–2644. https://doi.org/10.1162/jocn_a_00659
Chen, W., de Hemptinne, C., Miller, A. M., Leibbrand, M., Little, S. J., Lim, D. A., Larson, P. S., & Starr, P. A. (2020). Prefrontal-subthalamic Hyperdirect pathway modulates movement inhibition in humans. Neuron, 106(4), 579–588.e3. https://doi.org/10.1016/j.neuron.2020.02.012
Chowdhury, N. S., Livesey, E. J., Blaszczynski, A., & Harris, J. A. (2018). Variations in response control within at-risk gamblers and non-gambling controls explained by GABAergic inhibition in the motor cortex. Cortex, 103, 153–163. https://doi.org/10.1016/j.cortex.2018.03.004
Christou, E. A., Jakobi, J. M., Critchlow, A., Fleshner, M., & Enoka, R. M. (2004). The 1- to 2-Hz oscillations in muscle force are exacerbated by stress, especially in older adults. Journal of Applied Physiology, 97(1), 225–235. https://doi.org/10.1152/japplphysiol.00066.2004
Conway, B. A., Halliday, D. M., Farmer, S. F., Shahani, U., Maas, P., Weir, A. I., & Rosenberg, J. R. (1995). Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. The Journal of Physiology, 489(3), 917–924. https://doi.org/10.1113/jphysiol.1995.sp021104
Cook, R. D. (1977). Detection of influential observation in linear regression. Technometrics, 19(1), 15–18. https://doi.org/10.1080/00401706.1977.10489493
Coxon, J. P., Impe, A. V., Wenderoth, N., & Swinnen, S. P. (2012). Aging and inhibitory control of action: Cortico-subthalamic connection strength predicts stopping performance. Journal of Neuroscience, 32(24), 8401–8412. https://doi.org/10.1523/jneurosci.6360-11.2012
Coxon, J. P., Stinear, C. M., & Byblow, W. D. (2006). Intracortical inhibition during volitional inhibition of prepared action. Journal of Neurophysiology, 95(6), 3371–3383. https://doi.org/10.1152/jn.01334.2005
Davis, L. A., Alenazy, M. S., Almuklass, A. M., Feeney, D. F., Vieira, T., Botter, A., & Enoka, R. M. (2020). Force control during submaximal isometric contractions is associated with walking performance in persons with multiple sclerosis. Journal of Neurophysiology, 123(6), 2191–2200. https://doi.org/10.1152/jn.00085.2020
Dutra, I. C., Waller, D. A., & Wessel, J. R. (2018). Perceptual surprise improves action stopping by nonselectively suppressing motor activity via a neural mechanism for motor inhibition. Journal of Neuroscience, 38(6), 1482–1492. https://doi.org/10.1523/jneurosci.3091-17.2017
Echeverria-Altuna, I., Quinn, A. J., Zokaei, N., Woolrich, M. W., Nobre, A. C., & Ede, F. van. (2022). Transient beta activity and cortico-muscular connectivity during sustained motor behaviour. Progress in Neurobiology, 214, 102281. https://doi.org/10.1016/j.pneurobio.2022.102281
Ede, F. van, Winner, T., & Maris, E. (2015). Touch automatically upregulates motor readiness in humans. Journal of Neurophysiology, 114(6), 3121–3130. https://doi.org/10.1152/jn.00504.2015
Enoka, R. M., Christou, E. A., Hunter, S. K., Kornatz, K. W., Semmler, J. G., Taylor, A. M., & Tracy, B. L. (2003). Mechanisms that contribute to differences in motor performance between young and old adults. Journal of Electromyography and Kinesiology, 13(1), 1–12. https://doi.org/10.1016/s1050-6411(02)00084-6
Enoka, R. M., & Farina, D. (2021). Force steadiness: From motor units to voluntary actions. Physiology, 36(2), 114–130. https://doi.org/10.1152/physiol.00027.2020
Erika-Florence, M., Leech, R., & Hampshire, A. (2014). A functional network perspective on response inhibition and attentional control. Nature Communications, 5(1), 4073. https://doi.org/10.1038/ncomms5073
Farina, D., Negro, F., Gizzi, L., & Falla, D. (2012). Low-frequency oscillations of the neural drive to the muscle are increased with experimental muscle pain. Journal of Neurophysiology, 107(3), 958–965. https://doi.org/10.1152/jn.00304.2011
Feeney, D. F., Mani, D., & Enoka, R. M. (2018). Variability in common synaptic input to motor neurons modulates both force steadiness and pegboard time in young and older adults. The Journal of Physiology, 596(16), 3793–3806. https://doi.org/10.1113/jp275658
Feingold, J., Gibson, D. J., DePasquale, B., & Graybiel, A. M. (2015). Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks. Proceedings of the National Academy of Sciences, 112(44), 13687–13692. https://doi.org/10.1073/pnas.1517629112
Fiori, F., Chiappini, E., Candidi, M., Romei, V., Borgomaneri, S., & Avenanti, A. (2017). Long-latency interhemispheric interactions between motor-related areas and the primary motor cortex: A dual site TMS study. Scientific Reports, 7(1), 14936. https://doi.org/10.1038/s41598-017-13708-2
Fitzgerald, P. B., Fountain, S., & Daskalakis, Z. J. (2006). A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clinical Neurophysiology, 117(12), 2584–2596. https://doi.org/10.1016/j.clinph.2006.06.712
Frank, M. J., Samanta, J., Moustafa, A. A., & Sherman, S. J. (2007). Hold your horses: Impulsivity, deep brain stimulation, and medication in parkinsonism. Science, 318(5854), 1309–1312. https://doi.org/10.1126/science.1146157
Galganski, M. E., Fuglevand, A. J., & Enoka, R. M. (1993). Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. Journal of Neurophysiology, 69(6), 2108–2115. https://doi.org/10.1152/jn.1993.69.6.2108
Goode, C., Cole, D. M., & Bolton, D. A. E. (2019). Staying upright by shutting down? Evidence for global suppression of the motor system when recovering balance. Gait & Posture, 70, 260–263. https://doi.org/10.1016/j.gaitpost.2019.03.018
Guan, Y., & Wessel, J. R. (2022). Two types of motor inhibition after action errors in humans. The journal of neuroscience, JN-RM-1191-22. https://doi.org/10.1523/jneurosci.1191-22.2022.
Hallett, M., & Chokroverty, S. (2006). Magnetic stimulation in clinical neurophysiology. 2nd ed. American Journal of Neuroradiology, 27(8), 1799. http://www.ajnr.org/content/27/8/1799.abstract. Accessed 16 Oct 2022
Hamada, M., Galea, J. M., Lazzaro, V. D., Mazzone, P., Ziemann, U., & Rothwell, J. C. (2014). Two distinct interneuron circuits in human motor cortex are linked to different subsets of physiological and behavioral plasticity. The Journal of Neuroscience, 34(38), 12837–12849. https://doi.org/10.1523/jneurosci.1960-14.2014
Hannah, R., & Rothwell, J. C. (2017). Pulse duration as well as current direction determines the specificity of transcranial magnetic stimulation of motor cortex during contraction. Brain Stimulation, 10(1), 106–115. https://doi.org/10.1016/j.brs.2016.09.008
Herz, D. M., Tan, H., Brittain, J.-S., Fischer, P., Cheeran, B., Green, A. L., FitzGerald, J., Aziz, T. Z., Ashkan, K., Little, S., Foltynie, T., Limousin, P., Zrinzo, L., Bogacz, R., & Brown, P. (2017). Distinct mechanisms mediate speed-accuracy adjustments in cortico-subthalamic networks. ELife, 6, e21481. https://doi.org/10.7554/elife.21481
Hyngstrom, A. S., Kuhnen, H. R., Kirking, K. M., & Hunter, S. K. (2014). Functional implications of impaired control of submaximal hip flexion following stroke. Muscle & Nerve, 49(2), 225–232. https://doi.org/10.1002/mus.23886
Ilmoniemi, R. J., Hernandez-Pavon, J. C., Mäkelä, N. N., Metsomaa, J., Mutanen, T. P., Stenroos, M., & Sarvas, J. (2015). Dealing with artifacts in TMS-evoked EEG. In 2015 37th annual international conference of the IEEE engineering in medicine and biology society (EMBC), 2015 (pp. 230–233). https://doi.org/10.1109/embc.2015.7318342
Jahanshahi, M., & Rothwell, J. C. (2017). Inhibitory dysfunction contributes to some of the motor and non-motor symptoms of movement disorders and psychiatric disorders. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 372(1718), 20160198. https://doi.org/10.1098/rstb.2016.0198
Jana, S., Hannah, R., Muralidharan, V., & Aron, A. R. (2020). Temporal cascade of frontal, motor and muscle processes underlying human action-stopping. ELife, 9, e50371. https://doi.org/10.7554/elife.50371
Jong, R. D., Coles, M. G. H., Logan, G. D., & Gratton, G. (1990). In search of the point of no return: The control of response processes. Journal of Experimental Psychology: Human Perception and Performance, 16(1), 164–182. https://doi.org/10.1037/0096-1523.16.1.164
Kato, K., Watanabe, T., & Kanosue, K. (2015). Effects of muscle relaxation on sustained contraction of ipsilateral remote muscle. Physiological Reports, 3(11), e12620. https://doi.org/10.14814/phy2.12620
Kawakita, H., Kameyama, O., Ogawa, R., Hayes, K. C., Wolfe, D. L., & Allatt, R. D. (1991). Reinforcement of motor evoked potentials by remote muscle contraction. Journal of Electromyography and Kinesiology, 1(2), 96–106. https://doi.org/10.1016/1050-6411(91)90003-n
Kok, A., Ramautar, J. R., Ruiter, M. B. D., Band, G. P. H., & Ridderinkhof, K. R. (2004). ERP components associated with successful and unsuccessful stopping in a stop-signal task. Psychophysiology, 41(1), 9–20. https://doi.org/10.1046/j.1469-8986.2003.00127.x
Komeilipoor, N., Ilmoniemi, R. J., Tiippana, K., Vainio, M., Tiainen, M., & Vainio, L. (2017). Preparation and execution of teeth clenching and foot muscle contraction influence on corticospinal hand-muscle excitability. Scientific Reports, 7(1), 41249. https://doi.org/10.1038/srep41249
Kouzaki, M., & Shinohara, M. (2010). Steadiness in plantar flexor muscles and its relation to postural sway in young and elderly adults. Muscle & Nerve, 42(1), 78–87. https://doi.org/10.1002/mus.21599
Lazzaro, V. D., & Rothwell, J. C. (2014). Corticospinal activity evoked and modulated by non-invasive stimulation of the intact human motor cortex. The Journal of Physiology, 592(19), 4115–4128. https://doi.org/10.1113/jphysiol.2014.274316
Leocani, L., Cohen, L. G., Wassermann, E. M., Ikoma, K., & Hallett, M. (2000). Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain, 123(6), 1161–1173. https://doi.org/10.1093/brain/123.6.1161
Leventhal, D. K., Gage, G. J., Schmidt, R., Pettibone, J. R., Case, A. C., & Berke, J. D. (2012). Basal ganglia Beta oscillations accompany Cue utilization. Neuron, 73(3), 523–536. https://doi.org/10.1016/j.neuron.2011.11.032
Logan, G. D., Cowan, W. B., & Davis, K. A. (1984). On the ability to inhibit simple and choice reaction time responses: A model and a method. Journal of Experimental Psychology: Human Perception and Performance, 10(2), 276–291. https://doi.org/10.1037/0096-1523.10.2.276
Majid, D. S. A., Cai, W., George, J. S., Verbruggen, F., & Aron, A. R. (2012). Transcranial magnetic stimulation reveals dissociable mechanisms for global versus selective Corticomotor suppression underlying the stopping of action. Cerebral Cortex, 22(2), 363–371. https://doi.org/10.1093/cercor/bhr112
Mani, D., Almuklass, A. M., Hamilton, L. D., Vieira, T. M., Botter, A., & Enoka, R. M. (2018). Motor unit activity, force steadiness, and perceived fatigability are correlated with mobility in older adults. Journal of Neurophysiology, 120(4), 1988–1997. https://doi.org/10.1152/jn.00192.2018
Matzke, D., Verbruggen, F., & Logan, G. D. (2018). Stevens’ handbook of experimental psychology and cognitive neuroscience. 1–45. https://doi.org/10.1002/9781119170174.epcn510.
McFarland, D. J., Miner, L. A., Vaughan, T. M., & Wolpaw, J. R. (2000). Mu and Beta rhythm topographies during motor imagery and actual movements. Brain Topography, 12(3), 177–186. https://doi.org/10.1023/a:1023437823106
Miocinovic, S., Hemptinne, C. de, Chen, W., Isbaine, F., Willie, J. T., Ostrem, J. L., & Starr, P. A. (2018). Cortical potentials evoked by subthalamic stimulation demonstrate a short latency Hyperdirect pathway in humans. The Journal of Neuroscience, 38(43), 9129–9141. https://doi.org/10.1523/jneurosci.1327-18.2018
Mongold, S. J., Piitulainen, H., Legrand, T., Ghinst, M. V., Naeije, G., Jousmäki, V., & Bourguignon, M. (2022). Temporally stable beta sensorimotor oscillations and corticomuscular coupling underlie force steadiness. NeuroImage, 261, 119491. https://doi.org/10.1016/j.neuroimage.2022.119491
Nambu, A., Tokuno, H., & Takada, M. (2002). Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway. Neuroscience Research, 43(2), 111–117. https://doi.org/10.1016/s0168-0102(02)00027-5
Novembre, G., & Iannetti, G. D. (2021). Towards a unified neural mechanism for reactive adaptive behaviour. Progress in Neurobiology, 204, 102115. https://doi.org/10.1016/j.pneurobio.2021.102115
Novembre, G., Pawar, V., Bufacchi, R., Kilintari, M., Srinivasan, M., Rothwell, J., Haggard, P., & Iannetti, G. (2018). Saliency detection as a reactive process: Unexpected sensory events evoke cortico-muscular coupling. Journal of Neuroscience, 38(9), 2474–2417. https://doi.org/10.1523/jneurosci.2474-17.2017
Novembre, G., Pawar, V. M., Kilintari, M., Bufacchi, R. J., Guo, Y., Rothwell, J. C., & Iannetti, G. D. (2019). The effect of salient stimuli on neural oscillations, isometric force, and their coupling. NeuroImage, 198, 221–230. https://doi.org/10.1016/j.neuroimage.2019.05.032
Pfurtscheller, G., Graimann, B., Huggins, J. E., Levine, S. P., & Schuh, L. A. (2003). Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clinical Neurophysiology, 114(7), 1226–1236. https://doi.org/10.1016/s1388-2457(03)00067-1
Picazio, S., Veniero, D., Ponzo, V., Caltagirone, C., Gross, J., Thut, G., & Koch, G. (2014). Prefrontal control over Motor cortex cycles at Beta frequency during movement inhibition. Current Biology, 24(24), 2940–2945. https://doi.org/10.1016/j.cub.2014.10.043
Raud, L., Huster, R. J., Ivry, R. B., Labruna, L., Messel, M. S., & Greenhouse, I. (2020). A single mechanism for global and selective response inhibition under the influence of motor preparation. The Journal of Neuroscience, 40(41), 7921–7935. https://doi.org/10.1523/jneurosci.0607-20.2020
Rogasch, N. C., Sullivan, C., Thomson, R. H., Rose, N. S., Bailey, N. W., Fitzgerald, P. B., Farzan, F., & Hernandez-Pavon, J. C. (2017). Analysing concurrent transcranial magnetic stimulation and electroencephalographic data: A review and introduction to the open-source TESA software. NeuroImage, 147, 934–951. https://doi.org/10.1016/j.neuroimage.2016.10.031
Rossi, S., Antal, A., Bestmann, S., Bikson, M., Brewer, C., Brockmöller, J., Carpenter, L. L., Cincotta, M., Chen, R., Daskalakis, J. D., Lazzaro, V. D., Fox, M. D., George, M. S., Gilbert, D., Kimiskidis, V. K., Koch, G., Ilmoniemi, R. J., Lefaucheur, J. P., Leocani, L., et al. (2020). T. basis of this article began with a C. S. from the I. W. on “Present, Future of TMS: Safety, Ethical Guidelines”, Siena, October 17-20, 2018, updating through April. (2020). Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert Guidelines. Clinical Neurophysiology, 132(1), 269–306. https://doi.org/10.1016/j.clinph.2020.10.003
Sherman, M. A., Lee, S., Law, R., Haegens, S., Thorn, C. A., Hämäläinen, M. S., Moore, C. I., & Jones, S. R. (2016). Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice. Proceedings of the National Academy of Sciences, 113(33), E4885–E4894. https://doi.org/10.1073/pnas.1604135113
Shin, H., Law, R., Tsutsui, S., Moore, C. I., & Jones, S. R. (2017). The rate of transient beta frequency events predicts behavior across tasks and species. ELife, 6, e29086. https://doi.org/10.7554/elife.29086
Siegert, S., Ruiz, M. H., Brücke, C., Huebl, J., Schneider, G.-H., Ullsperger, M., & Kühn, A. A. (2014). Error signals in the subthalamic nucleus are related to post-error slowing in patients with Parkinson’s disease. Cortex, 60, 103–120. https://doi.org/10.1016/j.cortex.2013.12.008
Skinner, J. W., Christou, E. A., & Hass, C. J. (2019). Lower extremity muscle strength and force variability in persons with Parkinson disease. Journal of Neurologic Physical Therapy, 43(1), 56–62. https://doi.org/10.1097/npt.0000000000000244
Smith, M.-C., & Stinear, C. M. (2016). Transcranial magnetic stimulation (TMS) in stroke: Ready for clinical practice? Journal of Clinical Neuroscience, 31, 10–14. https://doi.org/10.1016/j.jocn.2016.01.034
Soh, C., Hynd, M., Rangel, B. O., & Wessel, J. R. (2021). Adjustments to proactive motor inhibition without effector-specific foreknowledge are reflected in a bilateral upregulation of sensorimotor β-burst rates. Journal of Cognitive Neuroscience, 33(5), 784–798. https://doi.org/10.1162/jocn_a_01682
Swann, N. C., Cai, W., Conner, C. R., Pieters, T. A., Claffey, M. P., George, J. S., Aron, A. R., & Tandon, N. (2012). Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: Electrophysiological responses and functional and structural connectivity. NeuroImage, 59(3), 2860–2870. https://doi.org/10.1016/j.neuroimage.2011.09.049
Swann, N., Tandon, N., Canolty, R., Ellmore, T. M., McEvoy, L. K., Dreyer, S., DiSano, M., & Aron, A. R. (2009). Intracranial EEG reveals a time- and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. Journal of Neuroscience, 29(40), 12675–12685. https://doi.org/10.1523/jneurosci.3359-09.2009
Tatz, J. R., Soh, C., & Wessel, J. R. (2021). Common and unique inhibitory control signatures of action-stopping and attentional capture suggest that actions are stopped in two stages. The journal of neuroscience, JN-RM-1105-21. https://doi.org/10.1523/jneurosci.1105-21.2021
Tazoe, T., Sakamoto, M., Nakajima, T., Endoh, T., Shiozawa, S., & Komiyama, T. (2009). Remote facilitation of supraspinal motor excitability depends on the level of effort. European Journal of Neuroscience, 30(7), 1297–1305. https://doi.org/10.1111/j.1460-9568.2009.06895.x
Verbruggen, F., Aron, A. R., Band, G. P., Beste, C., Bissett, P. G., Brockett, A. T., Brown, J. W., Chamberlain, S. R., Chambers, C. D., Colonius, H., Colzato, L. S., Corneil, B. D., Coxon, J. P., Dupuis, A., Eagle, D. M., Garavan, H., Greenhouse, I., Heathcote, A., Huster, R. J., & Boehler, C. N. (2019). A consensus guide to capturing the ability to inhibit actions and impulsive behaviors in the stop-signal task. ELife, 8, e46323. https://doi.org/10.7554/elife.46323
Volz, L. J., Hamada, M., Rothwell, J. C., & Grefkes, C. (2015). What makes the muscle twitch: Motor system connectivity and TMS-induced activity. Cerebral Cortex, 25(9), 2346–2353. https://doi.org/10.1093/cercor/bhu032
Wager, T. D., Sylvester, C.-Y. C., Lacey, S. C., Nee, D. E., Franklin, M., & Jonides, J. (2005). Common and unique components of response inhibition revealed by fMRI. NeuroImage, 27(2), 323–340. https://doi.org/10.1016/j.neuroimage.2005.01.054
Wagner, J., Wessel, J. R., Ghahremani, A., & Aron, A. R. (2018). Establishing a right frontal Beta signature for stopping action in scalp EEG: Implications for testing inhibitory control in other task contexts. Journal of Cognitive Neuroscience, 30(1), 107–118. https://doi.org/10.1162/jocn_a_01183
Wessel, J. R. (2020). β-Bursts reveal the trial-to-trial dynamics of movement initiation and cancellation. The Journal of Neuroscience, 40(2), 411–423. https://doi.org/10.1523/jneurosci.1887-19.2019
Wessel, J. R., & Aron, A. R. (2015). It’s not too late: The onset of the frontocentral P3 indexes successful response inhibition in the stop-signal paradigm. Psychophysiology, 52(4), 472–480. https://doi.org/10.1111/psyp.12374
Wessel, J. R., & Aron, A. R. (2017). On the Globality of motor suppression: Unexpected events and their influence on behavior and cognition. Neuron, 93(2), 259–280. https://doi.org/10.1016/j.neuron.2016.12.013
Wessel, J. R., Diesburg, D. A., Chalkley, N. H., & Greenlee, J. D. W. (2022). A causal role for the human subthalamic nucleus in non-selective cortico-motor inhibition. Current Biology, 32(17), 3785–3791.e3. https://doi.org/10.1016/j.cub.2022.06.067
Wessel, J. R., Jenkinson, N., Brittain, J.-S., Voets, S. H. E. M., Aziz, T. Z., & Aron, A. R. (2016). Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism. Nature Communications, 7(1), 11195. https://doi.org/10.1038/ncomms11195
Wessel, J. R., Reynoso, H. S., & Aron, A. R. (2013). Saccade suppression exerts global effects on the motor system. Journal of Neurophysiology, 110(4), 883–890. https://doi.org/10.1152/jn.00229.2013
Wessel, J. R., Waller, D. A., & Greenlee, J. D. (2019). Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism. ELife, 8, e42959. https://doi.org/10.7554/elife.42959
Wilson, J. M., Thompson, C. K., McPherson, L. M., Zadikoff, C., Heckman, C. J., & MacKinnon, C. D. (2020). Motor unit discharge variability is increased in mild-to-moderate Parkinson’s disease. Frontiers in Neurology, 11, 477. https://doi.org/10.3389/fneur.2020.00477
Witham, C. L., Riddle, C. N., Baker, M. R., & Baker, S. N. (2011). Contributions of descending and ascending pathways to corticomuscular coherence in humans. The Journal of Physiology, 589(15), 3789–3800. https://doi.org/10.1113/jphysiol.2011.211045
Zicher, B., Ibáñez, J., & Farina, D. (2022). Beta inputs to motor neurons do not directly contribute to volitional force modulation. The Journal of Physiology. https://doi.org/10.1113/jp283398
Acknowledgements
This work was funded by the National Science Foundation (NSF CAREER 1752355 to JRW). GN acknowledges support from the European Research Council (grant agreement 948186).
The data and materials reported here are available on the Open Science Framework ( https://osf.io/en8t9/ ) This experiment was not preregistered.
Funding
National Science Foundation (NSF CAREER 1752355 to JRW).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors report no financial conflict of interest.
Ethics approval
University of Iowa (IRB #201511709).
Consent to participate
Informed consent was obtained from all individual participants in the study.
Consent for publication
Participants gave informed consent as to the publishing of their data.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Significance statement
Inhibitory control allows humans to override inappropriate actions during goal-directed behavior. When inhibition is rapidly exerted on the motor system, it has broad, nonselective effects. For example, when a foot movement is rapidly stopped, other task-unrelated muscles also show signs of inhibition. This is typically shown using transcranial magnetic stimulation (TMS) of the motor cortex. However, TMS is contraindicated in many populations of interest, produces artifacts in neural recordings, is distracting to the subject, and has very limited time resolution. Here, we demonstrate clear nonselective effects of inhibitory control using isometric force recordings from a task-unrelated muscle during a stop-signal task. This simple method has high time resolution, no contraindications, and could be readily combined with other imaging methods.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rangel, B.O., Novembre, G. & Wessel, J.R. Measuring the nonselective effects of motor inhibition using isometric force recordings. Behav Res (2023). https://doi.org/10.3758/s13428-023-02197-z
Accepted:
Published:
DOI: https://doi.org/10.3758/s13428-023-02197-z