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Erschienen in: Experimental Brain Research 4/2017

01.04.2017 | Research Article

Cortical activity predicts good variation in human motor output

verfasst von: Sarine Babikian, Eva Kanso, Jason J. Kutch

Erschienen in: Experimental Brain Research | Ausgabe 4/2017

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Abstract

Human movement patterns have been shown to be particularly variable if many combinations of activity in different muscles all achieve the same task goal (i.e., are goal-equivalent). The nervous system appears to automatically vary its output among goal-equivalent combinations of muscle activity to minimize muscle fatigue or distribute tissue loading, but the neural mechanism of this “good” variation is unknown. Here we use a bimanual finger task, electroencephalography (EEG), and machine learning to determine if cortical signals can predict goal-equivalent variation in finger force output. 18 healthy participants applied left and right index finger forces to repeatedly perform a task that involved matching a total (sum of right and left) finger force. As in previous studies, we observed significantly more variability in goal-equivalent muscle activity across task repetitions compared to variability in muscle activity that would not achieve the goal: participants achieved the task in some repetitions with more right finger force and less left finger force (right > left) and in other repetitions with less right finger force and more left finger force (left > right). We found that EEG signals from the 500 milliseconds (ms) prior to each task repetition could make a significant prediction of which repetitions would have right > left and which would have left > right. We also found that cortical maps of sites contributing to the prediction contain both motor and pre-motor representation in the appropriate hemisphere. Thus, goal-equivalent variation in motor output may be implemented at a cortical level.
Literatur
Zurück zum Zitat Bernstein N (1967) Co-ordination and regulation of movements. Pergamon Press, Oxford Bernstein N (1967) Co-ordination and regulation of movements. Pergamon Press, Oxford
Zurück zum Zitat Blankertz B, Dornhege G, Lemm S, Krauledat M, Curio G, Müller K-R (2006) The berlin brain–computer interface: machine learning based detection of user specific brain states. J UCS 12:581–607 Blankertz B, Dornhege G, Lemm S, Krauledat M, Curio G, Müller K-R (2006) The berlin brain–computer interface: machine learning based detection of user specific brain states. J UCS 12:581–607
Zurück zum Zitat Blankertz B, Kawanabe M, Tomioka R, Hohlefeld F, Müller K-R, Nikulin VV (2007) Invariant common spatial patterns: Alleviating nonstationarities in brain–computer interfacing. In: Advances in neural information processing systems, pp 113–120 Blankertz B, Kawanabe M, Tomioka R, Hohlefeld F, Müller K-R, Nikulin VV (2007) Invariant common spatial patterns: Alleviating nonstationarities in brain–computer interfacing. In: Advances in neural information processing systems, pp 113–120
Zurück zum Zitat Blankertz B, Tomioka R, Lemm S, Kawanabe M, Muller K-R (2008) Optimizing spatial filters for robust eeg single-trial analysis signal processing magazine. IEEE 25:41–56 Blankertz B, Tomioka R, Lemm S, Kawanabe M, Muller K-R (2008) Optimizing spatial filters for robust eeg single-trial analysis signal processing magazine. IEEE 25:41–56
Zurück zum Zitat Churchland MM, Byron MY, Ryu SI, Santhanam G, Shenoy KV (2006) Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci 26:3697–3712CrossRefPubMed Churchland MM, Byron MY, Ryu SI, Santhanam G, Shenoy KV (2006) Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci 26:3697–3712CrossRefPubMed
Zurück zum Zitat Clauw D, Chrousos G (1998) Chronic pain and fatigue syndromes: overlapping clinical and neuroendocrine features and potential pathogenic mechanisms. Neuroimmunomodulation 4:134–153 Clauw D, Chrousos G (1998) Chronic pain and fatigue syndromes: overlapping clinical and neuroendocrine features and potential pathogenic mechanisms. Neuroimmunomodulation 4:134–153
Zurück zum Zitat de Freitas SMSF, Scholz JP (2010) A comparison of methods for identifying the Jacobian for uncontrolled manifold variance analysis. J Biomech 43:775–777CrossRefPubMed de Freitas SMSF, Scholz JP (2010) A comparison of methods for identifying the Jacobian for uncontrolled manifold variance analysis. J Biomech 43:775–777CrossRefPubMed
Zurück zum Zitat Deeny SP, Haufler AJ, Saffer M, Hatfield BD (2009) Electroencephalographic coherence during visuomotor performance: a comparison of cortico-cortical communication in experts and novices. J Mot Behav 41:106–116CrossRefPubMed Deeny SP, Haufler AJ, Saffer M, Hatfield BD (2009) Electroencephalographic coherence during visuomotor performance: a comparison of cortico-cortical communication in experts and novices. J Mot Behav 41:106–116CrossRefPubMed
Zurück zum Zitat Dornhege G (2007) Toward brain–computer interfacing. MIT press, Cambridge Dornhege G (2007) Toward brain–computer interfacing. MIT press, Cambridge
Zurück zum Zitat Dornhege G, Blankertz B, Krauledat M, Losch F, Curio G, Müller K-R (2006) Optimizing spatio-temporal filters for improving brain–computer interfacing. Adv Neural Inf Process Syst 18:315 Dornhege G, Blankertz B, Krauledat M, Losch F, Curio G, Müller K-R (2006) Optimizing spatio-temporal filters for improving brain–computer interfacing. Adv Neural Inf Process Syst 18:315
Zurück zum Zitat Fukunaga K (1990) Introduction to statistical pattern recognition. Academic Press, San Diego Fukunaga K (1990) Introduction to statistical pattern recognition. Academic Press, San Diego
Zurück zum Zitat Giszter SF, Mussa-Ivaldi FA, Bizzi E (1993) Convergent force fields organized in the frog’s spinal cord. Journal Neurosci 13:467–491 Giszter SF, Mussa-Ivaldi FA, Bizzi E (1993) Convergent force fields organized in the frog’s spinal cord. Journal Neurosci 13:467–491
Zurück zum Zitat Grillner S, Wallen P (1985) Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci 8:233–261CrossRefPubMed Grillner S, Wallen P (1985) Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci 8:233–261CrossRefPubMed
Zurück zum Zitat Hamill J, van Emmerik RE, Heiderscheit BC, Li L (1999) A dynamical systems approach to lower extremity running injuries. Clin Biomech 14:297–308CrossRef Hamill J, van Emmerik RE, Heiderscheit BC, Li L (1999) A dynamical systems approach to lower extremity running injuries. Clin Biomech 14:297–308CrossRef
Zurück zum Zitat Hamill J, Heiderscheit BC, Pollard CD (2005) Gender differences in lower extremity coupling variability during an unanticipated cutting maneuver. J Appl Biomech 21:143–152CrossRefPubMed Hamill J, Heiderscheit BC, Pollard CD (2005) Gender differences in lower extremity coupling variability during an unanticipated cutting maneuver. J Appl Biomech 21:143–152CrossRefPubMed
Zurück zum Zitat Hamill J, Palmer C, Van Emmerik RE (2012) Coordinative variability and overuse injury. BMC Sports Sci Med Rehabil 4:45CrossRef Hamill J, Palmer C, Van Emmerik RE (2012) Coordinative variability and overuse injury. BMC Sports Sci Med Rehabil 4:45CrossRef
Zurück zum Zitat Hastie T, Tibshirani R, Friedman J, Franklin J (2005) The elements of statistical learning: data mining, inference and prediction Math Intell 27:83–85 Hastie T, Tibshirani R, Friedman J, Franklin J (2005) The elements of statistical learning: data mining, inference and prediction Math Intell 27:83–85
Zurück zum Zitat Heinrichs-Graham E, Wilson TW (2016) Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging. NeuroImage 134:514–521CrossRefPubMed Heinrichs-Graham E, Wilson TW (2016) Is an absolute level of cortical beta suppression required for proper movement? Magnetoencephalographic evidence from healthy aging. NeuroImage 134:514–521CrossRefPubMed
Zurück zum Zitat Joshua M, Lisberger SG (2014) A framework for using signal, noise, and variation to determine whether the brain controls movement synergies or single muscles. J Neurophysiol 111:733–745CrossRefPubMed Joshua M, Lisberger SG (2014) A framework for using signal, noise, and variation to determine whether the brain controls movement synergies or single muscles. J Neurophysiol 111:733–745CrossRefPubMed
Zurück zum Zitat Kilpatrick LA et al (2014) Alterations in resting state oscillations and connectivity in sensory and motor networks in women with interstitial cystitis/painful bladder syndrome. J Urol 192:947–955CrossRefPubMedPubMedCentral Kilpatrick LA et al (2014) Alterations in resting state oscillations and connectivity in sensory and motor networks in women with interstitial cystitis/painful bladder syndrome. J Urol 192:947–955CrossRefPubMedPubMedCentral
Zurück zum Zitat Kouzaki M, Shinohara M (2006) The frequency of alternate muscle activity is associated with the attenuation in muscle fatigue. J Appl Phys 101:715–720 Kouzaki M, Shinohara M (2006) The frequency of alternate muscle activity is associated with the attenuation in muscle fatigue. J Appl Phys 101:715–720
Zurück zum Zitat Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292CrossRefPubMed Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292CrossRefPubMed
Zurück zum Zitat Kutch JJ et al (2015) Altered resting state neuromotor connectivity in men with chronic prostatitis/chronic pelvic pain syndrome: A MAPP: Research Network Neuroimaging Study. NeuroImage Clin 8:493–502CrossRefPubMedPubMedCentral Kutch JJ et al (2015) Altered resting state neuromotor connectivity in men with chronic prostatitis/chronic pelvic pain syndrome: A MAPP: Research Network Neuroimaging Study. NeuroImage Clin 8:493–502CrossRefPubMedPubMedCentral
Zurück zum Zitat Latash ML, Anson JG (2006) Synergies in health and disease: relations to adaptive changes in motor coordination Phys Ther 86:1151–1160PubMed Latash ML, Anson JG (2006) Synergies in health and disease: relations to adaptive changes in motor coordination Phys Ther 86:1151–1160PubMed
Zurück zum Zitat Latash ML, Li Z-M, Zatsiorsky VM (1998) A principle of error compensation studied within a task of force production by a redundant set of fingers. Exp Brain Res 122:131–138CrossRefPubMed Latash ML, Li Z-M, Zatsiorsky VM (1998) A principle of error compensation studied within a task of force production by a redundant set of fingers. Exp Brain Res 122:131–138CrossRefPubMed
Zurück zum Zitat Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multifinger force production tasks. Exp Brain Res 141:153–165CrossRefPubMed Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multifinger force production tasks. Exp Brain Res 141:153–165CrossRefPubMed
Zurück zum Zitat Lemm S, Blankertz B, Curio G, Muller K-R (2005) Spatio-spectral filters for improving the classification of single trial EEG. IEEE Trans Biomed Eng 52:1541–1548CrossRefPubMed Lemm S, Blankertz B, Curio G, Muller K-R (2005) Spatio-spectral filters for improving the classification of single trial EEG. IEEE Trans Biomed Eng 52:1541–1548CrossRefPubMed
Zurück zum Zitat Lipsitz LA (2002) Dynamics of stability the physiologic basis of functional health and frailty. J Geront Ser A Biol Sci Med Sci 57:B115–B125CrossRef Lipsitz LA (2002) Dynamics of stability the physiologic basis of functional health and frailty. J Geront Ser A Biol Sci Med Sci 57:B115–B125CrossRef
Zurück zum Zitat Medina JF, Lisberger SG (2007) Variation, signal, and noise in cerebellar sensory–motor processing for smooth-pursuit eye movements. J Neurosci 27:6832–6842CrossRefPubMedPubMedCentral Medina JF, Lisberger SG (2007) Variation, signal, and noise in cerebellar sensory–motor processing for smooth-pursuit eye movements. J Neurosci 27:6832–6842CrossRefPubMedPubMedCentral
Zurück zum Zitat Müller-Gerking J, Pfurtscheller G, Flyvbjerg H (1999) Designing optimal spatial filters for single-trial EEG classification in a movement task. Clin Neurophysiol 110:787–798CrossRefPubMed Müller-Gerking J, Pfurtscheller G, Flyvbjerg H (1999) Designing optimal spatial filters for single-trial EEG classification in a movement task. Clin Neurophysiol 110:787–798CrossRefPubMed
Zurück zum Zitat Pfurtscheller G, Aranibar A (1979) Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. Electroencephalogr Clin Neurophysiol 46:138–146CrossRefPubMed Pfurtscheller G, Aranibar A (1979) Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. Electroencephalogr Clin Neurophysiol 46:138–146CrossRefPubMed
Zurück zum Zitat Pfurtscheller G, Neuper C (1997) Motor imagery activates primary sensorimotor area in humans. Neurosci Lett 239:65–68CrossRefPubMed Pfurtscheller G, Neuper C (1997) Motor imagery activates primary sensorimotor area in humans. Neurosci Lett 239:65–68CrossRefPubMed
Zurück zum Zitat Pfurtscheller G, Neuper C, Flotzinger D, Pregenzer M (1997) EEG-based discrimination between imagination of right and left hand movement. Electroencephalogr Clin Neurophysiol 103:642–651CrossRefPubMed Pfurtscheller G, Neuper C, Flotzinger D, Pregenzer M (1997) EEG-based discrimination between imagination of right and left hand movement. Electroencephalogr Clin Neurophysiol 103:642–651CrossRefPubMed
Zurück zum Zitat Ramoser H, Muller-Gerking J, Pfurtscheller G (2000) Optimal spatial filtering of single trial EEG during imagined hand movement. Rehabil Eng IEEE Trans 8:441–446CrossRef Ramoser H, Muller-Gerking J, Pfurtscheller G (2000) Optimal spatial filtering of single trial EEG during imagined hand movement. Rehabil Eng IEEE Trans 8:441–446CrossRef
Zurück zum Zitat Rana M, Yani MS, Asavasopon S, Fisher BE, Kutch JJ (2015) Brain connectivity associated with muscle synergies in humans. J Neurosci 35:14708–14716CrossRefPubMedPubMedCentral Rana M, Yani MS, Asavasopon S, Fisher BE, Kutch JJ (2015) Brain connectivity associated with muscle synergies in humans. J Neurosci 35:14708–14716CrossRefPubMedPubMedCentral
Zurück zum Zitat Saltiel P, Wyler-Duda K, D’Avella A, Tresch MC, Bizzi E (2001) Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J Neurophysiol 85:605–619PubMed Saltiel P, Wyler-Duda K, D’Avella A, Tresch MC, Bizzi E (2001) Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J Neurophysiol 85:605–619PubMed
Zurück zum Zitat Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306CrossRefPubMed Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306CrossRefPubMed
Zurück zum Zitat Scholz JP, Kang N, Patterson D, Latash ML (2003) Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without down syndrome. Exp Brain Res 153:45–58CrossRefPubMed Scholz JP, Kang N, Patterson D, Latash ML (2003) Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without down syndrome. Exp Brain Res 153:45–58CrossRefPubMed
Zurück zum Zitat Seay JF, Haddad JM, Van Emmerik RE, Hamill J (2006) Coordination variability around the walk to run transition during human locomotion. Mot Control Champaign 10:178CrossRef Seay JF, Haddad JM, Van Emmerik RE, Hamill J (2006) Coordination variability around the walk to run transition during human locomotion. Mot Control Champaign 10:178CrossRef
Zurück zum Zitat Seay JF, Van Emmerik RE, Hamill J (2011) Low back pain status affects pelvis-trunk coordination and variability during walking and running. Clin Biomech 26:572–578CrossRef Seay JF, Van Emmerik RE, Hamill J (2011) Low back pain status affects pelvis-trunk coordination and variability during walking and running. Clin Biomech 26:572–578CrossRef
Zurück zum Zitat Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341–2356CrossRefPubMed Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341–2356CrossRefPubMed
Zurück zum Zitat Shim JK, Kim SW, Oh SJ, Kang N, Zatsiorsky VM, Latash ML (2005) Plastic changes in interhemispheric inhibition with practice of a two-hand force production task: a transcranial magnetic stimulation study. Neurosci Lett 374:104–108CrossRefPubMedPubMedCentral Shim JK, Kim SW, Oh SJ, Kang N, Zatsiorsky VM, Latash ML (2005) Plastic changes in interhemispheric inhibition with practice of a two-hand force production task: a transcranial magnetic stimulation study. Neurosci Lett 374:104–108CrossRefPubMedPubMedCentral
Zurück zum Zitat Singh T, Varadhan S, Zatsiorsky VM, Latash ML (2010) Fatigue and motor redundancy: adaptive increase in finger force variance in multi-finger tasks. J neurophysiol 103:2990–3000CrossRefPubMedPubMedCentral Singh T, Varadhan S, Zatsiorsky VM, Latash ML (2010) Fatigue and motor redundancy: adaptive increase in finger force variance in multi-finger tasks. J neurophysiol 103:2990–3000CrossRefPubMedPubMedCentral
Zurück zum Zitat Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334–350PubMed Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334–350PubMed
Zurück zum Zitat Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6:389–397CrossRefPubMed Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6:389–397CrossRefPubMed
Zurück zum Zitat Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226–1235CrossRefPubMed Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226–1235CrossRefPubMed
Zurück zum Zitat Turella L, Tucciarelli R, Oosterhof NN, Weisz N, Rumiati R, Lingnau A (2016) Beta band modulations underlie action representations for movement planning. NeuroImage 136:197–207 Turella L, Tucciarelli R, Oosterhof NN, Weisz N, Rumiati R, Lingnau A (2016) Beta band modulations underlie action representations for movement planning. NeuroImage 136:197–207
Zurück zum Zitat Woodworth D et al (2015) Unique microstructural changes in the brain associated with urological chronic pelvic pain syndrome (UCPPS) revealed by diffusion tensor MRI, super-resolution track density imaging, and statistical parameter mapping: A MAPP network neuroimaging study. PloS One 10:e0140250CrossRefPubMedPubMedCentral Woodworth D et al (2015) Unique microstructural changes in the brain associated with urological chronic pelvic pain syndrome (UCPPS) revealed by diffusion tensor MRI, super-resolution track density imaging, and statistical parameter mapping: A MAPP network neuroimaging study. PloS One 10:e0140250CrossRefPubMedPubMedCentral
Zurück zum Zitat Yang J-F, Scholz J (2005) Learning a throwing task is associated with differential changes in the use of motor abundance. Exp Brain Res 163:137–158CrossRefPubMed Yang J-F, Scholz J (2005) Learning a throwing task is associated with differential changes in the use of motor abundance. Exp Brain Res 163:137–158CrossRefPubMed
Metadaten
Titel
Cortical activity predicts good variation in human motor output
verfasst von
Sarine Babikian
Eva Kanso
Jason J. Kutch
Publikationsdatum
01.04.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Experimental Brain Research / Ausgabe 4/2017
Print ISSN: 0014-4819
Elektronische ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-017-4876-9

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