Experimental Brain Research

, Volume 233, Issue 12, pp 3447–3457 | Cite as

Cortical activity differs between position- and force-control knee extension tasks

  • Peter C. Poortvliet
  • Kylie J. Tucker
  • Simon Finnigan
  • Dion Scott
  • Paul Sowman
  • Paul W. Hodges
Research Article

Abstract

Neural control differs between position- and force-control tasks as evident from divergent effects of fatigue and pain. Unlike force-control tasks, position-control tasks focus on a postural goal to maintain a joint angle. Cortical involvement is suggested to be less during postural control, but whether this differs between position- and force-control paradigms remains unclear. Coherence estimates the functional communication between spatially distinct active regions within the cortex (cortico-cortical coherence; CCC) and between the cortex and muscles (corticomuscular coherence; CMC). We investigated whether cortical involvement differed between force-control and more posturally focused, position-control tasks. Seventeen adults performed position- and force-control knee extensor efforts at a submaximal load (10 % maximum voluntary contraction). Surface electromyography was recorded from the right knee extensor and flexor muscles and brain activity using electroencephalography (EEG). CCC and CMC in the beta (13–30 Hz) and gamma (30–45 Hz) frequency bands were calculated between combinations of intra- and inter-hemispheric pairs of electrodes, and between four EEG electrodes that approximated the left motor cortical area, and right knee extensor EMG, respectively. Differences in EEG power and muscle activity were also calculated. CCC was greater across distributed regions in the force-control task. Beta EEG power in the left hemisphere was higher for the position-control task. Although averaged CMC data differed between tasks, there was no task difference for individual CMC data. Muscle activity and force did not differ between tasks. The results demonstrate differential cortical contributions to control force- versus position-control tasks. This might contribute to differences in performance outcomes of these tasks that have been shown previously.

Keywords

Cortico-cortical coherence Corticomuscular coherence Postural control Electroencephalography Electromyography Knee extensor muscles 

Notes

Acknowledgments

Financial support was provided by the National Health and Medical Research Council of Australia (Research Fellowship [PH] ID401599 [KT] ID1009410; Project Grant—ID 569744). There was no conflict of interest.

References

  1. Andrew C, Pfurtscheller G (1996) Event-related coherence as a tool for studying dynamic interaction of brain regions. Electroencephalogr Clin Neurophysiol 98:144–148CrossRefPubMedGoogle Scholar
  2. Aoki F, Fetz EE, Shupe L, Lettich E, Ojemann GA (1999) Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks. Clin Neurophysiol 110:524–537. doi: 10.1016/s1388-2457(98)00064-9 CrossRefPubMedGoogle Scholar
  3. Baker SN, Olivier E, Lemon RN (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol (Lond) 501:225–241. doi: 10.1111/j.1469-7793.1997.225bo.x CrossRefGoogle Scholar
  4. Banich MT (1998) The missing link: the role of interhemispheric interaction in attentional processing. Brain Cogn 36:128–157. doi: 10.1006/brcg.1997.0950 CrossRefPubMedGoogle Scholar
  5. Baudry S, Enoka RM (2009) Influence of load type on presynaptic modulation of Ia afferent input onto two synergist muscles. Exp Brain Res 199:83–88. doi: 10.1007/s00221-009-1951-x CrossRefPubMedGoogle Scholar
  6. Baudry S, Rudroff T, Pierpoint LA, Enoka RM (2009) Load type influences motor unit recruitment in biceps brachii during a sustained contraction. J Neurophysiol 102:1725–1735. doi: 10.1152/jn.00382.2009 PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bayraktaroglu Z, von Carlowitz-Ghori K, Losch F, Nolte G, Curio G, Nikulin VV (2011) Optimal imaging of cortico-muscular coherence through a novel regression technique based on multi-channel EEG and un-rectified EMG. Neuroimage 57:1059–1067. doi: 10.1016/j.neuroimage.2011.04.071 CrossRefPubMedGoogle Scholar
  8. Classen J, Gerloff C, Honda M, Hallett M (1998) Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. J Neurophysiol 79:1567–1573PubMedGoogle Scholar
  9. Deeny S, Hillman C, Janelle C, Hatfield B (2001) EEG coherence and psychomotor efficiency in expert and nonexpert marksmen. Psychophysiology 38:S35–S35CrossRefGoogle Scholar
  10. Deeny SP, Hillman CH, Janelle CM, Hatfield BD (2003) Cortico-cortical communication and superior performance in skilled marksmen: an EEG coherence analysis. J Sport Exerc Psychol 25:188–204Google Scholar
  11. Deliagina TG, Zelenin PV, Beloozerova IN, Orlovsky GN (2007) Nervous mechanisms controlling body posture. Physiol Behav 92:148–154. doi: 10.1016/j.physbeh.2007.05.023 CrossRefPubMedGoogle Scholar
  12. Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716. doi: 10.1038/35094565 CrossRefPubMedGoogle Scholar
  13. Freeman WJ (1975) Parallel processing of signals in neural sets as manifested in EEG. Int J Man Mach Stud 7:347–369. doi: 10.1016/s0020-7373(75)80017-4 CrossRefGoogle Scholar
  14. Gahéry Y, Nieoullon A (1978) Postural and kinetic coordination following cortical stimuli which induce flexion movements in the cat’s limbs. Brain Res 149:25–37. doi: 10.1016/0006-8993(78)90585-1 CrossRefPubMedGoogle Scholar
  15. Gerloff C, Richard J, Hadley J, Schulman AE, Honda M, Hallett M (1998) Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain 121:1513–1531. doi: 10.1093/brain/121.8.1513 CrossRefPubMedGoogle Scholar
  16. Halliday DM, Farmer SF (2010) On the need for rectification of surface EMG. J Neurophysiol 103:3547. doi: 10.1152/jn.00222.2010 CrossRefPubMedGoogle Scholar
  17. Halliday DM, Rosenberg JR, Amjad AM, Breeze P, Conway BA, Farmer SF (1995) A framework for the analysis of mixed time series/point process data—theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64:237–278. doi: 10.1016/s0079-6107(96)00009-0 CrossRefPubMedGoogle Scholar
  18. Hellige JB (1990) Hemispheric-asymmetry. Annu Rev Psychol 41:55–80. doi: 10.1146/annurev.psych.41.1.55 CrossRefPubMedGoogle Scholar
  19. Homan RW, Herman J, Purdy P (1987) Cerebral location of international 10–20 system electrode placement. Electroencephalogr Clin Neurophysiol 66:376–382. doi: 10.1016/0013-4694(87)90206-9 CrossRefPubMedGoogle Scholar
  20. Hong SL, Newell KM (2008) Visual information gain and the regulation of constant force levels. Exp Brain Res 189:61–69. doi: 10.1007/s00221-008-1403-z CrossRefGoogle Scholar
  21. Horak FB (2006) Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 35:7–11. doi: 10.1093/ageing/afl077 CrossRefGoogle Scholar
  22. Hunter SK, Ryan DL, Ortega JD, Enoka RM (2002) Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans. J Neurophysiol 88:3087–3096. doi: 10.1152/jn.00232.2002 CrossRefPubMedGoogle Scholar
  23. Hunter SK, Yoon TJ, Farinella J, Griffith EE, Ng AV (2008) Time to task failure and muscle activation vary with load type for a submaximal fatiguing contraction with the lower leg. J Appl Physiol 105:463–472. doi: 10.1152/japplphysiol.90398.2008 CrossRefPubMedGoogle Scholar
  24. Jacobs JV, Horak FB (2007a) Cortical control of postural responses. J Neural Transm 114:1339–1348. doi: 10.1007/s00702-007-0657-0 PubMedCentralCrossRefPubMedGoogle Scholar
  25. Jacobs JV, Horak FB (2007b) External postural perturbations induce multiple anticipatory postural adjustments when subjects cannot pre-select their stepping foot. Exp Brain Res 179:29–42. doi: 10.1007/s00221-006-0763-5 CrossRefPubMedGoogle Scholar
  26. Jensen O, Kaiser J, Lachaux J-P (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30:317–324. doi: 10.1016/j.tins.2007.05.001 CrossRefPubMedGoogle Scholar
  27. Kilner JM, Baker SN, Salenius S, Jousmaki V, Hari R, Lemon RN (1999) Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles. J Physiol (Lond) 516:559–570. doi: 10.1111/j.1469-7793.1999.0559v.x CrossRefGoogle Scholar
  28. Kilner JM, Baker SN, Salenius S, Hari R, Lemon RN (2000) Human cortical muscle coherence is directly related to specific motor parameters. J Neurosci 20:8838–8845PubMedGoogle Scholar
  29. Kilner JM, Salenius S, Baker SN, Jackson A, Hari R, Lemon RN (2003) Task-dependent modulations of cortical oscillatory activity in human subjects during a bimanual precision grip task. Neuroimage 18:67–73. doi: 10.1006/nimg.2002.1322 CrossRefPubMedGoogle Scholar
  30. Klass M, Levenez M, Enoka RM, Duchateau J (2008) Spinal mechanisms contribute to differences in the time to failure of submaximal fatiguing contractions performed with different loads. J Neurophysiol 99:1096–1104. doi: 10.1152/jn.01252.2007 CrossRefPubMedGoogle Scholar
  31. Kristeva R, Patino L, Omlor W (2007) Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output. Neuroimage 36:785–792. doi: 10.1016/j.neuroimage.2007.03.025 CrossRefPubMedGoogle Scholar
  32. Maki BE, McIlroy WE (2007) Cognitive demands and cortical control of human balance-recovery reactions. J Neural Transm 114:1279–1296. doi: 10.1007/s00702-007-0764-y CrossRefPubMedGoogle Scholar
  33. Maluf KS, Enoka RM (2005) Task failure during fatiguing contractions performed by humans. J Appl Physiol 99:389–396. doi: 10.1152/japplphysiol.00207.2005 CrossRefPubMedGoogle Scholar
  34. Maluf KS, Shinohara M, Stephenson JL, Enoka RM (2005) Muscle activation and time to task failure differ with load type and contraction intensity for a human hand muscle. Exp Brain Res 167:165–177. doi: 10.1007/s00221-005-0017-y CrossRefPubMedGoogle Scholar
  35. Manganotti P, Gerloff C, Toro C et al (1998) Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr Clin Neurophysiol 109:50–62. doi: 10.1016/s0924-980x(97)00074-x CrossRefPubMedGoogle Scholar
  36. Masakado Y, Nielsen JB (2008) Task-and phase-related changes in cortico-muscular coherence. Keio J Med 57:50–56CrossRefPubMedGoogle Scholar
  37. Masakado Y, Ushiba J, Tsutsumi N, Takahashi Y, Tomita Y, Kimura A, Liu M (2008) EEG-EMG coherence changes in postural tasks. Electromyogr Clin Neurophysiol 48:27–33PubMedGoogle Scholar
  38. McClelland VM, Cvetkovic Z, Mills KR (2012) Modulation of corticomuscular coherence by peripheral stimuli. Exp Brain Res 219:275–292. doi: 10.1007/s00221-012-3087-7 CrossRefPubMedGoogle Scholar
  39. Miltner WHR, Braun C, Arnold M, Witte H, Taub E (1999) Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397:434–436. doi: 10.1038/17126 CrossRefPubMedGoogle Scholar
  40. Mima T, Hallett M (1999) Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism. Clin Neurophysiol 110:1892–1899. doi: 10.1016/s1388-2457(99)00238-2 CrossRefPubMedGoogle Scholar
  41. Mottram CJ, Jakobi JM, Semmler JG, Enoka RM (2005) Motor-unit activity differs with load type during a fatiguing contraction. J Neurophysiol 93:1381–1392. doi: 10.1152/jn.00837.2004 CrossRefPubMedGoogle Scholar
  42. Mottram CJ, Hunter SK, Rochette L, Anderson MK, Enoka RM (2006) Time to task failure varies with the gain of the feedback signal for women, but not for men. Exp Brain Res 174:575–587. doi: 10.1007/s00221-006-0498-3 CrossRefPubMedGoogle Scholar
  43. Murthy VN, Fetz EE (1992) Coherent 25-Hz to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci USA 89:5670–5674. doi: 10.1073/pnas.89.12.5670 PubMedCentralCrossRefPubMedGoogle Scholar
  44. Myers LJ, Lowery M, O’Malley M et al (2003) Rectification and non-linear pre-processing of EMG signals for cortico-muscular analysis. J Neurosci Methods 124:157–165. doi: 10.1016/s0165-0270(03)00004-9 CrossRefPubMedGoogle Scholar
  45. Nunez PL (eds) (1995) Mind, brain, and electroencephalography. In: Neocortical dynamics and human EEG rhythms. Oxford University Press, pp 133–194Google Scholar
  46. Perez MA, Lundbye-Jensen J, Nielsen JB (2006) Changes in corticospinal drive to spinal motoneurones following visuo-motor skill learning in humans. J Physiol (Lond) 573:843–855. doi: 10.1113/jphysiol.2006.105361 PubMedCentralCrossRefGoogle Scholar
  47. Pfurtscheller G, Andrew C (1999) Event-related changes of band power and coherence: methodology and interpretation. J Clin Neurophysiol 16:512–519. doi: 10.1097/00004691-199911000-00003 CrossRefPubMedGoogle Scholar
  48. Pfurtscheller G, Lopes da Silva FH (eds) (1999) Functional meaning of event-related desynchronization (ERD) and synchronization (ERS). In: Handbook of electroencephalography and clinical neurophysiology, vol 6. Elsevier, Amsterdam, pp 51–65Google Scholar
  49. Pinto Neto O, Christou EA (2010) Rectification of the EMG signal impairs the identification of oscillatory input to the muscle. J Neurophysiol 103:1093–1103. doi: 10.1152/jn.00792.2009 CrossRefGoogle Scholar
  50. Poortvliet PC, Tucker KJ, Hodges PW (2013) Changes in constraint of proximal segments effects time to task failure and activity of proximal muscles in knee position-control tasks. Clin Neurophysiol 124:732–739. doi: 10.1016/j.clinph.2012.09.025 CrossRefPubMedGoogle Scholar
  51. Poortvliet PC, Tucker KT, Hodges PW (2015) Experimental pain has a greater effect on single motor unit discharge during force-control than position-control tasks. Clin Neurophysiol 126:1378–1386. doi: 10.1016/j.clinph.2014.10.139 CrossRefPubMedGoogle Scholar
  52. Riddle CN, Baker SN (2006) Digit displacement, not object compliance, underlies task dependent modulations in human corticomuscular coherence. Neuroimage 33:618–627. doi: 10.1016/j.neuroimage.2006.07.027 CrossRefPubMedGoogle Scholar
  53. Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53:1–31. doi: 10.1016/0079-6107(89)90004-7 CrossRefPubMedGoogle Scholar
  54. Rudroff T, Barry BK, Stone AL, Barry CJ, Enoka RM (2007) Accessory muscle activity contributes to the variation in time to task failure for different arm postures and loads. J Appl Physiol 102:1000–1006. doi: 10.1152/japplphysiol.00564.2006 CrossRefPubMedGoogle Scholar
  55. Rudroff T, Justice JN, Matthews S, Zuo R, Enoka RM (2010) Muscle activity differs with load compliance during fatiguing contractions with the knee extensor muscles. Exp Brain Res 203:307–316. doi: 10.1007/s00221-010-2233-3 CrossRefPubMedGoogle Scholar
  56. Rudroff T, Justice JN, Holmes MR, Matthews SD, Enoka RM (2011) Muscle activity and time to task failure differ with load compliance and target force for elbow flexor muscles. J Appl Physiol 110:125–136. doi: 10.1152/japplphysiol.00605.2010 PubMedCentralCrossRefPubMedGoogle Scholar
  57. Salenius S, Portin K, Kajola M, Salmelin R, Hari R (1997) Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol 77:3401–3405PubMedGoogle Scholar
  58. Sauve K (1999) Gamma-band synchronous oscillations: Recent evidence regarding their functional significance. Conscious Cogn 8:213–224. doi: 10.1006/ccog.1999.0383 CrossRefPubMedGoogle Scholar
  59. Semmes J (1968) Hemispheric specialization: a possible clue to mechanism. Neuropsychologia 6:11–26CrossRefGoogle Scholar
  60. Serrien DJ, Brown P (2002) The functional role of interhemispheric synchronization in the control of bimanual timing tasks. Exp Brain Res 147:268–272. doi: 10.1007/s00221-002-1253-z CrossRefPubMedGoogle Scholar
  61. Serrien DJ, Brown P (2004) Changes in functional coupling patterns during bimanual task performance. NeuroReport 15:1387–1390. doi: 10.1097/01.wnr.0000131009.44068.51 CrossRefPubMedGoogle Scholar
  62. Serrien DJ, Spapé MM (2009) The role of hand dominance and sensorimotor congruence in voluntary movement. Exp Brain Res 199:195–200. doi: 10.1007/s00221-009-1998-8 PubMedCentralCrossRefPubMedGoogle Scholar
  63. Serrien DJ, Cassidy MJ, Brown P (2003) The importance of the dominant hemisphere in the organization of bimanual movements. Hum Brain Mapp 18:296–305. doi: 10.1002/hbm.10086 CrossRefPubMedGoogle Scholar
  64. Serrien DJ, Pogosyan AH, Brown P (2004) Cortico-cortical coupling patterns during dual task performance. Exp Brain Res 157:79–84. doi: 10.1007/s00221-003-1822-9 CrossRefPubMedGoogle Scholar
  65. Serrien DJ, Ivry RB, Swinnen SP (2006) Dynamics of hemispheric specialization and integration in the context of motor control. Nat Rev Neurosci 7:160–166. doi: 10.1038/nrn1849 CrossRefPubMedGoogle Scholar
  66. Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349–374 doi: 10.1146/annurev.ph.55.030193.002025 CrossRefPubMedGoogle Scholar
  67. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586. doi: 10.1146/annurev.neuro.18.1.555 CrossRefPubMedGoogle Scholar
  68. Slobounov S, Hallett M, Stanhope S, Shibasaki H (2005) Role of cerebral cortex in human postural control: an EEG study. Clin Neurophysiol 116:315–323. doi: 10.1016/j.clinph.2004.09.007 CrossRefPubMedGoogle Scholar
  69. Steinmetz H, Furst G, Meyer BU (1989) Craniocerebral topography within the international 10–20 system. Electroencephalogr Clin Neurophysiol 72:499–506. doi: 10.1016/0013-4694(89)90227-7 CrossRefPubMedGoogle Scholar
  70. Stephan KE, Fink GR, Marshall JC (2007) Mechanisms of hemispheric specialization: insights from analyses of connectivity. Neuropsychologia 45:209–228. doi: 10.1016/j.neuropsychologia.2006.07.002 PubMedCentralCrossRefPubMedGoogle Scholar
  71. Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J (1998) Induced gamma-band activity during the delay of a visual short-term memory task in humans. J Neurosci 18:4244–4254PubMedGoogle Scholar
  72. Thatcher RW, Walker RA (1985) EEG coherence and intelligence in children. Electroencephalogr Clin Neurophysiol 61:S161–S161. doi: 10.1016/0013-4694(85)90621-2 CrossRefGoogle Scholar
  73. Thatcher RW, Krause PJ, Hrybyk M (1986) Corticocortical associations and eeg coherence: a 2-compartmental model. Electroencephalogr Clin Neurophysiol 64:123–143. doi: 10.1016/0013-4694(86)90107-0 CrossRefPubMedGoogle Scholar
  74. Tucker DM, Roth DL, Bair TB (1986) Functional connections among cortical regions: topography of eeg coherence. Electroencephalogr Clin Neurophysiol 63:242–250. doi: 10.1016/0013-4694(86)90092-1 CrossRefPubMedGoogle Scholar
  75. Weiss S, Rappelsberger P (2000) Long-range EEG synchronization during word encoding correlates with successful memory performance. Cogn Brain Res 9:299–312CrossRefGoogle Scholar
  76. Womelsdorf T, Fries P (2006) Neuronal coherence during selective attentional processing and sensory-motor integration. J Physiol (Paris) 100:182–193. doi: 10.1016/j.jphysparis.2007.01.005 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Centre for Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation SciencesThe University of QueenslandBrisbaneAustralia
  2. 2.Centre for Sensorimotor Performance, School of Human Movement and Nutrition SciencesThe University of QueenslandBrisbaneAustralia
  3. 3.Asia-Pacific Centre for Neuromodulation, Centre for Clinical ResearchThe University of QueenslandBrisbaneAustralia
  4. 4.School of Biomedical SciencesThe University of QueenslandBrisbaneAustralia
  5. 5.Centre for Clinical Research, Royal Brisbane and Women’s HospitalThe University of QueenslandBrisbaneAustralia
  6. 6.Gallipoli Medical Research FoundationGreenslopes Private HospitalBrisbaneAustralia
  7. 7.Department of Cognitive ScienceMacquarie UniversitySydneyAustralia

Personalised recommendations