Experimental Brain Research

, Volume 204, Issue 2, pp 189–197

Theta frequency band activity and attentional mechanisms in visual and proprioceptive demand

  • J. C. Mizelle
  • Larry Forrester
  • Mark Hallett
  • Lewis A. Wheaton
Research article


In a companion manuscript we reported reduced electroencephalographic (EEG) activation at traditional sensorimotor areas in knee movements with high levels of task difficulty modulated by varying visual and proprioceptive sensory demands. Given that reduced cortical activity with more complex tasks is counter-intuitive, we suggested that high order cognitive-motor areas may show increased EEG activation to compensate for the observed decrease in sensorimotor regions. To test this hypothesis, we evaluated theta band activation at anterior frontal regions in a secondary analysis of our previous data. Unlike activation at sensorimotor areas, anterior frontal responses increased with each level of task difficulty as modulated by precision of visual targeting and/or proprioceptive demands from adding masses to the leg. Activity was increased as both unimodal visual and proprioceptive requirements became more demanding, but showed greater sensitivity to visual over proprioceptive processing requirements. Each level of bimodal task demands showed increasing activation, which was consistently greater when modulated through visual demands. These results are consistent with our hypothesis of increased contribution of anterior frontal regions for motor control in lower extremity movements with increasing sensory demands and further support different mechanisms for internally and externally guided movement.


EEG Theta band Sensorimotor control 


  1. Balslev D, Miall RC, Cole J (2007) Proprioceptive deafferentation slows down the processing of visual hand feedback. J Vis 7:(12)11–17Google Scholar
  2. Banati RB, Goerres GW, Tjoa C, Aggleton JP, Grasby P (2000) The functional anatomy of visual-tactile integration in man: a study using positron emission tomography. Neuropsychologia 38:115–124CrossRefPubMedGoogle Scholar
  3. Brown MR, DeSouza JF, Goltz HC, Ford K, Menon RS, Goodale MA, Everling S (2004) Comparison of memory- and visually guided saccades using event-related fMRI. J Neurophysiol 91:873–889CrossRefPubMedGoogle Scholar
  4. Caplan JB, Madsen JR, Schulze-Bonhage A, Aschenbrenner-Scheibe R, Newman EL, Kahana MJ (2003) Human theta oscillations related to sensorimotor integration and spatial learning. J Neurosci 23:4726–4736PubMedGoogle Scholar
  5. Carlson S, Martinkauppi S, Rama P, Salli E, Korvenoja A, Aronen HJ (1998) Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. Cereb Cortex 8:743–752CrossRefPubMedGoogle Scholar
  6. Cui RQ, Huter D, Egkher A, Lang W, Lindinger G, Deecke L (2000) High resolution DC-EEG mapping of the Bereitschaftspotential preceding simple or complex bimanual sequential finger movement. Exp Brain Res 134:49–57CrossRefPubMedGoogle Scholar
  7. Darling WG, Seitz RJ, Peltier S, Tellmann L, Butler AJ (2007) Visual cortex activation in kinesthetic guidance of reaching. Exp Brain Res 179:607–619CrossRefPubMedGoogle Scholar
  8. Davis KD, Hutchison WD, Lozano AM, Tasker RR, Dostrovsky JO (2000) Human anterior cingulate cortex neurons modulated by attention-demanding tasks. J Neurophysiol 83:3575–3577PubMedGoogle Scholar
  9. Dean HL, Platt ML (2006) Allocentric spatial referencing of neuronal activity in macaque posterior cingulate cortex. J Neurosci 26:1117–1127CrossRefPubMedGoogle Scholar
  10. Dean HL, Crowley JC, Platt ML (2004) Visual and saccade-related activity in macaque posterior cingulate cortex. J Neurophysiol 92:3056–3068CrossRefPubMedGoogle Scholar
  11. Delorme A, Westerfield M, Makeig S (2007) Medial prefrontal theta bursts precede rapid motor responses during visual selective attention. J Neurosci 27:11949–11959CrossRefPubMedGoogle Scholar
  12. DeSouza JF, Everling S (2004) Focused attention modulates visual responses in the primate prefrontal cortex. J Neurophysiol 91:855–862CrossRefPubMedGoogle Scholar
  13. Doppelmayr M, Finkenzeller T, Sauseng P (2008) Frontal midline theta in the pre-shot phase of rifle shooting: differences between experts and novices. Neuropsychologia 46:1463–1467CrossRefPubMedGoogle Scholar
  14. Druschky K, Kaltenhauser M, Hummel C, Druschky A, Huk WJ, Neundorfer B, Stefan H (2003) Somatosensory evoked magnetic fields following passive movement compared with tactile stimulation of the index finger. Exp Brain Res 148:186–195PubMedGoogle Scholar
  15. Efron B (1981) Nonparametric estimates of standard error: the jackknife, the bootstrap and other methods. Biometrika 68:589–599CrossRefGoogle Scholar
  16. Ferrera VP, Cohen JK, Lee BB (1999) Activity of prefrontal neurons during location and color delayed matching tasks. Neuroreport 10:1315–1322CrossRefPubMedGoogle Scholar
  17. Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47:381–391CrossRefPubMedGoogle Scholar
  18. Habeck C, Rakitin BC, Moeller J, Scarmeas N, Zarahn E, Brown T, Stern Y (2005) An event-related fMRI study of the neural networks underlying the encoding, maintenance, and retrieval phase in a delayed-match-to-sample task. Brain Res Cogn Brain Res 23:207–220CrossRefPubMedGoogle Scholar
  19. Hanlon CA, Buffington AL, McKeown MJ (2005) New brain networks are active after right MCA stroke when moving the ipsilesional arm. Neurology 64:114–120PubMedGoogle Scholar
  20. Hatfield BD, Haufler AJ, Hung TM, Spalding TW (2004) Electroencephalographic studies of skilled psychomotor performance. J Clin Neurophysiol 21:144–156CrossRefPubMedGoogle Scholar
  21. Hopfinger JB, Woldorff MG, Fletcher EM, Mangun GR (2001) Dissociating top-down attentional control from selective perception and action. Neuropsychologia 39:1277–1291CrossRefPubMedGoogle Scholar
  22. Hoshi E, Sawamura H, Tanji J (2005) Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity. J Neurophysiol 94:640–656CrossRefPubMedGoogle Scholar
  23. Ishii R, Shinosaki K, Ukai S, Inouye T, Ishihara T, Yoshimine T, Hirabuki N, Asada H, Kihara T, Robinson SE, Takeda M (1999) Medial prefrontal cortex generates frontal midline theta rhythm. Neuroreport 10:675–679CrossRefPubMedGoogle Scholar
  24. Isomura Y, Ito Y, Akazawa T, Nambu A, Takada M (2003) Neural coding of “attention for action” and “response selection” in primate anterior cingulate cortex. J Neurosci 23:8002–8012PubMedGoogle Scholar
  25. Kim YH, Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Mesulam MM (1999) The large-scale neural network for spatial attention displays multifunctional overlap but differential asymmetry. Neuroimage 9:269–277CrossRefPubMedGoogle Scholar
  26. Kondo H, Morishita M, Osaka N, Osaka M, Fukuyama H, Shibasaki H (2004a) Functional roles of the cingulo-frontal network in performance on working memory. Neuroimage 21:2–14CrossRefPubMedGoogle Scholar
  27. Kondo H, Osaka N, Osaka M (2004b) Cooperation of the anterior cingulate cortex and dorsolateral prefrontal cortex for attention shifting. Neuroimage 23:670–679CrossRefPubMedGoogle Scholar
  28. Ku Y, Ohara S, Wang L, Lenz FA, Hsiao SS, Bodner M, Hong B, Zhou YD (2007) Prefrontal cortex and somatosensory cortex in tactile crossmodal association: an independent component analysis of ERP recordings. PLoS ONE 2:e771Google Scholar
  29. Laurienti PJ, Wallace MT, Maldjian JA, Susi CM, Stein BE, Burdette JH (2003) Cross-modal sensory processing in the anterior cingulate and medial prefrontal cortices. Hum Brain Mapp 19:213–223CrossRefPubMedGoogle Scholar
  30. Lebedev MA, Messinger A, Kralik JD, Wise SP (2004) Representation of attended versus remembered locations in prefrontal cortex. PLoS Biol 2:e365CrossRefPubMedGoogle Scholar
  31. Missonnier P, Deiber MP, Gold G, Millet P, Gex-Fabry Pun M, Fazio-Costa L, Giannakopoulos P, Ibanez V (2006) Frontal theta event-related synchronization: comparison of directed attention and working memory load effects. J Neural Transm 113:1477–1486CrossRefPubMedGoogle Scholar
  32. Mizelle JC, Forrester LW, Hallett M, Wheaton LA (2010) Electroencephalographic reactivity to unimodal and bimodal visual and proprioceptive demands in sensorimotor integration. Exp Brain Res. doi:10.1007/s00221-010-2273-8
  33. Ohara S, Lenz F, Zhou YD (2006a) Sequential neural processes of tactile-visual crossmodal working memory. Neuroscience 139:299–309CrossRefPubMedGoogle Scholar
  34. Ohara S, Lenz FA, Zhou YD (2006b) Modulation of somatosensory event-related potential components in a tactile-visual cross-modal task. Neuroscience 138:1387–1395CrossRefPubMedGoogle Scholar
  35. Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2:417–424CrossRefPubMedGoogle Scholar
  36. Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342–353CrossRefPubMedGoogle Scholar
  37. Ramnani N, Owen AM (2004) Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci 5:184–194CrossRefPubMedGoogle Scholar
  38. Rao SC, Rainer G, Miller EK (1997) Integration of what and where in the primate prefrontal cortex. Science 276:821–824CrossRefPubMedGoogle Scholar
  39. Ricciardi E, Bonino D, Gentili C, Sani L, Pietrini P, Vecchi T (2006) Neural correlates of spatial working memory in humans: a functional magnetic resonance imaging study comparing visual and tactile processes. Neuroscience 139:339–349CrossRefPubMedGoogle Scholar
  40. Riehle A, Vaadia E (2005) Motor cortex in voluntary movements: a distributed system for distributed for distributed functions. CRC Press, Boca RatonGoogle Scholar
  41. Rushworth MF, Krams M, Passingham RE (2001) The attentional role of the left parietal cortex: the distinct lateralization and localization of motor attention in the human brain. J Cogn Neurosci 13:698–710CrossRefPubMedGoogle Scholar
  42. Russo GS, Backus DA, Ye S, Crutcher MD (2002) Neural activity in monkey dorsal and ventral cingulate motor areas: comparison with the supplementary motor area. J Neurophysiol 88:2612–2629CrossRefPubMedGoogle Scholar
  43. Sauseng P, Hoppe J, Klimesch W, Gerloff C, Hummel FC (2007) Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range. Eur J Neurosci 25:587–593CrossRefPubMedGoogle Scholar
  44. Serrien DJ, Ivry RB, Swinnen SP (2007) The missing link between action and cognition. Prog Neurobiol 82:95–107CrossRefPubMedGoogle Scholar
  45. Slobounov S, Hallett M, Newell KM (2004) Perceived effort in force production as reflected in motor-related cortical potentials. Clin Neurophysiol 115:2391–2402PubMedGoogle Scholar
  46. Small DM, Gitelman DR, Gregory MD, Nobre AC, Parrish TB, Mesulam MM (2003) The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention. Neuroimage 18:633–641CrossRefPubMedGoogle Scholar
  47. Stark E, Abeles M (2005) Applying resampling methods to neurophysiological data. J Neurosci Methods 145:133–144CrossRefPubMedGoogle Scholar
  48. Talati A, Hirsch J (2005) Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on “what”, “when”, and “where” related information: an fMRI study. J Cogn Neurosci 17:981–993CrossRefPubMedGoogle Scholar
  49. Vaillancourt DE, Thulborn KR, Corcos DM (2003) Neural basis for the processes that underlie visually guided and internally guided force control in humans. J Neurophysiol 90:3330–3340CrossRefPubMedGoogle Scholar
  50. Wenderoth N, Debaere F, Sunaert S, Swinnen SP (2005) The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour. Eur J Neurosci 22:235–246CrossRefPubMedGoogle Scholar
  51. Wheaton LA, Mizelle JC, Forrester LW, Bai O, Shibasaki H, Macko RF (2007) How does the brain respond to unimodal and bimodal sensory demand in movement of the lower extremity? Exp Brain Res 180:345–354CrossRefPubMedGoogle Scholar
  52. Yamasaki H, LaBar KS, McCarthy G (2002) Dissociable prefrontal brain systems for attention and emotion. Proc Natl Acad Sci USA 99:11447–11451CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • J. C. Mizelle
    • 1
    • 2
    • 3
  • Larry Forrester
    • 2
    • 3
    • 4
  • Mark Hallett
    • 5
  • Lewis A. Wheaton
    • 1
    • 3
  1. 1.School of Applied PhysiologyGeorgia Institute of TechnologyAtlantaUSA
  2. 2.Baltimore Department of Veterans AffairsBaltimoreUSA
  3. 3.Department Physical Therapy and Rehabilitation ScienceUniversity of Maryland School of MedicineBaltimoreUSA
  4. 4.Department of NeurologyUniversity of Maryland School of MedicineBaltimoreUSA
  5. 5.Human Motor Control SectionNational Institutes of Neurological Disorders and Stroke, National Institutes of HealthBethesdaUSA

Personalised recommendations