Skip to main content
Log in

Modulation of the response to a somatosensory stimulation of the hand during the observation of manual actions

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Observation of hand movements has been repeatedly demonstrated to increase the excitability of the motor cortical representation of the hand. Little attention, however, has been devoted to its effect on somatosensory processing. Movement execution is well known to decrease somatosensory cortical excitability, a phenomenon termed ‘gating’. As executed and observed actions share common cortical representations, we hypothesized that action observation (hand movements) should also modulate the cortical response to sensory stimulation of the hand. Seventeen healthy subjects participated in these experiments in which electroencephalographic (EEG) recordings of the somatosensory steady-state response (SSSR) were obtained. The SSSR provides a continuous measure of somatosensory processing. Recordings were made during a baseline condition and five observation conditions in which videos showed either a: (1) hand action; (2) passive stimulation of a hand; (3) static hand; (4) foot action; or (5) static object. The method employed consisted of applying a continuous 25 Hz vibratory stimulation to the index finger during the six conditions and measuring potential gating effects in the SSSR within the 25 Hz band (corresponding to the stimulation frequency). A significant effect of condition was found over the contralateral parietal cortex. Observation of hand actions resulted in a significant gating effect when compared to baseline (average gating of 22%). Observation of passive touch of the hand also gated the response (17% decrease). In conclusion, the results show that viewing a hand performing an action or being touched interferes with the processing of somatosensory information arising from the hand.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aglioti SM, Cesari P, Romani M, Urgesi C (2008) Action anticipation and motor resonance in elite basketball players. Nat Neurosci 11:1109–1116

    Article  PubMed  CAS  Google Scholar 

  • Avikainen S, Forss N, Hari R (2002) Modulated activation of the human SI and SII cortices during observation of hand actions. Neuroimage 15:640–646

    Article  PubMed  Google Scholar 

  • Aziz-Zadeh L, Maeda F, Zaidel E, Mazziotta J, Iacoboni M (2002) Lateralization in motor facilitation during action observation: a TMS study. Exp Brain Res 144:127–131

    Article  PubMed  Google Scholar 

  • Babiloni C, Babiloni F, Carducci F, Cincotti F, Cocozza G, Del PC, Moretti DV, Rossini PM (2002) Human cortical electroencephalography (EEG) rhythms during the observation of simple aimless movements: a high-resolution EEG study. Neuroimage 17:559–572

    Article  PubMed  Google Scholar 

  • Blakemore SJ, Bristow D, Bird G, Frith C, Ward J (2005) Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain 128:1571–1583

    Article  PubMed  Google Scholar 

  • Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13:400–404

    PubMed  CAS  Google Scholar 

  • Bufalari I, Aprile T, Avenanti A, Di Russo F, Aglioti SM (2007) Empathy for pain and touch in the human somatosensory cortex. Cer Cortex 17:2553–2561

    Article  Google Scholar 

  • Burke D, Gandevia SC (1988) Interfering cutaneous stimulation and muscle afferent contribution to cortical potentials. Electroencephalogr Clin Neurophysiol 70:118–125

    Article  PubMed  CAS  Google Scholar 

  • Caetano G, Jousmäki V, Hari R (2007) Actor’s and observer’s primary motor cortices stabilize similarly after seen or heard motor actions. Proc Natl Acad Sci USA 104:9058–9062

    Article  PubMed  CAS  Google Scholar 

  • Celnik P, Webster B, Glasser DM, Cohen LG (2008) Effects of action observation on physical training after stroke. Stroke 39:1814–1820

    Article  PubMed  Google Scholar 

  • Chan BL, Witt R, Charrow AP, Magee A, Howard R, Pasquina PF, Heilman KM, Tsao JW (2007) Mirror therapy for phantom limb pain. N Eng J Med 357:2206–2207

    Article  CAS  Google Scholar 

  • Chapman CE (1994) Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. Can J Physiol Pharmacol 72:558–570

    PubMed  CAS  Google Scholar 

  • Chapman CE, Jiang W, Lamarre Y (1988) Modulation of lemniscal input during conditioned arm movements in the monkey. Exp Brain Res 72:316–334

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Lee PL, Yang CY, Lin CP, Hung D, Decety J (2008) Gender differences in the mu rhythm of the human mirror-neuron system. PLoS ONE 3:e2113

    Article  PubMed  Google Scholar 

  • Cheron G, Dan B, Borenstein S (2000) Sensory and motor interfering influences on somatosensory evoked potentials. J Clin Neurophysiol 17:280–294

    Article  PubMed  CAS  Google Scholar 

  • Clark S, Tremblay F, Ste-Marie D (2004) Differential modulation of corticospinal excitability during observation, mental imagery and imitation of hand actions. Neuropsychologia 42:105–112

    Article  PubMed  Google Scholar 

  • Cochin S, Barthelemy C, Lejeune B, Roux S, Martineau J (1998) Perception of motion and qEEG activity in human adults. Electroencephalogr Clin Neurophysiol 107:287–295

    Article  PubMed  CAS  Google Scholar 

  • Cochin S, Barthelemy C, Roux S, Martineau J (1999) Observation and execution of movement: similarities demonstrated by quantified electroencephalography. Eur J Neurosci 11:1839–1842

    Article  PubMed  CAS  Google Scholar 

  • Dionne JK, Meehan SK, Legon W, Staines WR (2010) Crossmodal influences in somatosensory cortex: Interaction of vision and touch. Hum Brain Mapp 31:14–25

    PubMed  Google Scholar 

  • Ertelt D, Small S, Solodkin A, Dettmers C, McNamara A, Binkofski F, Buccino G (2007) Action observation has a positive impact on rehabilitation of motor deficits after stroke. Neuroimage 36:T164–T173

    Article  PubMed  Google Scholar 

  • Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophys 73:2608–2611

    CAS  Google Scholar 

  • Fadiga L, Craighero L, Olivier E (2005) Human motor cortex excitability during the perception of others’ action. Curr Opin Neurobiol 15:213–218

    Article  PubMed  CAS  Google Scholar 

  • Gangitano M, Mottaghy FM, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. Neuroreport 12:1489–1492

    Article  PubMed  CAS  Google Scholar 

  • Gazzola V, Keysers C (2009) The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI aata. Cer Cortex 19:1239–1255

    Article  Google Scholar 

  • Ghez C, Pisa M (1972) Inhibition of afferent transmission in cuneate nucleus during voluntary movement in the cat. Brain Res 40:145–151

    Article  PubMed  CAS  Google Scholar 

  • Giabbiconi CM, Dancer C, Zopf R, Gruber T, Müller MM (2004) Selective spatial attention to left or right hand flutter sensation modulates the steady-state somatosensory evoked potential. Brain Res Cogn Brain Res 20:58–66

    Article  PubMed  Google Scholar 

  • Giabbiconi CM, Trujillo-Barreto NJ, Gruber T, Muller MM (2007) Sustained spatial attention to vibration is mediated in primary somatosensory cortex. Neuroimage 35:255–262

    Article  PubMed  Google Scholar 

  • Hamalainen M, Hari R, Ilmoniemi RJ, Knuutila J, Lounasmaa OV (1993) Magnetoencephalography—theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Phys 65:413–497

    Article  CAS  Google Scholar 

  • Jiang W, Chapman CE, Lamarre Y (1990) Modulation of somatosensory evoked responses in the primary somatosensory cortex produced by intracortical microstimulation of the motor cortex in the monkey. Exp Brain Res 80:333–344

    Article  PubMed  CAS  Google Scholar 

  • Jones SJ, Power C (1984) Scalp topography of human SEPs: the effect of interfering tactile stimuli applied to the hand. Electroencephalogr Clin Neurophysiol 58:25–36

    Article  PubMed  CAS  Google Scholar 

  • Kelly EF, Folger SE (1999) EEG evidence of stimulus-directed response dynamics in human somatosensory cortex. Brain Res 815:326–336

    Article  PubMed  CAS  Google Scholar 

  • Maeda F, Kleiner-Fisman G, Pascual-Leone A (2002) Motor facilitation while observing hand actions: specificity of the effect and role of observer’s orientation. J Neurophys 87:1329–1335

    Google Scholar 

  • Mercier C, Sirigu A (2009) Training with virtual visual feedback to alleviate phantom limb pain. Neurorehab Neural Rep 23:587–594

    Article  Google Scholar 

  • Moseley GL (2006) Graded motor imagery for pathologic pain: a randomized controlled trial. Neurology 67:2129–2134

    Article  PubMed  Google Scholar 

  • Muthukumaraswamy SD, Johnson BW (2004a) Primary motor cortex activation during action observation revealed by wavelet analysis of the EEG. Clin Neurophys 115:1760–1766

    Article  Google Scholar 

  • Muthukumaraswamy SD, Johnson BW (2004b) Changes in rolandic mu rhythm during observation of a precision grip. Psychophysiology 41:152–156

    Article  PubMed  CAS  Google Scholar 

  • Nangini C, Ross B, Tam F, Graham SJ (2006) Magnetoencephalographic study of vibrotactile evoked transient and steady-state responses in human somatosensory cortex. Neuroimage 33:252–262

    Article  PubMed  CAS  Google Scholar 

  • Noss RS, Boles CD, Yingling CD (1996) Steady-state analysis of somatosensory evoked potentials. Electroencephalogr Clin Neurophysiol 100:453–461

    PubMed  CAS  Google Scholar 

  • Oouchida Y, Okada T, Nakashima T, Matsumura M, Sadato N, Naito E (2004) Your hand movements in my somatosensory cortex: a visuo-kinesthetic function in human area 2. Neuroreport 15:2019–2023

    Article  PubMed  Google Scholar 

  • Orgs G, Dombrowski JH, Heil M, Jansen-Osmann P (2008) Expertise in dance modulates alpha/beta event-related desynchronization during action observation. Eur J Neurosci 27:3380–3384

    Article  PubMed  Google Scholar 

  • Patuzzo S, Fiaschi A, Manganotti P (2003) Modulation of motor cortex excitability in the left hemisphere during action observation: a single- and paired-pulse transcranial magnetic stimulation study of self- and non-self-action observation. Neuropsychologia 41:1272–1278

    Article  PubMed  Google Scholar 

  • Perrin F, Pernier J, Bertrand O, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72:184–187

    Article  PubMed  CAS  Google Scholar 

  • Pineda JA (2005) The functional significance of mu rhythms: translating “seeing” and “hearing” into “doing”. Brain Res Brain Res Rev 50:57–68

    Article  PubMed  Google Scholar 

  • Pineda JA, Allison BZ, Vankov A (2000) The effects of self-movement, observation, and imagination on mu rhythms and readiness potentials (RP’s): toward a brain-computer interface (BCI). IEEE Trans Rehabil Eng 8:219–222

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran VS, Rogers-Ramachandran D (2008) Sensations referred to a patient’s phantom arm from another subjects intact arm: perceptual correlates of mirror neurons. Med Hypotheses 70:1233–1234

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Craighero L (2004) The mirror-neuron system. Ann Rev Neurosci 27:169–192

    Article  PubMed  CAS  Google Scholar 

  • Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Cogn Brain Res 3:131–141

    Article  CAS  Google Scholar 

  • Rossi S, Tecchio F, Pasqualetti P, Ulivelli M, Pizzella V, Romani GL, Passero S, Battistini N, Rossini PM (2002) Somatosensory processing during movement observation in humans. Clin Neurophysiol 113:16–24

    Article  PubMed  CAS  Google Scholar 

  • Salmelin R, Hari R (1994) Characterization of spontaneous MEG rhythms in healthy adults. Electroencephalogr Clin Neurophysiol 91:237–248

    Article  PubMed  CAS  Google Scholar 

  • Schaefer M, Xu B, Flor H, Cohen LG (2009) Effects of different viewing perspectives on somatosensory activations during observation of touch. Hum Brain Mapp 30:2722–2730

    Article  PubMed  Google Scholar 

  • Seki K, Perlmutter SI, Fetz EE (2003) Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309–1316

    Article  PubMed  CAS  Google Scholar 

  • Snyder AZ (1992) Steady-state vibration evoked potentials: descriptions of technique and characterization of responses. Electroencephalogr Clin Neurophysiol 84:257–268

    Article  PubMed  CAS  Google Scholar 

  • Stefan K, Cohen LG, Duque J, Mazzocchio R, Celnik P, Sawaki L, Ungerleider L, Classen J (2005) Formation of a motor memory by action observation. J Neurosci 25:9339–9346

    Article  PubMed  CAS  Google Scholar 

  • Strafella AP, Paus T (2000) Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11:2289–2292

    Article  PubMed  CAS  Google Scholar 

  • Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 3:151–162

    Article  PubMed  Google Scholar 

  • Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381:520–522

    Article  PubMed  CAS  Google Scholar 

  • Tobimatsu S, Zhang YM, Kato M (1999) Steady-state vibration somatosensory evoked potentials: physiological characteristics and tuning function. Clin Neurophysiol 110:1953–1958

    Article  PubMed  CAS  Google Scholar 

  • Tobimatsu S, Zhang YM, Suga R, Kato M (2000) Differential temporal coding of the vibratory sense in the hand and foot in man. Clin Neurophysiol 111:398–404

    Article  PubMed  CAS  Google Scholar 

  • Tremblay C, Robert M, Pascual-Leone A, Lepore F, Nguyen DK, Carmant L, Bouthillier A, Theoret H (2004) Action observation and execution: intracranial recordings in a human subject. Neurology 63:937–938

    PubMed  CAS  Google Scholar 

  • Yavuzer G, Selles R, Sezer N, Sutbeyaz S, Bussmann JB, Koseoglu F, Atay MB, Stam HJ (2008) Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil 89:393–398

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Réseau Provincial de Recherche en Adaptation-Réadaptation (REPAR). SH was supported by scholarships from the Centre Interdisciplinaire de Recherche en Réadaptation et en Intégration Sociale (CIRRIS) and from the Fonds de la Recherche en Santé du Québec (FRSQ) and the Canadian Institutes of Health Research (CIHR). PJ and CM were supported by salary awards from FRSQ and CIHR. CDV was supported by CNPQ, CAPES, FAPERJ and IBN-net. Authors thank P.-O. Lauzon for software development and assistance in data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Catherine Mercier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voisin, J.I.A., Rodrigues, E.C., Hétu, S. et al. Modulation of the response to a somatosensory stimulation of the hand during the observation of manual actions. Exp Brain Res 208, 11–19 (2011). https://doi.org/10.1007/s00221-010-2448-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-010-2448-3

Keywords

Navigation