Skip to main content
SpringerLink
Log in

Activity of human motor system during action observation is modulated by object presence

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

Abstract

Neurons in the monkey mirror neuron system (MNS) become active when actions are observed or executed. Increases in activity are greater when objects are engaged than when the actions are mimed. This modulation occurs even when object manipulation is hidden from view. We examined whether human motor systems are similarly modulated during action observation because such observation-related modulations are potentially mediated by a putative human MNS. Transcranial magnetic stimulation (TMS) was used to elicit motor-evoked potentials (MEPs) of a grasping muscle while participants observed actual or pantomimed grasping movements whose endpoints were sometimes hidden from view. MEP amplitudes were found to be modulated by object presence. Critically, the object-based modulation was found when the participant directly observed object manipulation and when the object manipulation had to be inferred because it was hidden. These findings parallel studies of MNS activity in monkeys and support the hypothesis that the MNS influences motor system activity during action observation. Although the object-based modulation of MEP amplitudes was consistent with the hypotheses, the direction of the modulation was not—MEP amplitudes decreased during action observation in contrast to the increase that has previously been observed. We suggest that the decrease in MEP amplitude on object-present trials resulted from inhibitory mechanisms that were activated to suppress the observation-evoked response codes from generating overt muscle activity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Notes

  1. Note that these specific comparisons were also statistically tested using a series of planned comparisons using one-tailed t tests (p < 0.05). The results of the secondary planned comparison analysis were consistent with the main Tukey’s HSD analysis reported here—MEP amplitudes on Object-Present trials were different from those on Object-Absent trials during the grasp and transport phases, but not rest phase, in both Full and Partial Vision conditions. Although a series of planned t test comparisons is a more conventional method for conducting such planned comparisons, we chose to report the results of the more conservative Tukey’s HSD test. We chose to report the more conservative test as the main analysis because: (1) the observed pattern of differences was in the opposite direction to what was predicted and what has been observed in previous studies; and (2) we were conducting a post hoc test of a non-significant interaction.

  2. Although the present study was motivated by previous neurophysiological research, it should be noted that the anticipatory and inferred modulation of the corticospinal tract is also broadly consistent with theoretical accounts of the processes of action observation, imitation, and joint action based on ideomotor theory (e.g., Prinz 2005; Sebanz and Knoblich 2009). According to ideomotor theory, action plans and their associated effects on the environment are tightly linked and maintained in a common representation (Hommel et al. 2001; Prinz 1997). The critical implication of this proposed common coding system for the present discussion is that, because action plans and effects are tightly linked in these common representations, it is possible that the perception (actual, imagined, or inferred) of a goal-directed action effect (e.g., the grasp and lifting of an apple) can automatically activate the motor plan associated with that effect. Thus, the pattern of corticospinal modulation observed here may have occurred because the anticipation and perception (Full Vision condition) or imagination/visualization (Partial Vision condition) of the grasp and lift activated the grasping plan in the motor system and, subsequently, the inhibitory mechanism preventing overt imitation. Because investigations of the cortical areas involved in ideomotor coding is in its early stages of development and has focused exclusively on single person action execution contexts (i.e., the research has not directly addressed action observation—Elsner et al. 2002; Melcher et al. 2008), it is unclear at this point how compatible the ideomotor account is with the neurophysiological research that motivated the present study. However, it is clear that, on the conceptual level, the pattern of effects observed in the present study is congruent with the ideomotor account of action observation and joint action.

  3. We thank an anonymous reviewer for pointing us in the direction of this literature.

References

  • Baldissera F, Cavallari P, Craighero L, Fadiga L (2001) Modulation of spinal excitability during observation of hand actions in humans. Eur J Neurosci 13:190–194

    Article  CAS  PubMed  Google Scholar 

  • Brass M, Heyes C (2005) Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn Sci 9:489–495

    Article  PubMed  Google Scholar 

  • Bryden MP (1977) Measuring handedness with questionnaires. Neuropsychologia 15:617–624

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Buccino G, Riggio L, Melli G, Binkofski F, Gallese V, Rizzolatti G (2005) Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. Brain Res Cogn Brain Res 24:355–363

    Article  CAS  PubMed  Google Scholar 

  • Carson RG, Welsh TN, Pamblanco-Valero MA (2005) Visual feedback alters the variations in corticospinal excitability that arise from rhythmic movements of the opposite limb. Exp Brain Res 161:325–334

    Article  CAS  PubMed  Google Scholar 

  • Cattaneo L, Caruana F, Jezzini A, Rizzolatti G (2009) Representation of goal and movements without overt motor behavior in the human motor cortex: a transcranial magnetic stimulation study. J Neurosci 29:11134–11138

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekharan S, Athreya D, Srinivasan N (2006) Twists and Oliver Twists in mental rotation: complementary actions as orphan processes. In: Sun R, Miyake N (eds) Proceedings of the 28th annual meeting of the cognitive science society. Vancouver, Canada, pp 1092–1097

    Google Scholar 

  • Chersi F, Thill S, Ziemke T, Borghi AM (2010) Sentence processing: linking language to motor chains. Front Neurorobotics 4:4

    PubMed  Google Scholar 

  • de Vega M, Robertson DA, Glenberg AM, Kaschak MP, Rinck M (2004) On doing two things at once: temporal constraints on actions in language comprehension. Mem Cognit 32:1033–1043

    Article  PubMed  Google Scholar 

  • Decety J, Grezes J, Costes N, Perani D, Jeannerod M, Procyk E (1997) Brain activity during observation of actions—influence of action content and subject’s strategy. Brain 120:1763–1777

    Article  PubMed  Google Scholar 

  • Decety J, Chaminade T, Grezes J, Meltzoff A (2002) A PET exploration of the neural mechanisms involved in reciprocal imitation. Neuroimage 15:265–272

    Article  CAS  PubMed  Google Scholar 

  • Elsner B, Hommel B, Mentschel C, Drzezga A, Prinz W, Conrad B, Siebner H (2002) Linking actions and their perceivable consequences in the human brain. Neuroimage 17:364–372

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308:662–667

    Article  CAS  PubMed  Google Scholar 

  • Ford K, Goltz H, Brown M, Everling S (2005) Neural processes associated with antisaccade task performance investigated with event-related fMRI. J Neurophysiol 94:429–440

    Article  PubMed  Google Scholar 

  • Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 data. Cereb Cortex 19:1239–1255

    Article  PubMed  Google Scholar 

  • Hari R, Forss N, Avikainen S, Veskari E, Salenius S, Rizzolatti G (1998) Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc Natl Acad Sci USA 95:15061–15065

    Article  CAS  PubMed  Google Scholar 

  • Hommel B, Müsseler J, Aschersleben G, Prinz W (2001) The theory of event coding (TEC): a framework for perception and action planning. Behav Brain Sci 24:849–878

    Article  CAS  PubMed  Google Scholar 

  • Howard LA, Tipper SP (1997) Hand deviations away from visual cues: indirect evidence for inhibition. Exp Brain Res 113:144–152

    Article  CAS  PubMed  Google Scholar 

  • Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286:2526–2528

    Article  CAS  PubMed  Google Scholar 

  • Kraskov A, Dancause N, Quallo MM, Shepherd S, Lemon RN (2009) Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression? Neuron 64:922–930

    Article  CAS  PubMed  Google Scholar 

  • Melcher T, Weidema M, Eenshuistra RM, Hommel B, Gruber O (2008) The neural substrate of the ideomotor principle: an event-related fMRI analysis. Neuroimage 39:1274–1288

    Article  PubMed  Google Scholar 

  • Mukamel R, Ekstrom AD, Kaplan J, Iacoboni M, Fried I (2010) Single-neuron responses in humans during execution and observation of actions. Curr Biol 20:750–756

    Article  CAS  Google Scholar 

  • Oliveri M, Finocchiaro C, Shapiro K, Gangitano M, Caramazza A, Pascual-Leone A (2004) All talk and no action: a transcranial magnetic stimulation study of motor cortex activation during action word production. J Cogn Neurosci 16:374–381

    Article  PubMed  Google Scholar 

  • Papeo L, Vallesi A, Isaja A, Rumiati RI (2009) Effects of TMS on different stages of motor and non-motor verb processing in the primary motor cortex. PLoS One 4:e4508

    Article  PubMed  Google Scholar 

  • Petrides M (2005) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci 360:781–795

    Article  PubMed  Google Scholar 

  • Prinz W (1997) Perception and action planning. Euro J Cogn Psychol 9:129–154

    Article  Google Scholar 

  • Prinz W (2005) An ideomotor approach to imitation. In: Hurley S, Chater N (eds) Perspectives on imitation: from neuroscience to social science. Cambridge, Massachusetts, United States, pp 141–156

    Google Scholar 

  • Ray M (2009) The mirror neuron system and observational learning. M.Sc. Thesis, University of Calgary

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Scorolli C, Borghi AM (2007) Sentence comprehension and action: effector specific modulation of the motor system. Brain Res 1130:119–124

    Article  CAS  PubMed  Google Scholar 

  • Sebanz N, Knoblich G (2009) Prediction in joint action: what, when, and where. Top Cogn Sci 1:353–367

    Article  Google Scholar 

  • Sohn YH, Hallett M (2004) Surround inhibition in human motor system. Exp Brain Res 158:397–404

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Umilta M, Kohler E, Gallese V, Fogassi L, Fadiga L, Keysers C, Rizzolatti G (2001) I know what you are doing: a neurophysiological study. Neuron 31:155–165

    Article  CAS  PubMed  Google Scholar 

  • van Leeuwen ML, van Barren RB, Martin D, Dijksterhuis A, Bekkering H (2009) Executive functioning and imitation: increasing working memory load facilitates behavioral imitation. Neuropsychologia 47:3265–3270

    Article  PubMed  Google Scholar 

  • Welsh TN, Elliott D (2004) Movement trajectories in the presence of a distracting stimulus: evidence for a response activation model of selective reaching. Q J Exp Psychol A 57:1031–1057

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported through grants from the Natural Sciences and Engineering Research Council, Alberta Ingenuity Fund, Ontario Ministry of Research and Innovation, and Canada Foundation for Innovation. Please note that this study was collected while the authors were members of the Faculty of Kinesiology at the University of Calgary.

Author information

Authors and Affiliations

  1. Institute of Neuroinformatics, University of Zurich and ETH Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Michael Villiger

  2. School of Interactive Computing, Georgia Institute of Technology, Technology Square Research Building, 85 Fifth Street NW, Atlanta, GA, 30308–0760, USA

    Sanjay Chandrasekharan

  3. Faculty of Physical Education and Health, University of Toronto, 55 Harbord St., Toronto, ON, M5S 2W6, Canada

    Timothy N. Welsh

Authors
  1. Michael Villiger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanjay Chandrasekharan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy N. Welsh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Villiger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Villiger, M., Chandrasekharan, S. & Welsh, T.N. Activity of human motor system during action observation is modulated by object presence. Exp Brain Res 209, 85–93 (2011). https://doi.org/10.1007/s00221-010-2522-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-010-2522-x

Keywords

Search

Navigation