Skip to main content
Log in

Automatic motor cortex activation for natural as compared to awkward grips of a manipulable object

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

Abstract

It has been suggested that, relative to natural objects, man-made object representations in the brain are more specifically defined by functional properties that reflect how an object is used and/or what it is used for (Warrington and Shallice 1984). We recorded 123-channel event-related potentials (ERP) in healthy participants during a mental rotation task involving a manipulable (hammer) and a non-manipulable (church) object. Both stimuli had standard and mirror-image versions rotated in four different orientations, resulting for the manipulable object in some natural and some awkward grips. Using spatial cluster analysis, time periods were determined during which the ERP maps differed between stimulus conditions. Specific maps appeared for natural versus awkward grips with the manipulable object at a very early stage (60–116 ms) as well as during a later stage (180–280 ms). Source estimations derived from the topographic data indicated that during the second time window the left motor cortex was significantly activated in the case of natural grips. We argue that the motor programs that are semantically associated with the object are automatically activated when it is presented in graspable orientations.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Binkofski F, Buccino G, Stephan KM, Rizzolatti G, Seitz RJ, Freund HJ (1999) A parieto-premotor network for object manipulation: evidence from neuroimaging. Exp Brain Res 128:210–213

    Article  PubMed  CAS  Google Scholar 

  • Brandeis D, Lehmann D (1986) Event-related potentials of the brain and cognitive processes: approaches and applications. Neuropsychologia 24:151–168

    Article  PubMed  CAS  Google Scholar 

  • Bullier J (2001) Integrated model of visual processing. Brain Res Rev 36:96–107

    Article  PubMed  CAS  Google Scholar 

  • Carpenter PA, Just MA, Keller TA, Eddy W, Thulborn K (1999) Graded functional activation in the visuospatial system with the amount of task demand. J Cogn Neurosci 11:9–24

    Article  PubMed  CAS  Google Scholar 

  • Chao LL, Martin A (2000) Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12:478–484

    Article  PubMed  CAS  Google Scholar 

  • Chao LL, Haxby JV, Martin A (1999) Attribute-based neural substrates in posterior temporal cortex for perceiving and knowing about objects. Nat Neurosci 2:913–919

    Article  PubMed  CAS  Google Scholar 

  • Cooper LA, Shepard RN (1973) Chronometric studies of the rotation of mental images. In: Chase WG (ed) Visual information processing. Academic Press, New York

    Google Scholar 

  • Craighero L, Fadiga L, Umilta C, Rizzolatti G (1996) Evidence for visuomotor priming effect. Neuroreport 8:347–349

    Article  PubMed  CAS  Google Scholar 

  • De’Sperati C, Stucchi N (1997) Recognizing the motion of a graspable object is guided by handedness. Neuroreport 8:2761–2765

    Article  PubMed  CAS  Google Scholar 

  • Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA (2002) Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp 15:95–111

    Article  PubMed  Google Scholar 

  • Gibson JJ (1979) The ecological approach to perception. Houghton Mifflin, Boston

    Google Scholar 

  • Grafton ST, Fagg AH, Woods RP, Arbib MA (1996) Functional anatomy of pointing and grasping in humans. Cereb Cortex 6:226–237

    Article  PubMed  CAS  Google Scholar 

  • Grafton ST, Fadiga L, Arbib MA, Rizzolatti G (1997) Premotor cortex activation during observation and naming of familiar tools. Neuroimage 6:231–236

    Article  PubMed  CAS  Google Scholar 

  • Grave de Peralta R, Gonzalez SL, Lantz G, Michel CM, Landis T (2001) Noninvasive localization of electromagnetic epileptic activity. Method descriptions and simulations. Brain Topogr 14:131–137

    Article  PubMed  Google Scholar 

  • Grave de Peralta R, Menendez R, Murray MM, Michel CM, Martuzzi R, Gonzalez Andino SL (2004) Electrical neuroimaging based on biophysical constraints. Neuroimage 21(2):527–539

    Article  PubMed  Google Scholar 

  • Grefkes C, Weiss PH, Zilles K, Fink GR (2002) Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalences between humans and monkeys. Neuron 35:173–184

    Article  PubMed  CAS  Google Scholar 

  • Grèzes J, Decety J (2002) Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia 40:212–222

    Article  PubMed  Google Scholar 

  • Grèzes J, Tucker M, Armony J, Ellis R, Passingham RE (2003) Objects automatically potentiate action: an fMRI study of implicit processing. Eur J Neurosci 17:2735–2740

    Article  PubMed  Google Scholar 

  • Harris IM, Miniussi C (2003) Parietal lobe contribution to mental rotation demonstrated with rTMS. J Cogn Neurosci 15(3):315–323

    Article  PubMed  Google Scholar 

  • Harris IM, Egan GF, Sonkkila C, Tochon-Danguy HJ, Paxinos G, Watson JD (2000) Selective right parietal lobe activation during mental rotation: a parametric PET study. Brain 123(Pt 1):65–73

    Article  PubMed  Google Scholar 

  • Indovina I, Sanes JN (2001) On somatotopic representation centers for finger movements in human primary motor cortex and supplementary motor area. Neuroimage 13:1027–1034

    Article  PubMed  CAS  Google Scholar 

  • Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18(7):314–320

    Article  PubMed  CAS  Google Scholar 

  • Kellenbach ML, Brett M, Patterson K (2003) Actions speak louder than functions: the importance of manipulability and action in tool representation. J Cogn Neurosci 15(1):30–46

    Article  PubMed  Google Scholar 

  • Lehmann D (1986) Principles of spatial analysis. In: Gevins AS, Rémond A (eds) Handbook of electroencephalography and clinical neurophysiology, vol 1: methods of analysis of brain electrical and magnetic signals. Amsterdam, pp 309–354

    Google Scholar 

  • Lehmann D, Skrandies W (1980) Reference-free of identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48(6):609–621

    Article  PubMed  CAS  Google Scholar 

  • Michel CM, Seeck M, Landis T (1999) Spatiotemporal dynamics of human cognition. News Physiol Sci 14(5):206–214

    PubMed  Google Scholar 

  • Michel CM, Thut G, Morand S, Khateb A, Pegna A, Grave de Peralta R, Gonzalez S, Seeck M, Landis T (2001) Electric source imaging of human brain functions. Brain Res Rev 36(2–3):108–118

    Article  PubMed  CAS  Google Scholar 

  • Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R (2004a) EEG source imaging. Clin Neurophysiol 115:2195–2222

    Article  PubMed  Google Scholar 

  • Michel CM, Seeck M, Murray MM (2005) The speed of visual cognition. In: Hallett M, Phillips L, Schomer D, Mark J (eds) Advances in clinical neurophysiology, vol 57 (in press)

  • Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G (1997) Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol 78:2226–2230

    PubMed  CAS  Google Scholar 

  • Murray MM, Michel CM, Grave de Peralta R, Ortigue S, Brunet D, Gonzalez Andino S, Schnider A (2004) Rapid discrimination of visual and multisensory memories revealed by electrical neuroimaging. Neuroimage 21:125–135

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Parsons LM (1987) Imagined spatial transformations of one’s hands and feet. Cogn Psychol 19:178–241

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD, Michel CM, Lehmann D (1995) Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42(7):658–665

    Article  PubMed  CAS  Google Scholar 

  • Pegna AJ, Khateb A, Spinelli L, Seeck M, Landis T, Michel CM (1997) Unravelling the cerebral dynamics of mental imagery. Hum Brain Mapp 5:410–421

    Article  CAS  PubMed  Google Scholar 

  • Peronnet F, Farah MJ (1989) Mental rotation: an event-related potential study with a validated mental rotation task. Brain Cogn 9:279–288

    Article  PubMed  CAS  Google Scholar 

  • Petit LS, Harris IM (2005) Anatomical limitations in mental transformations of body parts. Vis Cogn 12(5):737–758

    Article  Google Scholar 

  • Petit LS, Pegna AJ, Mayer E, Hauert CA (2003) Representation of anatomical constraints in motor imagery: mental rotation of a body segment. Brain Cogn 51:95–101

    Article  PubMed  CAS  Google Scholar 

  • Richter W, Ugurbil K, Georgopoulos A, Kim SG (1997) Time-resolved fMRI of mental rotation. Neuroreport 8:3697–3702

    Article  PubMed  CAS  Google Scholar 

  • Rizzolatti C, Camarada R, Fogassi L, Gentilucci M, Luppion G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. Area F5 and the control of distal movements. Exp Brain Res 71:491–507

    Article  PubMed  CAS  Google Scholar 

  • Rumiati RI, Weiss PH, Shallice T, Ottoboni G, Noth J, Zilles K, Fink GR (2004) Neural basis of pantomiming the use of visually presented objects. Neuroimage 21:1224–1231

    Article  PubMed  Google Scholar 

  • Sakata H, Taira M, Murata A, Mine S (1995) Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. Cereb Cortex 5:429–438

    Article  PubMed  CAS  Google Scholar 

  • Taira M, Mine S, Georgopoulos AP, Murata A, Sakata H (1990) Parietal cortex neurons of the monkey related to the visual guidance of hand movements. Exp Brain Res 83:29–36

    Article  PubMed  CAS  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 

  • Tucker M, Ellis R (1998) On the relations between seen objects and components of potential actions. J Exp Psychol Hum Percept Perform 24(3):830–846

    Article  PubMed  CAS  Google Scholar 

  • Tucker M, Ellis R (2004) Action priming by briefly presented objects. Acta Psychol 116:185–203

    Article  Google Scholar 

  • Viviani P, Stucchi N (1992) Motor-perceptual interactions. In: Stelmach GE, Requin J (eds) Tutorials in motor behavior II. Elsevier Science, Amsterdam, pp 229–248

    Google Scholar 

  • Warrington EK, Shallice T (1984) Category specific semantic impairments. Brain 107(3):829–854

    Article  PubMed  Google Scholar 

  • Yoshino A, Inoue M, Suzuki A (2000) A topographic electrophysiologic study of mental rotation. Cogn Brain Res 9:121–124

    Article  CAS  Google Scholar 

  • Zacks JM, Gilliam F, Ojemann JG (2003) Selective disturbance of mental rotation by cortical stimulation. Neuropsychologia 41:1659–1667

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by an iMURS Scholarship and the Postgraduate Research Fund from Macquarie University to L. Petit. I. Harris was supported by an ARC Postdoctoral Fellowship. We thank Denis Brunet for the development of the software package Cartool that was used for this analysis, and Rolando Grave de Peralta for the development of the inverse solution algorithm LAURA. We also wish to thank Dr. Jeff Hamm and an anonymous reviewer for their useful comments and suggestions on an earlier draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leila S. Petit.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Petit, L.S., Pegna, A.J., Harris, I.M. et al. Automatic motor cortex activation for natural as compared to awkward grips of a manipulable object. Exp Brain Res 168, 120–130 (2006). https://doi.org/10.1007/s00221-005-0092-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0092-0

Keywords

Navigation