Top

Published in:

Open Access 01-10-2011 | Research Article

Imitation of hand and tool actions is effector-independent

Authors: M. van Elk, H. T. van Schie, H. Bekkering

Published in: Experimental Brain Research | Issue 4/2011

Abstract

Following the theoretical notion that tools often extend one’s body, in the present study, we investigated whether imitation of hand or tool actions is modulated by effector-specific information. Subjects performed grasping actions toward an object with either a handheld tool or their right hand. Actions were initiated in response to pictures representing a grip at an object that could be congruent or incongruent with the required action (grip-type congruency). Importantly, actions could be cued by means of a tool cue, a hand cue, and a symbolic cue (effector-type congruency). For both hand and tool actions, an action congruency effect was observed, reflected in faster reaction times if the observed grip type was congruent with the required movement. However, neither hand actions nor tool actions were differentially affected by the effector represented in the picture (i.e., when performing a tool action, the action congruency effect was similar for tool cues and hand cues). This finding suggests that imitation of hand and tool actions is effector-independent and thereby supports generalist rather than specialist theories of imitation.

Aicken MD, Wilson AD, Williams JH, Mon-Williams M (2007) Methodological issues in measures of imitative reaction times. Brain Cogn 63:304–308. doi:10.1016/j.bandc.2006.09.005 PubMedCrossRef

Anisfeld M (1991) Neonatal imitation. Dev Rev 11:60–97. doi:10.1016/0273-2297(91)90003-7 CrossRef

Arbib MA, Bonaiuto JB, Jacobs S, Frey SH (2009) Tool use and the distalization of the end-effector. Psychol Res 73:441–462. doi:10.1007/s00426-009-0242-2 PubMedCrossRef

Bach P, Knoblich G, Gunter TC, Friederici AD, Prinz W (2005) Action comprehension: deriving spatial and functional relations. J Exp Psychol Hum Percept Perform 31:465–479. doi:10.1037/0096-1523.31.3.465 PubMedCrossRef

Bekkering H, Wohlschlager A, Gattis M (2000) Imitation of gestures in children is goal-directed. Q J Exp Psychol A 53:153–164PubMedCrossRef

Bird G, Brindley R, Leighton J, Heyes C (2007) General processes, rather than “goals,” explain imitation errors. J Exp Psychol Hum Percept Perform 33:1158–1169. doi:10.1037/0096-1523.33.5.1158 PubMedCrossRef

Brass M, Heyes C (2005) Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn Sci 9:489–495. doi:10.1016/j.tics.2005.08.007 PubMedCrossRef

Brass M, Bekkering H, Wohlschlager A, Prinz W (2000) Compatibility between observed and executed finger movements: comparing symbolic, spatial, and imitative cues. Brain Cogn 44:124–143. doi:10.1006/brcg.2000.1225 PubMedCrossRef

Brass M, Bekkering H, Prinz W (2001) Movement observation affects movement execution in a simple response task. Acta Psychol (Amst) 106:3–22. doi:10.1016/S0001-6918(00)00024-X CrossRef

Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, Rizzolatti G (2004) Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron 42:323–334. doi:10.1016/S0896-6273(04)00181-3 PubMedCrossRef

Byrne RW, Russon AE (1998) Learning by imitation: a hierarchical approach. Behav Brain Sci 21:667–684; discussion 684–721

Catmur C, Heyes C (2010) Time course analyses confirm independence of imitative and spatial compatibility. J Exp Psychol Hum Percept Perform. doi:10.1037/a0019325

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. doi:10.1523/JNEUROSCI.2605-09.2009 PubMedCrossRef

Chong TT, Cunnington R, Williams MA, Mattingley JB (2009) The role of selective attention in matching observed and executed actions. Neuropsychologia 47:786–795. doi:10.1016/j.neuropsychologia.2008.12.008 PubMedCrossRef

Clark A (2004) Natural-born cyborgs: minds, technologies and the future of human intelligence. Oxford University Press, Oxford

Dassonville P, Lewis SM, Zhu XH, Ugurbil K, Kim SG, Ashe J (2001) The effect of stimulus-response compatibility on cortical motor activation. Neuroimage 13:1–14. doi:10.1006/nimg.2000.0671 PubMedCrossRef

Ferrari PF, Rozzi S, Fogassi L (2005) Mirror neurons responding to observation of actions made with tools in monkey ventral premotor cortex. J Cogn Neurosci 17:212–226. doi:10.1162/0898929053124910 PubMedCrossRef

Franz EA, Ford S, Werner S (2007) Brain and cognitive processes of imitation in bimanual situations: Making inferences about mirror neuron systems. Brain Res 1145:138–149. doi:10.1016/j.brainres.2007.01.136 PubMedCrossRef

Gazzola V, van der Worp H, Mulder T, Wicker B, Rizzolatti G, Keysers C (2007) Aplasics born without hands mirror the goal of hand actions with their feet. Curr Biol 17:1235–1240. doi:10.1016/j.cub.2007.06.045 PubMedCrossRef

Gentilucci M, Roy AC, Stefanini S (2004) Grasping an object naturally or with a tool: are these tasks guided by a common motor representation? Exp Brain Res 157:496–506. doi:10.1007/s00221-004-1863-8 PubMedCrossRef

Glover S (2004) Separate visual representations in the planning and control of action. Behav Brain Sci 27:3–24; discussion 24–78

Grafton ST, Hamilton AF (2007) Evidence for a distributed hierarchy of action representation in the brain. Hum Mov Sci 26:590–616. doi:10.1016/j.humov.2007.05.009 PubMedCrossRef

Heiser M, Iacoboni M, Maeda F, Marcus J, Mazziotta JC (2003) The essential role of Broca’s area in imitation. Eur J Neurosci 17:1123–1128. doi:10.1046/j.1460-9568.2003.02530.x PubMedCrossRef

Heyes C (2011) Automatic imitation. Psychol Bull 137:463–483. doi:10.1037/a0022288 PubMedCrossRef

Holmes NP, Calvert GA, Spence C (2004) Extending or projecting peripersonal space with tools? Multisensory interactions highlight only the distal and proximal ends of tools. Neurosci Lett 372:62–67. doi:10.1016/j.neulet.2004.09.024 PubMedCrossRef

Holmes NP, Sanabria D, Calvert GA, Spence C (2007) Tool-use: capturing multisensory spatial attention or extending multisensory peripersonal space? Cortex 43:469–489. doi:10.1016/S0010-9452(08)70471-4 PubMedCrossRef

Hommel B, Musseler 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; discussion 878–937

Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286:2526–2528. doi:10.1126/science.286.5449.2526 PubMedCrossRef

Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7:2325–2330PubMedCrossRef

Jacobs S, Danielmeier C, Frey SH (2010) Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool. J Cogn Neurosci 22:2594–2608. doi:10.1162/jocn.2009.21372 PubMedCrossRef

Jansson E, Wilson AD, Williams JH, Mon-Williams M (2007) Methodological problems undermine tests of the ideo-motor conjecture. Exp Brain Res 182:549–558. doi:10.1007/s00221-007-1013-1 PubMedCrossRef

Jonas M, Biermann-Ruben K, Kessler K et al (2007a) Observation of a finger or an object movement primes imitative responses differentially. Exp Brain Res 177:255–265. doi:10.1007/s00221-006-0660-y PubMedCrossRef

Jonas M, Siebner HR, Biermann-Ruben K et al (2007b) Do simple intransitive finger movements consistently activate frontoparietal mirror neuron areas in humans? Neuroimage 36(Suppl 2):T44–T53. doi:10.1016/j.neuroimage.2007.03.028 PubMedCrossRef

Jones SS (2009) The development of imitation in infancy. Phil Trans R Soc Lond B Biol Sci 364:2325–2335. doi:10.1098/rstb.2009.0045 CrossRef

Kilner JM, Paulignan Y, Blakemore SJ (2003) An interference effect of observed biological movement on action. Curr Biol 13:522–525. doi:10.1016/S0960-9822(03)00165-9 PubMedCrossRef

Koski L, Iacoboni M, Dubeau MC, Woods RP, Mazziotta JC (2003) Modulation of cortical activity during different imitative behaviors. J Neurophysiol 89:460–471. doi:10.1152/jn.00248.2002 PubMedCrossRef

Maravita A, Spence C, Kennett S, Driver J (2002) Tool-use changes multimodal spatial interactions between vision and touch in normal humans. Cognition 83:B25–B34. doi:10.1016/S0010-0277(02)00003-3 PubMedCrossRef

Massen C (2009) Observing human interaction with physical devices. Exp Brain Res 199:49–58. doi:10.1007/s00221-009-1971-6 PubMedCrossRef

Massen C, Prinz W (2009) Movements, actions and tool-use actions: an ideomotor approach to imitation. Phil Trans R Soc Lond B Biol Sci 364:2349–2358. doi:10.1098/rstb.2009.0059 CrossRef

Meltzoff AN, Moore MK (1989) Imitation in newborn infants: exploring the range of gestures imitated and the underlying mechanisms. Dev Psychol 25:954–962. doi: 10.1037/0012-1649.25.6.954

Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83:639–651PubMed

Newman-Norlund RD, Noordzij ML, Meulenbroek RG, Bekkering H (2007a) Exploring the brain basis of joint action: co-ordination of actions, goals and intentions. Soc Neurosci 2:48–65. doi:10.1080/17470910701224623 PubMedCrossRef

Newman-Norlund RD, van Schie HT, van Zuijlen AM, Bekkering H (2007b) The mirror neuron system is more active during complementary compared with imitative action. Nat Neurosci 10:817–818. doi:10.1038/nn1911 PubMedCrossRef

Newman-Norlund RD, Ondobaka S, van Schie HT, van Elswijk G, Bekkering H (2010) Virtual lesions of the IFG abolish response facilitation for biological and non-biological cues. Front Behav Neurosci 4:5. doi:10.3389/neuro.08.005.2010 PubMed

Perani D, Fazio F, Borghese NA, Tettamanti M, Ferrari S, Decety J, Gilardi MC (2001) Different brain correlates for watching real and virtual hand actions. Neuroimage 14:749–758. doi:10.1006/nimg.2001.0872 PubMedCrossRef

Press C, Bird G, Flach R, Heyes C (2005) Robotic movement elicits automatic imitation. Brain Res Cogn Brain Res 25:632–640. doi:10.1016/j.cogbrainres.2005.08.020 PubMedCrossRef

Prinz W (1997) Perception and action planning. J Cogn Psychol 9:129–154. doi:10.1080/713752551 CrossRef

Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661–670. doi:10.1038/35090060 PubMedCrossRef

Rosenbaum DA, Inhoff AW, Gordon AM (1984) Choosing between movement sequences: A hierarchical editor model. J Exp Psychol Hum Percept Perform 113:372–393. doi:10.1037/0096-3445.113.3.372

Rosenbaum DA, Cohen RG, Jax SA, Weiss DJ, van der Wel R (2007) The problem of serial order in behavior: Lashley’s legacy. Hum Mov Sci 26:525–554. doi:10.1016/j.humov.2007.04.001 PubMedCrossRef

Schultz AE, Kuiken TA (2011) Neural interfaces for control of upper limb prostheses: the state of the art and future possibilities. PM R 3:55–67. doi:10.1016/j.pmrj.2010.06.016 PubMed

Shin YK, Proctor RW, Capaldi EJ (2010) A review of contemporary ideomotor theory. Psychol Bull 136:943–974. doi:10.1037/a0020541 PubMedCrossRef

Tai YF, Scherfler C, Brooks DJ, Sawamoto N, Castiello U (2004) The human premotor cortex is ‘mirror’ only for biological actions. Curr Biol 14:117–120. doi:10.1016/j.cub.2004.01.005 PubMedCrossRef

Umilta MA, Escola L, Intskirveli I et al (2008) When pliers become fingers in the monkey motor system. Proc Natl Acad Sci USA 105:2209–2213. doi:10.1073/pnas.0705985105 PubMedCrossRef

van der Helden J, van Schie HT, Rombouts C (2010) Observational learning of new movement sequences is reflected in fronto-parietal coherence. PLoS One 5:e14482. doi:10.1371/journal.pone.0014482 PubMedCrossRef

van Elk M, van Schie HT, Bekkering H (2008) Conceptual knowledge for understanding other’s actions is organized primarily around action goals. Exp Brain Res 189:99–107. doi:10.1007/s00221-008-1408-7 PubMedCrossRef

van Schie HT, van Waterschoot BM, Bekkering H (2008) Understanding action beyond imitation: reversed compatibility effects of action observation in imitation and joint action. J Exp Psychol Hum Percept Perform 34:1493–1500. doi:10.1037/a0011750 PubMedCrossRef

Wohlschlager A, Gattis M, Bekkering H (2003) Action generation and action perception in imitation: an instance of the ideomotor principle. Phil Trans R Soc Lond B Biol Sci 358:501–515. doi:10.1098/rstb.2002.1257 CrossRef

Title: Imitation of hand and tool actions is effector-independent
Authors: M. van Elk
H. T. van Schie
H. Bekkering
Publication date: 01-10-2011
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 4/2011
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-011-2852-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Imitation of hand and tool actions is effector-independent

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2011

Anatomically constrained minimum variance beamforming applied to EEG

On-line effects of quadripulse transcranial magnetic stimulation (QPS) on the contralateral hemisphere studied with somatosensory evoked potentials and near infrared spectroscopy

Frames of reference and categorical and coordinate spatial relations: a hierarchical organisation

Form of the compensatory stepping response to repeated laterally directed postural disturbances

Locomoting-to-reach: information variables and control strategies for nested actions

Rhythmic arm cycling differentially modulates stretch and H-reflex amplitudes in soleus muscle