Top

Published in:

01-07-2013 | Research Article

Imitation behavior is sensitive to visual perspective of the model: an fMRI study

Authors: Rui Watanabe, Takahiro Higuchi, Yoshiaki Kikuchi

Published in: Experimental Brain Research | Issue 2/2013

Abstract

Imitation behavior and accompanying brain activity can be affected by the perspective of the model adopted. The present study was designed to understand the effect of a model’s perspective in terms of the view (1st person vs. 3rd person) and the anatomical congruency of the limb between the model and the performer (congruent vs. incongruent). Eighteen young participants observed video clips of a model’s finger-lifting behavior and lifted the same finger on their right hand as quickly as possible. Half of the video clips were filmed from the view of the participant (the 1st person view), whereas the other half were filmed from the perspective of facing a mirror (the 3rd person view). Each video clip depicted the finger lifting of the model’s right (congruent) or left (incongruent) hand. Comparisons of the latency to imitate among the four perspective conditions showed significantly shorter latency for the 1st person-congruent and 3rd person-incongruent conditions. Hemodynamic measurements with functional magnetic resonance imaging showed that shorter latency was explained with less involvement of the brain areas that are activated when a task is relatively complex. The brain areas considered to be a part of neural substrates of imitation were significantly activated under the 1st person view conditions regardless of the hand congruency. These findings suggest that, although the latency to imitate finger lifting was determined by the complexity of the task induced with the model’s perspective, imitation behavior seemed to be more effectively guided with the models filmed from the 1st person view.

Alaerts K, Heremans E, Swinnen SP, Wenderoth N (2009) How are observed actions mapped to the observer’s motor system? Influence of posture and perspective. Neuropsychologia 47:415–422PubMedCrossRef

Allison T, Puce A, McCarthy G (2000) Social perception from visual cues: role of the STS region. Trend Cogn Sci 4:267–278CrossRef

Bekkering H, Wohlschlager A (2000) Imitation of gestures in children is goal–directed. Q J Exp Psychol A 53A(1):153–164

Botvinick M, Nystrom LE, Fissell K, Carter CS, Cohen JD (1999) Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402:179–181PubMedCrossRef

Brass M, Heys C (2005) Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cog Sci 9(10):489–495CrossRef

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(2):124–143PubMedCrossRef

Brass M, Bekkering H, Prinz W (2001) Movement observation affects movement execution in a simple response task. Acta Psychol 106(1–2):3–22CrossRef

Buccino G, Binfoski F, Lucia R (2003) The mirror neuron system and action recognition. Brain Lang 89:370–376CrossRef

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(2):323–334PubMedCrossRef

Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749PubMedCrossRef

Chaminade T, Meltzoff AN, Decety J (2005) An fMRI study of imitation: action representation and body schema. Neuropsychologia 43:115–127PubMedCrossRef

Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215PubMedCrossRef

Ehrsson H, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H (2000) Cortical activity in precision-versus power-grip tasks: an fMRI study. J Neurophysiol 83(1):528–536PubMed

Felician O, Romaiguere P, Anton JL, Nazarian B, Roth M, Poncet M, Roll JP (2004) The role of human left superior parietal lobule in body part localization. Ann Neurol 55(5):749–751PubMedCrossRef

Gleissner B, Meltzoff AN, Bekkering H (2000) Children’s coding of human action: cognitive factors influencing imitation in 3-year-olds. Dev Sci 3:405–414CrossRef

Goldenberg G, Karnath H (2006) The neural basis of imitation is body part specific. J Neurosci 26:6282–6287PubMedCrossRef

Grafton S, Mazziotta J, Woods R, Phelps M (1992) Human functional anatomy of visually guided finger movements. Brain 115:565–587PubMedCrossRef

Grezes J, Decety J (2001) Functional anatomy of execution, mental simulation, observation, and verb generation of actions: a meta-analysis. Hum Brain Mapp 12(1):1–19PubMedCrossRef

Grezes J, Costes N, Decety J (1999) The effects of learning and intention on the neural network involved in the perception of meaningless actions. Brain 122:1875–1877PubMedCrossRef

Heiser M, Iacoboni M, Maeda F, Marcus J, Mazziotta JC (2003) The essential role of Broca’s area in imitation. Eur J Neurosci 17(5):1123–1128PubMedCrossRef

Iacoboni M, Dapretto M (2006) The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7(12):942–951PubMedCrossRef

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

Iacoboni M, Koski L, Brass M, Bekkering M, Woods H, Dubeau RP, Mazziotta MC, Rizzolatti G (2001) Reafferent copies of imitated actions in the right superior temporal cortex. Proc Natl Acad Sci USA 98(24):13995–13999PubMedCrossRef

Iacoboni M, Molnar-Szakacs I, Gallese V, Buccino G, Mazziotta JC, Rizzolatti G (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3(3):e79PubMedCrossRef

Iacoboni M (2005) Neural mechanisms of imitation. Curr Opin Neurobio 15(6):632–637CrossRef

Ishihara M, Imanaka K (2008) Visual perception and motor preparation of manual aiming: A review of behavioral studies and neural correlates. In: Nilsson IL, Lindberg WV (eds) Visual perception: new research. Nova Science Publishers, Hauppauge, pp 1–48

Ishihara M, Imanaka K, Mori S (2002) Lateralized effects of target location on reaction times when preparing for manual aiming at a visual target. Hum Mov Sci 21(5–6):563–582PubMedCrossRef

Jackson PL, Meltzoff AN, Decety J (2006) Neural circuits involved in imitation and perspective-taking. Neuroimage 31(1):429–439PubMedCrossRef

Jastorff J, Orban GA (2009) Human functional magnetic resonance imaging reveals separation and integration of shape and motion cues in biological motion processing. J Neurosci 29(22):7315–7329PubMedCrossRef

Johnson-Frey SH, Maloof FR, Newman-Norlund R, Farrer C, Inati S, Grafton ST (2003) Actions or hand-object interactions? Human inferior frontal cortex and action observation. Neuron 39(6):1053–1058PubMedCrossRef

Karnath HO, Baier B, Nagele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex? J Neurosci 25(31):7134–7138PubMedCrossRef

Koski L, Wohlschlager A, Bekkering H, Woods RP, Dubeau M-C, Mazziotta J, Iacoboni M (2002) Modulation of motor and premotor activity during imitation of target-directed actions. Cereb Cortex 12:847–855PubMedCrossRef

Koski L, Iacoboni M, Dubeau MC, Woods RP, Mazziotta JC (2003) Modulation of cortical activity during different imitative behaviors. J Neurophysiol 89(1):460–471PubMedCrossRef

Magno E, Foxe J, Mloholm S, Robertson I, Garavan H (2006) The anterior cingulate and error avoidance. J Neurosci 26(18):4679–4773CrossRef

Mengotti P, Corradi-Dell’acqua C, Rumiati RI (2012) Imitation components in the human brain: an fMRI study. Neuroimage 59(2):1622–1630PubMedCrossRef

Molenberghs P, Cunnington R, Mattingley JB (2009) Is the mirror neuron system involved in imitation? A short review and meta-analysis. Neurosci Biobehav Rev 33(7):975–980PubMedCrossRef

Molenberghs P, Brander C, Mattingly JB, Cunnington R (2010) The role of superior temporal sulcus and the mirror neuron system in imitation. Hum Brain Map 31(9):1316–1326CrossRef

Molnar-Szakacs I, Iacoboni M, Koski L, Mazziotta JC (2005) Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation. Cereb Cortex 15(7):986–994PubMedCrossRef

Ocampo B, Kritikos A, Cunnington R (2011) How frontoparietal brain regions mediate imitative and complementary actions: an fMRI study. PLoS ONE 6(10):e26496CrossRef

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

Parkinson A, Condon L, Jackson SR (2010) Parietal cortex coding of limb posture: in search of the body-schema. Neuropsychologia 48:3228–3234PubMedCrossRef

Prinz W (1997) Perception and action planning. Eur J Cogn Psychol 9(2):129–154CrossRef

Rizzolatti G, Arbib M (1998) Language within our grasp. Trends Neurosci 21(5):188–194PubMedCrossRef

Sadato N, Campbell G, Ibanez V, Deiber M, Hallett M (1996) Complexity affects regional cerebral blood flow change during sequential finger movements. J Neurosci 16(8):2691–2700PubMed

Saito DN, Okada T, Morita Y, Yonekura Y, Sadato N (2003) Tactile-visual cross-modal shape matching: a functional MRI study. Brain Res Cogn Brain Res 17(1):14–25PubMedCrossRef

Schluter ND, Krams M, Rushworth MF, Passingham RE (2001) Cerebral dominance for action in the human brain: the selection of actions. Neuropsychologia 39(2):105–113PubMedCrossRef

Schofield WN (1976) Do children find movements which cross the body midline difficult? Q J Exp Psychol 28:571–582CrossRef

Tanaka S, Inui T (2002) Cortical involvement for action imitation of hand/arm postures versus finger configurations: an fMRI study. NeuroReport 13(13):1599–1602PubMedCrossRef

Tsakiris M, Hesse MD, Boy C, Haggard P, Fink GR (2007) Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cereb Cortex 17(10):2235–2244PubMedCrossRef

van Elk M, van Schie HT, Bekkering H (2011) Imitation of hand and tool action is effector-independent. Exp Brain Res 214(4):539–547PubMedCrossRef

Vingerhoets G, Stevens L, Meesdom M, Honore P, Vandemaele P, Achten E (2012) Influence of perspective on the neural correlates of motor resonance during natural action observation. Neuropsychol Rehabil 22(5):752–767PubMedCrossRef

Wakita M, Hiraishi H (2011) Effects of handedness and viewing perspective on Broca’s area activity. NeuroReport 22(7):331–336PubMedCrossRef

Watanabe R, Watanabe S, Kuruma H, Murakami Y, Senoo A, Matsuda T (2011) Neural activation during imitation of movements presented from four different perspectives: a functional magnetic resonance imaging study. Neurosci Lett 503(2):100–104PubMedCrossRef

Williams JH, Whiten A, Waiter GD, Pechey S, Perrett DI (2007) Cortical and subcortical mechanisms at the core of imitation. Soc Neurosci 2(1):66–78PubMedCrossRef

Title: Imitation behavior is sensitive to visual perspective of the model: an fMRI study
Authors: Rui Watanabe
Takahiro Higuchi
Yoshiaki Kikuchi
Publication date: 01-07-2013
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 2/2013
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-013-3548-7

At a glance: The STEP trials

Springer Medicine

Imitation behavior is sensitive to visual perspective of the model: an fMRI study

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2013

The influence of motor cortical stimulus intensity on the relaxation rate of human lower limb muscles

Dopamine, norepinephrine, and the management of sensorimotor bindings: individual differences in updating of stimulus–response episodes are predicted by DAT1, but not DBH5′-ins/del

Quantifying connectivity via efferent and afferent pathways in motor control using coherence measures and joint position perturbations

A 7T fMRI study of cerebellar activation in sequential finger movement tasks

“Self pop-out”: agency enhances self-recognition in visual search

Adaptation of lift forces in object manipulation through action observation