Abstract
A region in human lateral occipital cortex (the 'extrastriate body area' or EBA) has been implicated in the perception of body parts. Here we report functional magnetic resonance imaging (fMRI) evidence that the EBA is strongly modulated by limb (arm, foot) movements to a visual target stimulus, even in the absence of visual feedback from the movement. Therefore, the EBA responds not only during the perception of other people's body parts, but also during goal-directed movements of the observer's body parts. In addition, both limb movements and saccades to a detected stimulus produced stronger signals than stimulus detection without motor movements ('covert detection') in the calcarine sulcus and lingual gyrus. These motor-related modulations cannot be explained by simple visual or attentional factors related to the target stimulus, and suggest a potentially widespread influence of actions on visual cortex.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).
Corbetta, M., Miezin, F.M., Dobmeyer, S., Shulman, G.L. & Petersen, S.E. Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J. Neurosci. 11, 2383–2402 (1991).
Miller, E.K., Li, L. & Desimone, R. Activity of neurons in anterior inferior temporal cortex during a short-term memory task. J. Neurosci. 13, 1460–1478 (1993).
Macaluso, E., Frith, C.D. & Driver, J. Crossmodal spatial influences of touch on extrastriate visual areas take current gaze direction into account. Neuron 34, 647–658 (2002).
Wurtz, R.H. & Mohler, C.W. Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. J. Neurophysiol. 39, 745–765 (1976).
Tolias, A.S. et al. Eye movements modulate visual receptive fields of V4 neurons. Neuron 29, 757–767 (2001).
Chelazzi, L. & Corbetta, M. in The New Cognitive Neurosciences (ed. Gazzaniga, M.S.) 667–686 (MIT, Cambridge, Massachusetts, 2000).
Fischer, B., Boch, R. & Bach, M. Stimulus versus eye movements: comparison of neural activity in the striate and prelunate visual cortex (A17 and A19) of trained rhesus monkey. Exp. Brain. Res. 43, 69–77 (1981).
Downing, P.E., Jiang, Y., Shuman, M. & Kanwisher, N. A cortical area selective for visual processing of the human body. Science 293, 2470–2473 (2001).
Grossman, E.D. & Blake, R. Brain areas active during visual perception of biological motion. Neuron 35, 1167–1175 (2002).
Goldberg, M.E. & Bushnell, M.C. Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. J. Neurophysiol. 46, 773–787 (1981).
Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron 21, 761–773 (1998).
O'Craven, K.M. & Kanwisher, N. Mental imagery of faces and places activates corresponding stiimulus-specific brain regions. J. Cogn. Neurosci. 12, 1013–1023 (2000).
Porro, C.A. et al. Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J. Neurosci. 16, 7688–7698 (1996).
Hanakawa, T. et al. Functional properties of brain areas associated with motor execution and imagery. J. Neurophysiol. 89, 989–1002 (2003).
Corbetta, M., Kincade, J.M., Ollinger, J.M., McAvoy, M.P. & Shulman, G.L. Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat. Neurosci. 3, 292–297 (2000).
Tootell, R.B., Tsao, D. & Vanduffel, W. Neuroimaging weighs in: humans meet macaques in “Primate” visual cortex. J. Neurosci. 23, 3981–3989 (2003).
Spelke, E. Initial knowledge: six suggestions. Cognition 50, 431–445 (1994).
Burton, H. et al. Adaptive changes in early and late blind: a fMRI study of Braille reading. J. Neurophysiol. 87, 589–607 (2002).
Amedi, A., Malach, R., Hendler, T., Peled, S. & Zohary, E. Visuo-haptic object-related activation in the ventral visual pathway. Nat. Neurosci. 4, 324–330 (2001).
Evarts, E.V. & Fromm, C. Transcortical reflexes and servo control of movement. Can. J. Physiol. Pharmacol. 59, 757–775 (1981).
Sperry, R.W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950).
Wurtz, R.H. & Sommer, M.A. Identifying corollary discharges for movement in the primate brain. Prog. Brain. Res. 144, 47–60 (2004).
Nakamura, K. & Colby, C.L. Visual, saccade-related, and cognitive activation of single neurons in monkey exstrastriate area V3A. J. Neurophysiol. 84, 677–692 (2000).
Duhamel, J.R., Colby, C.L. & Goldberg, M.E. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 90–92 (1992).
Blanke, O., Ortigue, S., Landis, T. & Seeck, M. Stimulating illusory own-body perceptions. Nature 419, 269–270 (2002).
Halligan, P.W., Marshall, J.C. & Wade, D.T. Unilateral somatoparaphrenia after right hemisphere stroke: a case description. Cortex 31, 173–182 (1995).
Coslett, H.B. Evidence for a disturbance of the body schema in neglect. Brain Cogn. 37, 527–544 (1998).
Iacoboni, M. et al. Reafferent copies of imitated actions in the right superior temporal cortex. Proc. Natl. Acad. Sci. USA 98, 13995–13999 (2001).
Jellema, T., Baker, C.I., Wicker, B. & Perrett, D.I. Neural representation for the perception of the intentionality of actions. Brain Cogn. 44, 280–302 (2000).
Perrett, D.I. et al. Frameworks of analysis for the neural representation of animate objects and actions. J. Exp. Biol. 146, 87–113 (1989).
Rizzolatti, G., Fadiga, L., Gallese, V. & Fogassi, L. Premotor cortex and the recognition of motor actions. Brain Res. Cogn. Brain. Res. 3, 131–141 (1996).
Rizzolatti, G., Fogassi, L. & Gallese, V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat. Rev. Neurosci. 2, 661–670 (2001).
Iacoboni, M. et al. Cortical mechanisms of human imitation. Science 286, 2526–2528 (1999).
Galletti, C. et al. The cortical connections of area V6: an occipito-parietal network processing visual information. Eur. J. Neurosci. 13, 1572–1588 (2001).
Astafiev, S.V. et al. Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J. Neurosci. 23, 4689–4699 (2003).
Falchier, A., Clavagnier, S., Barone, P. & Kennedy, H. Anatomical evidence of multimodal integration in primate striate cortex. J. Neurosci. 22, 5749–5759 (2002).
Hikosaka, K., Iwai, E., Saito, H. & Tanaka, K. Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. J. Neurophysiol. 60, 1615–1637 (1988).
Ollinger, J.M., Shulman, G.L. & Corbetta, M. Separating processes within a trial in event-related functional MRI I. The method. Neuroimage 13, 210–217 (2001).
Ollinger, J.M., Corbetta, M. & Shulman, G.L. Separating processes within a trial in event-related functional MRI II. Analysis. Neuroimage 13, 218–229 (2001).
Shulman, G.L. et al. Areas involved in encoding and applying directional expectations to moving objects. J. Neurosci. 19, 9480–9496 (1999).
Ollinger, J.M. & McAvoy, M.P. A homogeneity correction for post-hoc ANOVAs in fMRI. Neuroimage 11, S604 (2000).
Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme Medical, New York, 1988).
Van Essen, D.C. et al. Mapping visual cortex in monkeys and humans using surface-based atlases. Vision Res. 41, 1359–1378 (2001).
Rinaman, W.C., Heil, C., Strauss, M.T., Mascagni, M. & Souza, M. in Standard Mathematical Tables and Formulae (ed. Zwillinger, D.) 569–669 (CRC Press, Boca Raton, 1996).
Acknowledgements
This research was supported by grants from National Institutes of Health (EY00379, EY001248, 5P50NS06833). We thank A. Snyder and M. McAvoy for image analysis and statistical advice; and C. Lewis, T. Phan, F. Miezin and M. Cowan for technical support. We also thank P. Downing and N. Kanwisher for providing the photographs of human body parts and object parts.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Fig. 1
Movement-related BOLD responses in the medial occipital cortex, group-averaged data. The statistical map shows significant differences between right hand Pointing, right Foot pointing, and covert Attention (Experiment 2). Graphs show the group-averaged BOLD timecourses, averaged over target direction (see legend for Fig. 1), from visual and motor regions active in the statistical map. Calc. S/Cu = Calcarine sulcus/Cuneus, LG = lingual gyrus, SMA = supplementary motor area, SII = secondary somatosensory area. Error bars represent s.e.m. (JPG 35 kb)
Supplementary Fig. 2
Pointing vs. Imagery in the EBA (single subjects). Coronal slices on which significant BOLD responses have been superimposed. (a) Pointing with right hand, no visual feedback; (b) Imagining of pointing with right hand; (c) EBA localizer, observation of body parts vs. observation of object parts; (d) EBA voxels with significantly greater activity during pointing than imagery. Graphics show percent signal change response for Pointing (P), Imagery (I), and Saccade (S) tasks vs. fixation baseline in left and right EBA from voxels in (d) (top row), response to body parts (BP) and object parts (OP) vs. fixation baseline from the same voxels in (d) (middle row) and response for Pointing (P) and Imagery (I) tasks vs. fixation baseline in the entire left and right EBA (i.e. from significantly (z = 2.6, P < 0.01 uncorrected) active voxels in EBA localizer) (bottom row). Error bars represent s.e.m. (JPG 75 kb)
Supplementary Fig. 3
Attention-control for movement-related modulation of EBA. (a) Planning activity in EBA for right Hand pointing, Saccade, and Attention tasks. The BOLD response is time-locked to the presentation of a 100 ms foveal arrow cueing one of two peripheral locations followed by a 4.3 second delay. Note similar preparatory response in EBA for pointing and covert attention, and weaker response for planning an eye movement. (b) BOLD response time-locked to the presentation of targets at attended (valid) and unattended (invalid) locations during right hand Pointing (R. hand), right foot pointing (R. foot), and Attention tasks. There is a stronger response during invalid than valid trials, which is effector-independent. Moreover, the response for Pointing and Attention is not significantly different. Error bars represent s.e.m. (GIF 10 kb)
Rights and permissions
About this article
Cite this article
Astafiev, S., Stanley, C., Shulman, G. et al. Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat Neurosci 7, 542–548 (2004). https://doi.org/10.1038/nn1241
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1241
This article is cited by
-
Brain activity associated with quadriceps strength deficits after anterior cruciate ligament reconstruction
Scientific Reports (2023)
-
Visual stimulation by extensive visual media consumption can be beneficial for motor learning
Scientific Reports (2023)
-
Neural interactions in occipitotemporal cortex during basic human movement perception by dynamic causal modeling
Brain Imaging and Behavior (2021)
-
Grasping performance depends upon the richness of hand feedback
Experimental Brain Research (2021)
-
The overlooked ubiquity of first-person experience in the cognitive sciences
Synthese (2021)