Concurrent Cortical Representations of Function- and Size-Related Object Affordances: An fMRI Study

Springer Science and Business Media LLC - Tập 18 - Trang 1221-1232 - 2018
Dimitrios Kourtis1,2, Pieter Vandemaele3, Guy Vingerhoets2
1Psychology, Faculty of Natural Sciences, University of Stirling, Stirling, UK
2Department of Experimental Psychology, Ghent University, Ghent, Belgium
3Department of Radiology, Ghent University, Ghent, Belgium

Tóm tắt

Previous work has shown that the perception of a graspable object may automatically potentiate actions that are tailored to specific action-related features of the object (e.g., its size) and may be related to its immediate grasping as well as to its long-term, functional use. We investigated the neural correlates of function- and size-related object affordances that may be concurrently potentiated by a graspable object. Participants were lying in a MR scanner holding a large switch in one hand and a small switch in the other hand. They passively attended a large or a small object with clearly separated functional and graspable end that was displayed centrally at an average angle of 45 degrees. Participants responded to the direction of an arrow that was overlaid on the object after a mean period of 1,000 ms after object onset and was pointing to the left or to the right with equal probability. Response times were shorter when the arrow pointed to the functional end of the object and when the responses were made with the switch that was congruent to the size of the perceived object. A clear distinction was found in the representation of function- and size-related affordances; the former was represented in the posterior parietal cortex and the latter in prefrontal, premotor, and primary sensorimotor cortices. We conclude that different aspects of object-directed actions may be automatically potentiated by individual object features and are represented in distinct brain areas.

Tài liệu tham khảo

Aguirre, G.K., Detre, J.A., Alsop, D.C., D'Esposito, M., 1996. The parahippocampus subserves topographical learning in man. Cerebral Cortex 6, 823-829. https://doi.org/10.1093/cercor/6.6.823 Andersen, R.A., Buneo, C.A., 2002. Intentional maps in posterior parietal cortex. Annual Review 25, 189-220. https://doi.org/10.1146/annurev.neuro.25.112701.142922 Anderson, S.J., Yamagishi, N., Karavia, V., 2002. Attentional processes link perception and action. Proceedings of the Biological Sciences 269, 1225-1232. https://doi.org/10.1098/rspb.2002.1998 Ansuini, C., Giosa, L., Turella, L., Altoè, G., Castiello, U., 2008. An object for an action, the same object for other actions: effects on hand shaping. Experimental Brain Research 185, 111-119. https://doi.org/10.1007/s00221-007-1136-4 Binkofski, F., Buccino, G., Posse, S., Seitz, R.J., Rizzolatti, G., Freund, H., 1999. A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. The European Journal of Neuroscience 11, 3276-3286. https://doi.org/10.1046/j.1460-9568.1999.00753.x Binkofski, F., Buxbaum, L.J., 2013. Two action systems in the human brain. Brain and Language 127, 222-229. https://doi.org/10.1016/j.bandl.2012.07.007 Blakemore, S.J., Sirigu, A., 2003. Action prediction in the cerebellum and in the parietal lobe. Experimental Brain Research 153, 239-245. https://doi.org/10.1007/s00221-003-1597-z Borghi, A.M., Riggio, L. 2009. Sentence comprehension and simulation of object temporary, canonical and stable affordances. Brain Research 1253m 117-128. https://doi.org/10.1016/j.brainres.2008.11.064 Borghi, A.M., Riggio, L. 2015. Stable and variable affordances are both automatic and flexible. Frontiers in Human Neuroscience 9, 351. https://doi.org/10.3389/fnhum.2015.00351 Bub, D.N., Masson, M.E., Cree, G.S., 2008. Evocation of functional and volumetric gestural knowledge by objects and words. Cognition 106, 27-58. https://doi.org/10.1016/j.cognition.2006.12.010 Buxbaum, L.J., Kalenine, S., 2010. Action knowledge, visuomotor activation, and embodiment in the two action systems. Annals of the New York Academy of Sciences 1191, 201-218. https://doi.org/10.1111/j.1749-6632.2010.05447.x Buxbaum, L.J., Kyle, K.M., Tang, K., Detre, J.A., 2006. Neural substrates of knowledge of hand postures for object grasping and functional object use: Evidence from fMRI. Brain Research 1117, 175-185. https://doi.org/10.1016/j.brainres.2006.08.010 Castiello, U., Begliomini, C., 2008. The cortical control of casually guided grasping. Neuroscientist 14, 157-170. https://doi.org/10.1177/1073858407312080 Chao, L.L., Haxby, J.V., Martin, A., 1999. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neuroscience 2, 913-919. https://doi.org/10.1038/13217 Chao, L.L., Martin, A., 2000. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478-484. https://doi.org/10.1006/nimg.2000.0635 Cho, S.S., Pellecchia, G., Ko, J.H., Ray, N., Obeso, I., Houle, S., Strafella, A.P., 2012. Effect of continuous theta burst stimulation of the right dorsolateral prefrontal cortex on cerebral blood flow changes during decision making. Brain Stimulation 5, 116-123. https://doi.org/10.1016/j.brs.2012.03.007 Chouinard, P.A., Large, M.E., Chang, E.C., Goodale, M.A., 2009. Dissociable neural mechanisms for determining the perceived heaviness of objects and the predicted weight of objects during lifting: an fMRI investigation of the size-weight illusion. Neuroimage 44, 200-212. https://doi.org/10.1016/j.neuroimage.2008.08.023 Cisek, P., Kalaska, J.F., 2002. Simultaneous encoding of multiple potential reach directions in dorsal premotor cortex. Journal of Neurophysiology 87, 1149-1154. Costantini, M., Ambrosini, E., Tieri, G., Sinigaglia, C., Commiteri, G., 2010. Where does an object trigger an action? An investigation about affordances in space. Experimental Brain Research 207, 95-103. https://doi.org/10.1007/s00221-010-2435-8 Coull, J.T., Frackowiak, R.S., Frith, C.D., 1998. Monitoring for target objects: activation of right frontal and parietal cortices with increasing time on task. Neuropsychologia 36, 1325-1334. https://doi.org/10.1016/S0028-3932(98)00035-9 Creem-Regehr, S.H., Lee, J.N., 2005. Neural representations of graspable objects: are tools special? Brain Research. Cognitive Brain Research 22, 457-469. https://doi.org/10.1016/j.cogbrainres.2004.10.006 Derbyshire, N., Ellis, R., Tucker, M., 2006. The potentiation of two components of the reach-to-grasp action during object categorization in visual memory. Acta Psychologica 122, 74-98. https://doi.org/10.1016/j.actpsy.2005.10.004 Duncan, J., 1984. Selective attention and the organization of visual information. Journal of Experimental Psychology. General 113, 501-517. https://doi.org/10.1037/0096-3445.113.4.501 Ellis, A.W., Burani, C., Izura, C., Bromiley, A., Venneri, A., 2006. Traces of vocabulary acquisition in the brain: Evidence from covert object naming. Neuroimage 33, 958-968. https://doi.org/10.1016/j.neuroimage.2006.07.040 Ellis, R., Tucker, M., 2000. Micro-affordance: the potentiation of components of actions by seen objects. British Journal of Psychology 91, 451-471. https://doi.org/10.1348/000712600161934 Goebel, R., Esposito, F., Formisano, E., 2006. Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single-subject to cortically aligned group general linear model analysis and selforganizing group independent component analysis. Human Brain Mapping 27, 392-401. https://doi.org/10.1002/hbm.20249 Goodale, M.A., Milner, A.D., 1992. Separate visual pathways for perception and action. Trends in Neurosciences 15, 20-25. https://doi.org/10.1016/0166-2236(92)90344-8 Grafton, S.T., 2010. The cognitive neuroscience of prehension: recent development. Experimental Brain Research 204, 475-491. https://doi.org/10.1007/s00221-010-2315-2 Grafton, S.T., Arbib, M.A., Fadiga, L., Rizzolatti, G., 1996. Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination. Experimental Brain Research 112, 103–111. https://doi.org/10.1007/BF00227183 Grafton, S.T., Fagg, A.H., Arbib, M.A., 1998. Dorsal premotor cortex and conditional movement selection: A PET functional mapping study. Journal of Neurophysiology 79,1092-1097. https://doi.org/10.1152/jn.1998.79.2.1092 Grefkes, C., Fink, G.R., 2005. The functional organization of the intraparietal sulcus in humans and monkeys. Journal of Anatomy 207, 3–17. https://doi.org/10.1111/j.1469-7580.2005.00426.x Grèzes, J., Decety, J., 2002. Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia 40, 212-222. https://doi.org/10.1016/S0028-3932(01)00089-6 Grèzes, J., Tucker, M., Armony, J., Ellis, R., Passingham, R.E., 2003. Objects automatically potentiate action: an fMRI study of implicit processing. The European Journal of Neuroscience 17, 2735-2740. https://doi.org/10.1046/j.1460-9568.2003.02695.x Grill-Spector, K., Malach, R., 2004. The human visual cortex. Annual Review of Neuroscience 27, 649-677. https://doi.org/10.1146/annurev.neuro.27.070203.144220 Haaland, K.Y., Harrington, D.L., Knight, R.T., 2000. Neural representation of skilled movement. Brain 123, 2306-2313. https://doi.org/10.1093/brain/123.11.2306 Hoshi, E., Tanji, J., 2004. Differential roles of neuronal activity in the supplementary and presupplementary motor areas: From information retrieval to motor planning and execution. Journal of Neurophysiology 92, 3482-3499. https://doi.org/10.1152/jn.00547.2004 Hou, Y.Y., Liu, T.S., 2012. Neural correlates of object-based attentional selection in human cortex. Neuropsychologia 50, 2916-2925. https://doi.org/10.1016/j.neuropsychologia.2012.08.022 Jax, S.A., Buxbaum, L.J., 2010. Response interference between functional and structural actions linked to the same familiar object. Cognition 115, 350-355. https://doi.org/10.1016/j.cognition.2010.01.004 Jenmalm, P., Schmitz, C., Forssberg, H., Ehrsson, H.H., 2006. Lighter or heavier than predicted: neural correlates of corrective mechanisms during erroneously programmed lifts. The Journal of Neuroscience 26, 9015-9021. https://doi.org/10.1523/JNEUROSCI.5045-05.2006 Johnson-Frey, S.H., 2004. The neural bases of complex tool use in humans. Trends in Cognitive Sciences 8, 71-78. https://doi.org/10.1016/j.tics.2003.12.002 Johnson-Frey, S.H., Newman-Norlund, R., Grafton, S.T., 2005. A distributed left hemisphere network active during planning of everyday tool skills. Cerebral Cortex, 15, 681-695. https://doi.org/10.1093/cercor/bhh169 Jueptner, M., Weiller, C., 1998. A review of differences between basal ganglia and cerebellar control of movement as revealed by functional imaging studies. Brain 121, 1437-1449. https://doi.org/10.1093/brain/121.8.1437 Kourtis, D., Vingerhoets, G., 2015. Perceiving objects by their function: An EEG study on feature saliency and prehensile affordances. Biological Psychology 110, 138-147. https://doi.org/10.1016/j.biopsycho.2015.07.017 Kourtzi, Z., Kanwisher, N., 2001. Representations of perceived object shape by the human lateral occipital cortex. Science 293, 1506-1509. https://doi.org/10.1126/science.1061133 Króliczak, G., Frey, S.H., 2009. A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. Cerebral Cortex 19, 2396-2410. https://doi.org/10.1093/cercor/bhn261 Kuhtz-Buschbeck, J.P., Ehrsson, H.H., Forssberg, H., 2001. Human brain activity in the control of fine static precision grip forces: an fMRI study. The European Journal of Neuroscience 14, 382-390. https://doi.org/10.1046/j.0953-816x.2001.01639.x Lee, J. H., van Donkelaar, P., 2006. The human dorsal premotor cortex generates on-line error corrections during sensorimotor adaptation. The Journal of Neuroscience 26, 3330-3334. https://doi.org/10.1523/JNEUROSCI.3898-05.2006 Lee, K.M., Chang, K.H., Roh, J.K. 1999. Subregions within the supplementary motor area activated at different stages of movement preparation and execution. Neuroimage 9, 117-123. https://doi.org/10.1006/nimg.1998.0393 Lhermitte, F., 1983. Utilization behavior and its relation to the lesions of the frontal lobes. Brain 106, 237-255. https://doi.org/10.1093/brain/106.2.237 Lieberman M.D., Cunningham W.A. ,2009. Type I and type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423–428. https://doi.org/10.1093/scan/nsp052 Makris, S., Grant, S., Hadar, A.A., Yarrow, K., 2013. Binocular vision enhances a rapidly evolving affordance effect: Behavioural and TMS evidence. Brain and Cognition 83, 279-287. https://doi.org/10.1016/j.bandc.2013.09.004 Makris, S., Hadar, A.A., Yarrow, K., 2011. Viewing objects and planning actions: On the potentiation of grasping behaviours by visual objects. Brain and Cognition 77, 257-264. https://doi.org/10.1016/j.bandc.2011.08.002 Mayka, M.A., Corcos, D.M., Leurgans, S.E., Vaillancourt, D.E., 2006. Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis. Neuroimage 31, 1453-1474. https://doi.org/10.1016/j.neuroimage.2006.02.004 Milner, A.D., Goodale, M.A., 1995. The Visual Brain in Action. Oxford University Press. Oxford. Milner, A.D., Goodale, M.A., 2008. Two visual systems re-reviewed. Neuropsychologia 46, 774-785. https://doi.org/10.1016/j.neuropsychologia.2007.10.005 Nachev, P., Wydell, H., O’Neill, K., Husain, M., Kennard, C., 2007. The role of the pre-supplementary motor area in the control of action. Neuroimage 36, T155-Y163. https://doi.org/10.1016/j.neuroimage.2007.03.034 Nitschke, M.F., Kleinschmidt, A., Wessel, K., Frahm, J., 1996. Somatotopic motor representation in the human anterior cerebellum. A high-resolution functional MRI study. Brain 119, 1023-1029. https://doi.org/10.1093/brain/119.3.1023 Oldfield, R.C., 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97-11. https://doi.org/10.1016/0028-3932(71)90067-4 Pellicano, A., Iani, C., Borghi, A.M., Rubichi, S., Nicoletti, R., 2010. Simon-like and functional affordance effects with tools: The effects of object perceptual discrimination and object action state. The Quarterly Journal of Experimental Psychology (Hove) 63, 2190-2201. https://doi.org/10.1080/17470218.2010.486903 Phillips, J.C., Ward, R., 2002. S-R correspondence effects of irrelevant visual affordance: Time course and specificity of response activation. Visual Cognition 9, 540-558. https://doi.org/10.1080/13506280143000575 Randerath, J., Goldenberg, G., Spijkers, W., Li, Y., Hermsdörfer, J., 2010. Different left brain regions are essential for grasping a tool compared with its subsequent use. Neuroimage 53, 171-180. https://doi.org/10.1016/j.neuroimage.2010.06.038 Riggio, L., Iani, C., Gherri, E., Benatti, F., Rubichi, S., Nicoletti, R. 2008. The role of attention in the occurrence of the affordance effect. Acta Psychologica 127, 449-458. https://doi.org/10.1016/j.actpsy.2007.08.008 Rizzolatti, G., Matelli, M., 2003. Two different streams form the dorsal visual system: anatomy and functions. Experimental Brain Research 153, 146-157. https://doi.org/10.1007/s00221-003-1588-0 Rushworth, M.F., Johansen-Berg, H., Gobel, S.M., Devlin, J.T., 2003. The left parietal and premotor cortices: motor attention and selection. Neuroimage 20, S89-100. https://doi.org/10.1016/j.neuroimage.2003.09.011 Sakreida, K., Effnert, I., Thill, S., Menz, M.M., Jirake, D., Eickhofff, C.R., Ziemke, T., Eickhoffgh, S.B., Borghi, A.B., Binkofski, F., 2016. Affordance processing in segregated perieto-frontal dorsal stream sub-pathways. Neuroscience and Biobehavioral Reviews 69, 89-112. https://doi.org/10.1016/j.neubiorev.2016.07.032 Schwarzlose, R.F., Swisher, J.D., Dang, S.B., Kanwisher, N. 2008. The distribution of category and location information across object-selective regions in human visual cortex. Proceedings of the National Academy of Sciences of the United States of America 105, 4447-4452. https://doi.org/10.1073/pnas.0800431105 Stoodley, C.J., Schmahmann, J.D., 2009. Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. Neuroimage 44, 489-501. https://doi.org/10.1016/j.neuroimage.2008.08.039 Striemer, C.L., Chouinard, P.A., Goodale, M.A., 2011. Programs for action in superior parietal cortex: A triple-pulse TMS investigation. Neuropsychologia 49, 2391-2399. https://doi.org/10.1016/j.neuropsychologia.2011.04.015 Symes, E., Ellis, R., Tucker, M., 2007. Visual object affordances: Object orientation. Acta Psychologica 124, 238-255. https://doi.org/10.1016/j.actpsy.2006.03.005 Tipper, S.P., Paul, M.A., Hayes, A.E., 2006. Vision-for-action: The effects of object property discrimination and action state on affordance compatibility effects. Psychonomic Bulletin and Review 13, 493-498. https://doi.org/10.3758/BF03193875 Tucker, M., Ellis, R., 1998. On the relations between seen objects and components of potential actions. Journal of Experimental Psychology. Human Perception and Performance 24, 830-846. https://doi.org/10.1037/0096-1523.24.3.830 Tucker, M., Ellis, R. 2001. The potentiation of grasp types during visual object categorization. Visual Cognition 8, 769-800. https://doi.org/10.1080/13506280042000144 Ungerleider, L.G., Mishkin, M., 1982. Two cortical visual systems, in: Ingle, D.J., Goodale, M.A., Manfield, R.J.W. (Eds.), Analysis of Visual Behavior. MIT Press. Cambridge. Vaesen, K., 2012. The cognitive bases of human tool use. The Behavioral and Brain Sciences 35, 203-218. https://doi.org/10.1017/S0140525X11001452 Vainio, L., Symes, E., Ellis, R., Tucker, M., Ottoboni, G., 2007. On the relations between action planning, object identification, and motor representation of observed actions and objects. Cognition 108, 444-465. https://doi.org/10.1016/j.cognition.2008.03.007 Valyear, K.F., Cavina-Pratesi, C., Stiglick, A.J., Culham, J.C., 2007. Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp? Neuroimage 36, T94-T108. https://doi.org/10.1016/j.neuroimage.2007.03.031 Valyear, K.F., Gallivan, J.P., McLean, D.A., Culham, J.C., 2012. fMRI repetition suppression for familiar but not arbitrary action with tools. The Journal of Neuroscience 32, 4247-4259. https://doi.org/10.1523/JNEUROSCI.5270-11.2012 Vingerhoets, G., 2008. Knowing about tools. Neural correlates of tool familiarity and experience. Neuroimage 40, 1380-1391. https://doi.org/10.1016/j.neuroimage.2007.12.058 Vingerhoets, G., 2014. Contribution of the posterior parietal cortex in reaching, grasping, and using objects and tools. Frontiers in Psychology 5, 151. https://doi.org/10.3389/fpsyg.2014.00151 Vingerhoets, G., Acke, F., Alderweireldt, A.S., Nys, J., Vandemaele, P., Achten, E., 2012. Cerebral lateralization of praxis in right- and left-handedness: Same pattern, different strength. Human Brain Mapping 33, 763-777. https://doi.org/10.1002/hbm.21247 Vingerhoets, G., Acke, F., Vandemaele, P., Achten, E., 2009a. Tool responsive regions in the posterior parietal cortex: Effect of differences in motor goal and target object during imagined transitive movements. Neuroimage 47, 1832-1843. https://doi.org/10.1016/j.neuroimage.2009.05.100 Vingerhoets, G., Clauwaert, A., 2015. Functional connectivity associated with hand shape generation: Imitating novel hand postures and pantomiming tool grips challenge different nodes of a shared neural network. Human Brain Mapping 36, 3426-3440. https://doi.org/10.1002/hbm.22853 Vingerhoets, G., Nys, J., Honore, P., Vanderkerckhove, E., Vandemaele, P., 2013. Human left ventral premotor cortex mediates matching of hand posture to object use. PLoS One 8, e70480. https://doi.org/10.1371/journal.pone.0070480 Vingerhoets, G., Vandamme, K., Vercammen, A., 2009b. Conceptual and physical object qualities contribute differently to motor affordances. Brain and Cognition 69, 481-489. https://doi.org/10.1016/j.bandc.2008.10.003 Vogt, B.A., Vogt, L., Laureys, S., 2006. Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage 29, 452-466. https://doi.org/10.1016/j.neuroimage.2005.07.048 Ward, N.S., Bestmann, S., Hartwigsen, G., Weiss, M.M., Christensen, L.O., Frackowiak, R.S., Rothwell, J.C., Siebner, H.R., 2010. Low-frequency transcranial magnetic stimulation over left dorsal premotor cortex improves the dynamic control of visuospatially cued actions. The Journal of Neuroscience 30, 9216-9223. https://doi.org/10.1523/JNEUROSCI.4499-09.2010 Whatmough, C., Chertkow, H., Murtha, S., Hanratty, K., 2002. Dissociable brain regions process object meaning and object structure during picture naming. Neuropsychologia 40, 174-186. https://doi.org/10.1016/S0028-3932(01)00083-5