Abstract
Humans are faster to grasp an object such as a tool if they have previewed the same object beforehand. This priming effect is strongest when actors gesture the use of the tool rather than simply move it, possibly because the previewed tool activates action-specific routines in dorsal-stream motor networks. Here, we examined whether real tools, which observers could physically act upon, serve as more potent primes than two-dimensional images of tools, which do not afford physical action. Participants were presented with a prime stimulus that could be either a real tool or a visually matched photograph of a tool. After a brief delay, participants interacted with a real tool target, either by ‘grasping to move,’ or ‘grasping to use’ it. The identities of the prime and target tools were either the same (congruent trials; e.g., spatula–spatula) or different (incongruent trials; e.g., whisk–spatula). As expected, participants were faster to initiate grasps during trials when they had to move the tool rather than gesture its use. Priming effects were observed for grasp-to-use, but not grasp-to-move, responses. Surprisingly, however, both pictures of tools and real tools primed action responses equally. Our results indicate that tool priming effects are driven by pictorial cues and their implied actions, even in the absence of volumetric cues that reflect the tangibility and affordances of the prime.
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References
Adamo M, Ferber S (2009) A picture says more than a thousand words: behavioural and ERP evidence for attentional enhancements due to action affordances. Neuropsychologia 47:1600–1608. doi:10.1016/j.neuropsychologia.2008.07.009
Binkofski F, Buxbaum LJ (2013) Two action systems in the human brain. Brain Lang 127:222–229. doi:10.1016/j.bandl.2012.07.007
Binkofski F, Buccino G, Stephan KM et al (1999) A parieto-premotor network for object manipulation: evidence from neuroimaging. Exp Brain Res 128:210–213. doi:10.1007/s002210050838
Blake R, Wilson H (2011) Binocular vision. Vision Res 51:754–770. doi:10.1016/j.visres.2010.10.009
Bub DN, Masson MEJ (2006) Gestural knowledge evoked by objects as part of conceptual representations. Aphasiology 20:1112–1124. doi:10.1080/02687030600741667
Bub DN, Masson MEJ, Cree GS (2008) Evocation of functional and volumetric gestural knowledge by objects and words. Cognition 106:27–58. doi:10.1016/j.cognition.2006.12.010
Buccino G, Sato M, Cattaneo L et al (2009) Broken affordances, broken objects: a TMS study. Neuropsychologia 47:3074–3078. doi:10.1016/j.neuropsychologia.2009.07.003
Buckingham G, Cant JS, Goodale MA (2009) Living in a material world: how visual cues to material properties affect the way that we lift objects and perceive their weight. J Neurophysiol 102:3111–3118. doi:10.1152/jn.00515.2009
Buckingham G, Ranger NS, Goodale MA (2011) The material–weight illusion induced by expectations alone. Atten Percept Psychophys 73:36–41. doi:10.3758/s13414-010-0007-4
Bushong B, King LM, Camerer CF, Rangel A (2010) Pavlovian processes in consumer choice: the physical presence of a good increases willingness-to-pay. Am Econ Rev 100:1556–1571. doi:10.1257/aer.100.4.1556
Cant JS, Goodale MA (2011) Scratching beneath the surface: new insights into the functional properties of the lateral occipital area and parahippocampal place area. J Neurosci 31:8248–8258. doi:10.1523/JNEUROSCI.6113-10.2011
Cant JS, Westwood DA, Valyear KF, Goodale MA (2005) No evidence for visuomotor priming in a visually guided action task. Neuropsychologia 43:216–226. doi:10.1016/j.neuropsychologia.2004.11.008
Carr TH, McCauley C, Sperber RD (1982) Words, pictures, and priming: on semantic activation, conscious identification, and the automaticity of information processing. Am Psychol Assoc 8:757–777. doi:10.1037/0096-1523.8.6.757
Castiello U (1998) Attentional coding for three-dimensional objects and two-dimensional shapes. Differential interference effects. Exp Brain Res 123:289–297. doi:10.1007/s002210050571
Castiello U (2001) The effects of abrupt onset of 2-D and 3-D distractors on prehension movements. Percept Psychophys 63:1014–1025. doi:10.3758/BF03194520
Chainay H, Humphreys GW (2002) Privileged access to action for objects relative to words. Psychon Bull Rev 9:348–355. doi:10.3758/BF03196292
Chainay H, Naouri L, Pavec A (2011) Orientation priming of grasping decision for drawings of objects and blocks, and words. Mem Cognit 39:614–624. doi:10.3758/s13421-010-0049-9
Chainay H, Brüers S, Martin H, Osiurak F (2014) Transport and use of common objects: influence of weight on action planning. Vis cogn 22:1154–1172. doi:10.1080/13506285.2014.975883
Chao LL, Martin A (2000) Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12:478–484. doi:10.1006/nimg.2000.0635
Choi SH, Na DL, Kang E et al (2001) Functional magnetic resonance imaging during pantomiming tool-use gestures. Exp Brain Res 139:311–317. doi:10.1007/s002210100777
Craighero L, Fadiga L, Umiltà CA, Rizzolatti G (1996) Evidence for visuomotor priming effect. Neuroreport 8:347–349. doi:10.1097/00001756-199612200-00068
Culham JC, Danckert SL, DeSouza JFX et al (2003) Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153:180–189. doi:10.1007/s00221-003-1591-5
DeLoache JS, Pierroutsakos SL, Uttal DH et al (1998) Grasping the nature of pictures. Psychol Sci 9:205–210. doi:10.1111/1467-9280.00039
Eastough D, Edwards MG (2007) Movement kinematics in prehension are affected by grasping objects of different mass. Exp Brain Res 176:193–198. doi:10.1007/s00221-006-0749-3
Frey SH (2007) What puts the how in where? Tool use and the divided visual streams hypothesis. Cortex 43:368–375. doi:10.1016/S0010-9452(08)70462-3
Fridman EA, Immisch I, Hanakawa T et al (2006) The role of the dorsal stream for gesture production. Neuroimage 29:417–428. doi:10.1016/j.neuroimage.2005.07.026
Gallivan JP, Cavina-Pratesi C, Culham JC (2009) Is that within reach? fMRI reveals that the human superior parieto-occipital cortex encodes objects reachable by the hand. J Neurosci 29:4381–4391. doi:10.1523/JNEUROSCI.0377-09.2009
Gallivan JP, Cant JS, Goodale MA, Flanagan JR (2014) Representation of object weight in human ventral visual cortex. Curr Biol 24:1866–1873. doi:10.1016/j.cub.2014.06.046
Gibson JJ (1979) The ecological approach to visual. Perception. doi:10.2307/989638
Glover S, Rosenbaum DA, Graham J, Dixon P (2004) Grasping the meaning of words. Exp Brain Res 154:103–108. doi:10.1007/s00221-003-1659-2
Goldenberg G, Hentze S, Hermsdörfer J (2004) The effect of tactile feedback on pantomime of tool use in apraxia. Neurology 63:1863–1867. doi:10.1212/01.WNL.0000144283.38174.07
Goodale MA, Jakobson LS, Keillor JM (1994) Differences in the visual control of pantomimed and natural grasping movements. Neuropsychologia 32:1159–1178. doi:10.1016/0028-3932(94)90100-7
Grèzes J, Decety J (2002) Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia 40:212–222. doi:10.1016/S0028-3932(01)00089-6
Grèzes J, Tucker M, Armony J et al (2003) Objects automatically potentiate action: An fMRI study of implicit processing. Eur J Neurosci 17:2735–2740. doi:10.1046/j.1460-9568.2003.02695.x
Handy TC, Grafton ST, Shroff NM et al (2003) Graspable objects grab attention when the potential for action is recognized. Nat Neurosci 6:421–427. doi:10.1038/nn1031
Helbig HB, Graf M, Kiefer M (2006) The role of action representations in visual object recognition. Exp Brain Res 174:221–228. doi:10.1007/s00221-006-0443-5
Hermsdörfer J, Li Y, Randerath J et al (2011) Anticipatory scaling of grip forces when lifting objects of everyday life. Exp Brain Res 212:19–31. doi:10.1007/s00221-011-2695-y
Holmes SA, Heath M (2013) Goal-directed grasping: the dimensional properties of an object influence the nature of the visual information mediating aperture shaping. Brain Cogn 82:18–24. doi:10.1016/j.bandc.2013.02.005
Hunt JL, Nickel BG, Gigault C (2000) Anamorphic images. Am J Phys 68:232. doi:10.1119/1.19406
James TW, Humphrey GK, Gati JS et al (2002) Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron 35:793–801. doi:10.1016/S0896-6273(02)00803-6
Janczyk M, Pfister R, Crognale MA, Kunde W (2012) Effective rotations: action effects determine the interplay of mental and manual rotations. J Exp Psychol Gen 141:489–501. doi:10.1037/a0026997
Jax SA, Buxbaum LJ (2010) Response interference between functional and structural actions linked to the same familiar object. Cognition 115:350–355. doi:10.1016/j.cognition.2010.01.004
Johnson-Frey SH, McCarty M, Keen R (2004) Reaching beyond spatial perception: effects of intended future actions on visually guided prehension. Vis Cogn 11:371–399. doi:10.1080/13506280344000329
Johnson-Frey SH, Newman-Norlund R, Grafton ST (2005) A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex 15:681–695. doi:10.1093/cercor/bhh169
Kellenbach ML, Brett M, Patterson K (2003) Actions speak louder than functions: the importance of manipulability and action in tool representation. J Cogn Neurosci 15:30–46. doi:10.1162/089892903321107800
Kiefer M, Sim E-J, Helbig H, Graf M (2011) Tracking the time course of action priming on object recognition: evidence for fast and slow influences of action on perception. J Cogn Neurosci 23:1864–1874. doi:10.1162/jocn.2010.21543
Konen CS, Mruczek REB, Montoya JL, Kastner S (2013) Functional organization of human posterior parietal cortex: grasping- and reaching-related activations relative to topographically organized cortex. J Neurophysiol 109:2897–2908. doi:10.1152/jn.00657.2012
Kunde W, Pfister R, Janczyk M (2012) The locus of tool-transformation costs. J Exp Psychol Hum Percept Perform 38:703–714. doi:10.1037/a0026315
Lewis JW (2006) Cortical networks related to human use of tools. Neuroscience 12:211–231. doi:10.1177/1073858406288327
Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769. doi:10.1146/annurev.physiol.66.082602.092845
Makris S, Hadar AA, Yarrow K (2011) Viewing objects and planning actions: on the potentiation of grasping behaviours by visual objects. Brain Cogn 77:257–264. doi:10.1016/j.bandc.2011.08.002
Makris S, Hadar AA, Yarrow K (2013) Are object affordances fully automatic? A case of covert attention. Behav Neurosci 127:797–802. doi:10.1037/a0033946
Marr D (1982) Vision: a computational investigation into the human representation and processing of visual information. Freeman, San Francisco
Martin A, Wiggs CL, Ungerleider LG, Haxby JV (1996) Neural correlates of category-specific knowledge. Nature 379:649–652. doi:10.1038/379649a0
Masson MEJ, Bub DN, Breuer AT (2011) Priming of reach and grasp actions by handled objects. J Exp Psychol Hum Percept Perform 37:1688. doi:10.1037/a0026023
Myachykov A, Ellis R, Cangelosi A, Fischer MH (2013) Visual and linguistic cues to graspable objects. Exp Brain Res 229:545–559. doi:10.1007/s00221-013-3616-z
Osiurak F, Roche K, Ramone J, Chainay H (2013) Handing a tool to someone can take more time than using it. Cognition 128:76–81. doi:10.1016/j.cognition.2013.03.005
Peeters R, Simone L, Nelissen K et al (2009) The representation of tool use in humans and monkeys: common and uniquely human features. J Neurosci 29:11523–11539. doi:10.1523/JNEUROSCI.2040-09.2009
Randerath J, Martin KR, Frey SH (2013) Are tool properties always processed automatically? The role of tool use context and task complexity. Cortex 49:1679–1693. doi:10.1016/j.cortex.2012.08.016
Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153:146–157. doi:10.1007/s00221-003-1588-0
Rosenbaum DA, Vaughan J, Barnes HJ, Jorgensen MJ (1992) Time course of movement planning: selection of handgrips for object manipulation. J Exp Psychol Learn Mem Cogn 18:1058–1073. doi:10.1037/0278-7393.18.5.1058
Schacter DL, Wig GS, Stevens WD (2007) Reductions in cortical activity during priming. Curr Opin Neurobiol 17:171–176. doi:10.1016/j.conb.2007.02.001
Snow JC, Pettypiece CE, McAdam TD et al (2011) Bringing the real world into the fMRI scanner: repetition effects for pictures versus real objects. Sci Rep 1:130. doi:10.1038/srep00130
Snow JC, Skiba RM, Coleman TL, Berryhill ME (2014) Real-world objects are more memorable than photographs of objects. Front Hum Neurosci 8:837. doi:10.3389/fnhum.2014.00837
Tucker M, Ellis R (1998) On the relations between seen objects and components of potential actions. J Exp Psychol Hum Percept Perform 24:830–846. doi:10.1037/0096-1523.24.3.830
Tucker M, Ellis R (2001) The potentiation of grasp types during visual object categorization. Vis Cogn 8:769–800. doi:10.1080/13506280042000144
Tucker M, Ellis R (2004) Action priming by briefly presented objects. Acta Psychol (Amst) 116:185–203. doi:10.1016/j.actpsy.2004.01.004
Valyear KF, Culham JC, Sharif N et al (2006) A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: a human fMRI study. Neuropsychologia 44:218–228. doi:10.1016/j.neuropsychologia.2005.05.004
Valyear KF, Chapman CS, Gallivan JP et al (2011) To use or to move: Goal-set modulates priming when grasping real tools. Exp Brain Res 212:125–142. doi:10.1007/s00221-011-2705-0
Valyear KF, Gallivan JP, McLean AD, Culham JC (2012) fMRI repetition suppression for familiar but not arbitrary actions with tools. J Neurosci 32:4247–4259. doi:10.1523/JNEUROSCI.5270-11.2012
Westwood DA, Danckert J, Servos P, Goodale MA (2002) Grasping two-dimensional images and three-dimensional objects in visual-form agnosia. Exp Brain Res 144:262–267. doi:10.1007/s00221-002-1068-y
Wilf M, Holmes NP, Schwartz I, Makin TR (2013) Dissociating between object affordances and spatial compatibility effects using early response components. Front Psychol 4:591. doi:10.3389/fpsyg.2013.00591
Yoon EY, Humphreys GW (2007) Dissociative effects of viewpoint and semantic priming on action and semantic decisions: evidence for dual routes to action from vision. Q J Exp Psychol 60:601–623. doi:10.1080/17470210600701007
Yu AB, Abrams RA, Zacks JM (2014) Limits on action priming by pictures of objects. J Exp Psychol Hum Percept Perform 40:1861–1873. doi:10.1037/a0037397
Acknowledgments
This work was funded by a Discovery Grant and Discovery Accelerator Supplement from the Natural Sciences and Engineering Research Council (NSERC) of Canada (249877-2006-RGPIN) to J.C.C., an Ontario Graduate Scholarship to S.M., and an Undergraduate Student Research Award from NSERC to S.S. We thank Kevin Stubbs, Derek Quinlan, and Joey Paciocco for technical assistance.
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Squires, S.D., Macdonald, S.N., Culham, J.C. et al. Priming tool actions: Are real objects more effective primes than pictures?. Exp Brain Res 234, 963–976 (2016). https://doi.org/10.1007/s00221-015-4518-z
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DOI: https://doi.org/10.1007/s00221-015-4518-z