Abstract
Action representation of manipulable objects has been found to be involved in object recognition. Recently, studies have indicated the existence of two distinct action systems: functional action specifying how to use an object and structural action concerning how to grasp an object. Despite evidence revealing the systems’ anatomical and functional differences, few preceding studies have dissociated their respective roles in object recognition. The present study aimed to tease apart their roles in the recognition of manipulable objects with a priming paradigm. Specifically, we used static stimuli (photos, Experiments 1 and 2) and dynamic stimuli (video clips, Experiments 3 and 4) depicting functional and structural action hand gestures as primes and measured the magnitude of functional and structural action priming effect in object recognition. We found that static and dynamic priming stimuli induced a robust action priming effect only for functional action prime-target pairs. Naming latencies of the target objects were shorter when functional action representations of the prime and target were congruent than when they were incongruent. Moreover, as compared to static priming photos, dynamic priming stimuli induced a larger functional action priming effect. By contrast, neither static nor dynamic priming stimuli elicited a structural action priming effect. Behavioral data from our four experiments provide consistent evidence of the dominant role of functional action representation in the recognition of manipulable objects, suggesting that action knowledge regarding how to use rather than grasp an object is more likely an intrinsic component of objects’ conceptual representation.
Similar content being viewed by others
References
Almeida J, Mahon BZ, Caramazza A (2010) The role of the dorsal visual processing stream in tool identification. Psychol Sci 21(6):772–778
Almeida J, Fintzi AR, Mahon BZ (2013) Tool manipulation knowledge is retrieved by way of the ventral visual object processing pathway. Cortex 49(9):2334–2344
Almeida J, Amaral L, Garcea FE, Aguiar de Sousa D, Xu S, Mahon BZ, Martins IP (2018) Visual and visuomotor processing of hands and tools as a case study of cross talk between the dorsal and ventral streams. Cogn Neuropsychol 35(5–6):288–303
Binkofski F, Buxbaum LJ (2013) Two action systems in the human brain. Brain Lang 127(2):222–229
Borghi AM, Riggio L (2015) Stable and variable affordances are both automatic and flexible. Front Hum Neurosci 9:351–351
Borghi AM, Bonfiglioli C, Lugli L, Ricciardelli P, Rubichi S, Nicoletti R (2005) Visual hand primes and manipulable objects. In: COGSCI2005. XXVII annual conference of the cognitive science society. Lawrence Erlbaum Associates Inc., Mahwah, NJ, pp 322–327
Borghi AM, Bonfiglioli C, Lugli L, Ricciardelli P, Rubichi S, Nicoletti R (2007) Are visual stimuli sufficient to evoke motor information? Studies with hand primes. Neurosci Lett 411(1):17–21
Bub D, Masson M (2006) Gestural knowledge evoked by objects as part of conceptual representations. Aphasiology 20(9):1112–1124
Bub DN, Masson ME (2012) On the dynamics of action representations evoked by names of manipulable objects. J Exp Psychol Gen 141(3):502–517
Bub DN, Masson ME, Cree GS (2008) Evocation of functional and volumetric gestural knowledge by objects and words. Cognition 106(1):27–58
Bub DN, Masson ME, Lin T (2013) Features of planned hand actions influence identification of graspable objects. Psychol Sci 24(7):1269–1276
Buxbaum LJ, Kalénine S (2010) Action knowledge, visuomotor activation, and embodiment in the two action systems. Ann N Y Acad Sci 1191(1):201–218
Campanella F, Shallice T (2011) Manipulability and object recognition: is manipulability a semantic feature? Exp Brain Res 208(3):369–383
Chao LL, Martin A (2000) Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12(4):478–484
Chouinard PA, Goodale MA (2010) Category-specific neural processing for naming pictures of animals and naming pictures of tools: an ALE meta-analysis. Neuropsychologia 48(2):409–418
Cloutman LL (2013) Interaction between dorsal and ventral processing streams: where, when and how? Brain Lang 127(2):251–263
Creem-Regehr SH, Dilda V, Vicchrilli AE, Federer F, Lee JN (2007) The influence of complex action knowledge on representations of novel graspable objects: evidence from functional magnetic resonance imaging. J Int Neuropsychol Soc 13(6):1009–1020
Evans C, Edwards MG, Taylor LJ, Ietswaart M (2016) Perceptual decisions regarding object manipulation are selectively impaired in apraxia or when tDCS is applied over the left IPL. Neuropsychologia 86:153–166
Gerlach C, Law I, Paulson OB (2002) When action turns into words. Activation of motor-based knowledge during categorization of manipulable objects. J Cogn Neurosci 14(8):1230–1239
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25
Grèzes J, Tucker M, Armony J, Ellis R, Passingham RE (2003) Objects automatically potentiate action: an fMRI study of implicit processing. Eur J Neurosci 17(12):2735–2740
Harris IM, Murray AM, Hayward WG, O’callaghan C, Andrews S (2012) Repetition blindness reveals differences between the representations of manipulable and nonmanipulable objects. J Exp Psychol Hum Percept Perform 38(5):1228–1241
Helbig HB, Graf M, Kiefer M (2006) The role of action representations in visual object recognition. Exp Brain Res 174(2):221–228
Helbig HB, Steinwender J, Graf M, Kiefer M (2010) Action observation can prime visual object recognition. Exp Brain Res 200(3–4):251–258
Ishibashi R, Ralph MAL, Saito S, Pobric G (2011) Different roles of lateral anterior temporal lobe and inferior parietal lobule in coding function and manipulation tool knowledge: evidence from an rTMS study. Neuropsychologia 49(5):1128–1135
Jax SA, Buxbaum LJ (2010) Response interference between functional and structural actions linked to the same familiar object. Cognition 115(2):350–355
Jax SA, Buxbaum LJ (2013) Response interference between functional and structural object-related actions is increased in patients with ideomotor apraxia. J Neuropsychol 7(1):12–18
Jeannerod M, Decety J, Michel F (1994) Impairment of grasping movements following a bilateral posterior parietal lesion. Neuropsychologia 32(4):369–380
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(8):1864–1874
Kristensen S, Garcea FE, Mahon BZ, Almeida J (2016) Temporal frequency tuning reveals interactions between the dorsal and ventral visual streams. J Cogn Neurosci 28(9):1295–1302
Lee C, Middleton E, Mirman D, Kalénine S, Buxbaum LJ (2013) Incidental and context-responsive activation of structure-and function-based action features during object identification. J Exp Psychol Hum Percept Perform 39(1):257–270
Lee C, Huang H-W, Federmeier KD, Buxbaum LJ (2018) Sensory and semantic activations evoked by action attributes of manipulable objects: evidence from ERPs. NeuroImage 167:331–341
Mahon BZ, Kumar N, Almeida J (2013) Spatial frequency tuning reveals interactions between the dorsal and ventral visual systems. J Cogn Neurosci 25(6):862–871
Masson ME, Bub DN, Newton-Taylor M (2008) Language-based access to gestural components of conceptual knowledge. Quart J Exp Psychol 61(6):869–882
McNair NA, Harris IM (2012) Disentangling the contributions of grasp and action representations in the recognition of manipulable objects. Exp Brain Res 220(1):71–77
Myung J, Blumstein SE, Sedivy JC (2006) Playing on the typewriter, typing on the piano: Manipulation knowledge of objects. Cognition 98(3):223–243
Osiurak F, Roche K, Ramone J, Chainay H (2013) Handing a tool to someone can take more time than using it. Cognition 128(1):76–81
Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153(2):146–157
Rueschemeyer S-A, van Rooij D, Lindemann O, Willems RM, Bekkering H (2010) The function of words: distinct neural correlates for words denoting differently manipulable objects. J Cogn Neurosci 22(8):1844–1851
Sim EJ, Helbig HB, Graf M, Kiefer M (2014) When action observation facilitates visual perception: activation in visuo-motor areas contributes to object recognition. Cereb Cortex 25(9):2907–2918
Sirigu A, Cohen L, Duhamel J-R, Pillon B, Dubois B, Agid Y (1995) A selective impairment of hand posture for object utilization in apraxia. Cortex 31(1):41–55
Ungerleider LG, Haxby JV (1994) `What’and `where’in the human brain. Curr Opin Neurobiol 4(2):157–165
Vainio L, Symes E, Ellis R, Tucker M, Ottoboni G (2008) On the relations between action planning, object identification, and motor representations of observed actions and objects. Cognition 108(2):444–465
Vingerhoets G (2008) Knowing about tools: neural correlates of tool familiarity and experience. Neuroimage 40(3):1380–1391
Wadsworth HM, Kana RK (2011) Brain mechanisms of perceiving tools and imagining tool use acts: a functional MRI study. Neuropsychologia 49(7):1863–1869
Watson CE, Buxbaum LJ (2014) Uncovering the architecture of action semantics. J Exp Psychol Hum Percept Perform 40(5):1832–1848
Wolk DA, Coslett HB, Glosser G (2005) The role of sensory-motor information in object recognition: evidence from category-specific visual agnosia. Brain Lang 94(2):131–146
Acknowledgements
This research was supported by the grant of the National Natural Science Foundation of China (Grant nos. 61632004 and 61773379) and the grant of the German Research Foundation (DFG) and the National Natural Science Foundation of China in project Crossmodal Learning (NSFC61621136008/DFGTRR-169).
Author information
Authors and Affiliations
Contributions
LN, YL, and WYY designed the experiments. LN collected and analyzed the data. LN, YL, and WYY wrote the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial and non-financial interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ni, L., Liu, Y. & Yu, W. The dominant role of functional action representation in object recognition. Exp Brain Res 237, 363–375 (2019). https://doi.org/10.1007/s00221-018-5426-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-018-5426-9