[en] Tools are wielded by their handles, but a lot of information about their function comes from their heads (the action-ends). Here we investigated whether eye saccadic movements are primed by tool handles, or whether they are primed by tool heads. We measured human saccadic reaction times while subjects were performing an attentional task. We found that saccades were executed quicker when performed to the side congruent with the tool head, even though "toolness" was irrelevant for the task. Our results show that heads are automatically processed by the visual system to orient eye movements, indicating that eyes are attracted by functional parts of manipulable objects and by the characteristic information these parts convey.
Disciplines :
Neurosciences & behavior
Author, co-author :
Pilacinski, Artur; Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3000-115, Coimbra, Portugal. ap@uc.pt ; CINEICC, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal. ap@uc.pt
de Haan, Stella ; Université de Liège - ULiège > Département de Psychologie > Neuropsychologie ; Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3000-115, Coimbra, Portugal ; CINEICC, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal
Donato, Rita; Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3000-115, Coimbra, Portugal ; CINEICC, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal ; Department of General Psychology, University of Padova, Padova, Italy ; Human Inspired Technology Research Centre, University of Padova, Padova, Italy
Almeida, Jorge; Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3000-115, Coimbra, Portugal ; CINEICC, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal
This work was supported by an ERC starting Grant “ContentMAP” (#802553) to JA. AP was supported by a Foundation for Science and Technology of Portugal and Programa COMPETE Grant (PTDC/PSI-GER/30745/2017). SdH was supported by a Foundation for Science and Technology of Portugal and Programa COMPETE Grant (PTDC/PSI-GER/30757/2017). We want to thank Jon Walbrin for his helpful comments and Francesca Gaiti and Joao Pottes for their help in data collection.
Almeida, J., Fintz, A. & Mahon, B. Tool manipulation knowledge is retrieved by way of the ventral visual object processing pathway. Cortex 49(9), 2334–2344 (2013). DOI: 10.1016/j.cortex.2013.05.004
Goodale, M. A., Milner, A. D., Jakobson, L. S. & Carey, D. P. A neurological dissociation between perceiving objects and grasping them. Nature 349(6305), 154–156. 10.1038/349154a0 (1991). DOI: 10.1038/349154a0
Mahon, B., Kumar, N. & Almeida, J. Spatial frequency tuning reveals visuomotor interactions between the dorsal and ventral visual systems. J. Cogn. Neurosci. 25(6), 862–871 (2013). DOI: 10.1162/jocn_a_00370
Gibson, J. J. The theory of affordances. In Perceiving, Acting, and Knowing: Toward an Ecological Psychology (eds Shaw, R. & Bransford, J.) 67–82 (Lawrence Erlbaum, 1977).
Osiurak, F., Rossetti, Y. & Badets, A. Neuroscience and biobehavioral reviews what is an affordance? 40 years later. Neurosci. Biobehav. Rev. 77(April), 403–417. 10.1016/j.neubiorev.2017.04.014 (2017). DOI: 10.1016/j.neubiorev.2017.04.014
Natraj, N., Pella, Y. M., Borghi, A. M. & Wheaton, L. A. The visual encoding of tool-object affordances. J. Neurosci. 310, 512–527. 10.1016/j.neuroscience.2015.09.060 (2015). DOI: 10.1016/j.neuroscience.2015.09.060
Federico, G. & Brandimonte, M. A. Tool and object affordances: an ecological eye-tracking study. Brain Cogn. 135, 103582 (2019). DOI: 10.1016/j.bandc.2019.103582
Myachykov, A., Ellis, R., Cangelosi, A. & Fischer, M. H. Visual and linguistic cues to graspable objects. Exp. Brain Res. 10.1007/s00221-013-3616-z (2013). DOI: 10.1007/s00221-013-3616-z
Van der Linden, L., Mathôt, S. & Vitu, F. The role of object affordances and center of gravity in eye movements toward isolated daily-life objects. J. Vis. 15(5), 1–18. 10.1167/15.5.8 (2015). DOI: 10.1167/15.5.8
Roberts, K. L. & Humphreys, G. W. Action-related objects influence the distribution of visuospatial attention. Q. J. Exp. Psychol. 64(4), 669–688. 10.1080/17470218.2010.520086 (2011). DOI: 10.1080/17470218.2010.520086
Skiba, R. M. & Snow, J. C. Attentional capture for tool images is driven by the head end of the tool, not the handle. Atten. Percept. Psychophys. 10.3758/s13414-016-1179-3 (2016). DOI: 10.3758/s13414-016-1179-3
Mathôt, S., Schreij, D. & Theeuwes, J. OpenSesame: an open-source, graphical experiment builder for the social sciences. Behav. Res. Methods 44(2), 314–324. 10.3758/s13428-011-0168-7 (2012). DOI: 10.3758/s13428-011-0168-7
Bahill, A. T., Clark, M. R. & Stark, L. The main sequence, a tool for studying human eye movements. Math. Biosci. 24, 191–204 (1975). DOI: 10.1016/0025-5564(75)90075-9
Federico, G. & Brandimonte, M. A. Looking to recognize: The pre-eminence of semantic over sensorimotor processing in human tool use. Sci. Rep. 10, 6157 (2020). DOI: 10.1038/s41598-020-63045-0
Almeida, J. et al. Visual and visuomotor processing of hands and tools as a case study of cross talk between the dorsal and ventral streams. Cogn. Neuropsychol. 24, 1–16 (2018).
Bracci, S., Cavina-Pratesi, C., Ietswaart, M., Caramazza, A. & Peelen, M. V. Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex. J. Neurophysiol. 107(5), 1443–1456. 10.1152/jn.00619.2011 (2012). DOI: 10.1152/jn.00619.2011
Amaral, L., Bergström, F. & Almeida, J. Overlapping but distinct: distal connectivity dissociates hand and tool processing networks. Cortex 140, 1–13. 10.1016/j.cortex.2021.03.011 (2021). DOI: 10.1016/j.cortex.2021.03.011
Tucker, M. & Ellis, R. On the relations between seen objects and components of potential actions. J. Exp. Psychol. Hum. Percept. Perform. 24, 830–846. 10.1037/0096-1523.24.3.830 (1998). DOI: 10.1037/0096-1523.24.3.830
Bartoli, E., Maffongelli, L., Jacono, M. & D’Ausilio, A. Representing tools as hand movements: early and somatotopic visuomotor transformations. Neuropsychologia 10.1016/j.neuropsychologia.2014.06.025 (2014). DOI: 10.1016/j.neuropsychologia.2014.06.025
Squires, S. D., Macdonald, S. N., Culham, J. C. & Snow, J. C. Priming tool actions: are real objects more effective primes than pictures?. Exp. Brain Res. 10.1007/s00221-015-4518-z (2016). DOI: 10.1007/s00221-015-4518-z
Valyear, K. F. et al. To use or to move: goal-set modulates priming when grasping real tools. Exp. Brain Res. 212, 125–142. 10.1007/s00221-011-2705-0 (2011). DOI: 10.1007/s00221-011-2705-0
Kithu, M. C., Saccone, E. J., Crewther, S. G., Goodale, M. A. & Chouinard, P. A. A pantomiming priming study on the grasp and functional use actions of tools. Exp. Brain Res. 10.1007/s00221-019-05581-4 (2019). DOI: 10.1007/s00221-019-05581-4
Massen, C. & Prinz, W. Movements, actions and tool-use actions: an ideomotor approach to imitation. Philos. Trans. R. Soc. B Biol. Sci. 10.1098/rstb.2009.0059 (2009). DOI: 10.1098/rstb.2009.0059
Handy, T. C., Grafton, S. T., Shroff, N. M., Ketay, S. & Gazzaniga, M. S. Graspable objects grab attention when the potential for action is recognized. Nat. Neurosci. 10.1038/nn1031 (2003). DOI: 10.1038/nn1031
Anderson, S. J., Yamagishi, N. & Karavia, V. Attentional processes link perception and action. Proc. R. Soc. Lond. B 269, 1225–1232 (2002). DOI: 10.1098/rspb.2002.1998
Tipper, S. P., Paul, M. A. & Hayes, A. E. Vision-for-action: the effects of object property discrimination and action state on affordance compatibility effects. Psychon. Bull. Rev. 13(3), 493–498. 10.3758/BF03193875 (2006). DOI: 10.3758/BF03193875
Cho, D. T. & Proctor, R. W. The object-based Simon effect: grasping affordance or relative location of the graspable part?. J. Exp. Psychol. Hum. Percept. Perform. 36, 853–861 (2010). DOI: 10.1037/a0019328
Cho, D. T. & Proctor, R. W. Correspondence effects for objects with opposing left and right protrusions. J. Exp. Psychol. Hum. Percept. Perform. 37, 737–749 (2011). DOI: 10.1037/a0021934
Cho, D. T. & Proctor, R. W. Object-based correspondence effects for action-relevant and surface-property judgments with keypress responses: evidence for a basis in spatial coding. Psychol. Res. 77, 618–636 (2013). DOI: 10.1007/s00426-012-0458-4
Pellicano, A. et al. The unimanual handle-to-hand correspondence effect: evidence for a location coding account. Psychol. Res. 83, 1383–1399 (2019). DOI: 10.1007/s00426-018-1009-4
Osiurak, F. & Badets, A. Tool use and affordance: manipulation-based versus reasoning-based approaches. Psychol. Rev. 123, 534–568 (2016). DOI: 10.1037/rev0000027
Azaad, S., Laham, S. M. & Shields, P. A meta-analysis of the object-based compatibility effect. Cognition 190, 105–127 (2019). DOI: 10.1016/j.cognition.2019.04.028
Kostov, K., & Janyan, A. Critical bottom-up attentional factors in the handle orientation effect: asymmetric luminance transients and object-center eccentricity relative to fixation. Psychol. Res. (in press).
Pellicano, A., & Binkofski, F. The prominent role of perceptual salience in object discrimination: over discrimination of graspable side does not activate grasping affordances. Psychol. Res. (in press)
Kristensen, S., Garcea, F. E., Mahon, B. Z. & Almeida, J. Temporal frequency tuning reveals interactions between the dorsal and ventral visual streams. J. Cogn. Neurosci. 28(9), 1295–1302 (2016). DOI: 10.1162/jocn_a_00969
Walbrin, J., & Almeida, J. High-level representations in human occipito-temporal cortex are indexed by distal connectivity. J. Neurosci. JN-RM-2857-20 (2021).
Garcea, F. E. et al. Domain-specific diaschisis: lesions to parietal action areas modulate neural responses to tools in the ventral stream. Cereb. Cortex 29(7), 3168–3181 (2018). DOI: 10.1093/cercor/bhy183
Lee, D., Mahon, B. Z. & Almeida, J. Action at a distance on object-related ventral temporal representations. Cortex 117, 157–167 (2019). DOI: 10.1016/j.cortex.2019.02.018
Almeida, J. et al. Grasping with the eyes: the role of elongation in visual recognition of manipulable objects. Cogn. Affect. Behav. Neurosci. 14(1), 319–335. 10.3758/s13415-013-0208-0 (2014). DOI: 10.3758/s13415-013-0208-0
Almeida, J., Mahon, B. Z. & Caramazza, A. The role of the dorsal visual processing stream in tool identification. Psychol. Sci. 21(6), 772–778 (2010). DOI: 10.1177/0956797610371343
Almeida, J., Mahon, B. Z., Nakayama, K. & Caramazza, A. Unconscious processing dissociates along categorical lines. Proc. Natl. Acad. Sci. USA 105(39), 15214–15218 (2008). DOI: 10.1073/pnas.0805867105
Fang, F. & He, S. Cortical responses to invisible objects in the human dorsal and ventral pathways. Nat. Neurosci. 8(10), 1380–1385 (2005). DOI: 10.1038/nn1537
Cavanagh, P., Hunt, A. R., Afraz, A. & Rolfs, M. Visual stability based on remapping of attention pointers. Trends Cogn. Sci. 14(4), 147–153. 10.1016/j.tics.2010.01.007 (2010). DOI: 10.1016/j.tics.2010.01.007
Garcea, F. E., Kristensen, S., Almeida, J. & Mahon, B. Z. Resilience to the contralateral visual field bias as a window into object representations. Cortex 81, 14–23 (2016). DOI: 10.1016/j.cortex.2016.04.006
Kiefer, M., Sim, E. J., Helbig, H. & Graf, M. 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. 10.1162/jocn.2010.21543 (2011). DOI: 10.1162/jocn.2010.21543
Chen, Q., Garcea, F. E., Almeida, J. & Mahon, B. Z. Connectivity-based constraints on category-specificity in the ventral object processing pathway. Neuropsychologia 105, 184–196 (2017). DOI: 10.1016/j.neuropsychologia.2016.11.014
Ruttorf, M., Kristensen, S., Schad, L. R., & Almeida, J. Transcranial direct current stimulation alters functional network structure in humans: a graph theoretical analysis. IEEE Trans. Med. Imaging (2019).
Fabbri, S., Stubbs, K. M., Cusack, R. & Culham, J. C. Disentangling representations of object and grasp properties in the human brain. J. Neurosci. 10.1523/JNEUROSCI.0313-16.2016 (2016). DOI: 10.1523/JNEUROSCI.0313-16.2016
Posner, M. I., Rafal, R. D., Choate, L. S. & Vaughan, J. Inhibition of return: neural basis and function. Cogn. Neuropsychol. 2, 211–228 (1985). DOI: 10.1080/02643298508252866
Frischen, A. & Tipper, S. P. Orienting attention via observed gaze shift evokes longer term inhibitory effects: implications for social interactions, attention, and memory. J. Exp. Psychol. Gen. 133(4), 516–533. 10.1037/0096-3445.133.4.516 (2004). DOI: 10.1037/0096-3445.133.4.516
