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Planning Functional Grasps of Simple Tools Invokes the Hand-independent Praxis Representation Network: An fMRI Study

  • Łukasz Przybylski (a1) and Gregory Króliczak (a1)

Objectives: Neuropsychological and neuroimaging evidence indicates that tool use knowledge and abilities are represented in the praxis representation network (PRN) of the left cerebral hemisphere. We investigated whether PRN would also underlie the planning of function-appropriate grasps of tools, even though such an assumption is inconsistent with some neuropsychological evidence for independent representations of tool grasping and skilled tool use. Methods: Twenty right-handed participants were tested in an event-related functional magnetic resonance imaging (fMRI) study wherein they planned functionally appropriate grasps of tools versus grasps of non-tools matched for size and/or complexity, and later executed the pantomimed grasps of these objects. The dominant right, and non-dominant left hands were used in two different sessions counterbalanced across participants. The tool and non-tool stimuli were presented at three different orientations, some requiring uncomfortable hand rotations for effective grips, with the difficulty matched for both hands. Results: Planning functional grasps of tools (vs. non-tools) was associated with significant asymmetrical increases of activity in the temporo/occipital-parieto-frontal networks. The greater involvement of the left hemisphere PRN was particularly evident when hand movement kinematics (including wrist rotations) for grasping tools and non-tools were matched. The networks engaged in the task for the dominant and non-dominant hand were virtually identical. The differences in neural activity for the two object categories disappeared during grasp execution. Conclusions: The greater hand-independent engagement of the left-hemisphere praxis representation network for planning functional grasps reveals a genuine effect of an early affordance/function-based visual processing of tools. (JINS, 2017, 23, 108–120)

Corresponding author
Correspondence and reprint requests to: Grzegorz Króliczak, Instytut Psychologii UAM, Ul. Szamarzewskiego 89, 60-568 Poznań, Poland. E-mail:
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Beckmann, C.F., Jenkinson, M., & Smith, S.M. (2003). General multilevel linear modeling for group analysis in FMRI. Neuroimage, 20(2), 10521063. doi: 10.1016/S1053-8119(03)00435-X
Begliomini, C., Nelini, C., Caria, A., Grodd, W., & Castiello, U. (2008). Cortical activations in humans grasp-related areas depend on hand used and handedness. PLoS One, 3(10), e3388.
Belardinelli, A., Barabas, M., Himmelbach, M., & Butz, M.V. (2016). Anticipatory eye fixations reveal tool knowledge for tool interaction. Experimental Brain Reseach, 234, 24152431. doi: 10.1007/s00221-016-4646-0
Bidula, S.P., & Kroliczak, G. (2015). Structural asymmetry of the insula is linked to the lateralization of gesture and language. European Journal of Neuroscience, 41(11), 14381447. doi: 10.1111/ejn.12888
Binkofski, F., & Buxbaum, L.J. (2013). Two action systems in the human brain. Brain and Language, 127(2), 222229. doi: 10.1016/j.bandl.2012.07.007
Binkofski, F., Dohle, C., Posse, S., Stephan, K.M., Hefter, H., Seitz, R.J., & Freund, H.J. (1998). Human anterior intraparietal area subserves prehension: A combined lesion and functional MRI activation study. Neurology, 50(5), 12531259. doi: 10.1212/WNL.50.5.1253
Bracci, S., Cavina-Pratesi, C., Ietswaart, M., Caramazza, A., & Peelen, M.V. (2012). Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex. Journal of Neurophysiology, 107(5), 14431456. doi: 10.1152/jn.00619.2011
Brandi, M.L., Wohlschlager, A., Sorg, C., & Hermsdorfer, J. (2014). The neural correlates of planning and executing actual tool use. The Journal of Neuroscience, 34(39), 1318313194. doi: 10.1523/JNEUROSCI.0597-14.2014
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(1), 175185. doi: 10.1016/j.brainres.2006.08.010
Buxbaum, L.J., Shapiro, A.D., & Coslett, H.B. (2014). Critical brain regions for tool-related and imitative actions: A componential analysis. Brain, 137(Pt 7), 19711985. doi: 10.1093/brain/awu111
Castiello, U., & Begliomini, C. (2008). The cortical control of visually guided grasping. Neuroscientist, 14(2), 157170.
Chao, L.L., Weisberg, J., & Martin, A. (2002). Experience-dependent modulation of category-related cortical activity. Cereb Cortex, 12(5), 545551.
Creem-Regehr, S.H., & Lee, J.N. (2005). Neural representations of graspable objects: Are tools special? Brain Research. Cognitive Brain Research, 22(3), 457469.
Culham, J.C., Danckert, S.L., DeSouza, J.F., Gati, J.S., Menon, R.S., & Goodale, M.A. (2003). Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Experimental Brain Research, 153(2), 180189. doi: 10.1007/s00221-003-1591-5
Eklund, A., Nichols, T.E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America, 113(28), 79007905. doi: 10.1073/pnas.1602413113
Ellis, R., & Tucker, M. (2000). Micro-affordance: The potentiation of components of action by seen objects. British Journal of Psychology, 91(Pt 4), 451471.
Elsinger, C.L., Harrington, D.L., & Rao, S.M. (2006). From preparation to online control: Reappraisal of neural circuitry mediating internally generated and externally guided actions. Neuroimage, 31(3), 11771187.
Fabbri, S., Stubbs, K.M., Cusack, R., & Culham, J.C. (2016). Disentangling Representations of Object and Grasp Properties in the Human Brain. The Journal of Neuroscience, 36(29), 76487662. doi: 10.1523/JNEUROSCI.0313-16.2016
Fischl, B. (2012). FreeSurfer. Neuroimage, 62(2), 774781. doi: 10.1016/j.neuroimage.2012.01.021
Frey, S.H. (2007). What puts the how in where? Tool use and the divided visual streams hypothesis. Cortex, 43(3), 368375.
Frey, S.H. (2008). Tool use, communicative gesture and cerebral asymmetries in the modern human brain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363(1499), 19511957. doi: 10.1098/rstb.2008.0008
Frey, S.H., Vinton, D., Norlund, R., & Grafton, S.T. (2005). Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Brain Research. Cognitive Brain Research, 23(2-3), 397405. doi: 10.1016/j.cogbrainres.2004.11.010
Gallivan, J.P., Cavina-Pratesi, C., & Culham, J.C. (2009). Is that within reach? fMRI reveals that the human superior parieto-occipital cortex encodes objects reachable by the hand. Journal of Neuroscience, 29(14), 43814391. doi: 10.1523/JNEUROSCI.0377-09.2009
Gallivan, J.P., & Culham, J.C. (2015). Neural coding within human brain areas involved in actions. Current Opinion in Neurobiology, 33, 141149. doi: 10.1016/j.conb.2015.03.012
Garofeanu, C., Kroliczak, G., Goodale, M.A., & Humphrey, G.K. (2004). Naming and grasping common objects: A priming study. Experimental Brain Research, 159(1), 5564. doi: 10.1007/s00221-004-1932-z
Gibson, J.J. (1977). The theory of affordances. In R. Shaw & J. Bransford (Eds.), Perceiving, acting, and knowing. Toward an ecological psychology (pp. 6782). Hillsdale, NJ: Lawrence Erlbaum Associates.
Gibson, J.J. (1986). The ecological approach to visual perception. Hillsdale, NJ: Lawrence Erlbaum Associates.
Goldenberg, G., Hartmann, K., & Schlott, I. (2003). Defective pantomime of object use in left brain damage: Apraxia or asymbolia? Neuropsychologia, 41(12), 15651573.
Goldenberg, G., & Spatt, J. (2009). The neural basis of tool use. Brain, 132(Pt 6), 16451655. doi: 10.1093/brain/awp080
Goodale, M.A., Gonzalez, C.L., & Kroliczak, G. (2008). Action rules: Why the visual control of reaching and grasping is not always influenced by perceptual illusions. Perception, 37(3), 355366. doi: 10.1068/p5876
Goodale, M.A., Kroliczak, G., & Westwood, D.A. (2005). Dual routes to action: Contributions of the dorsal and ventral streams to adaptive behavior. Progress in Brain Research, 149, 269283. doi: 10.1016/S0079-6123(05)49019-6
Haaland, K.Y., & Harrington, D.L. (1996). Hemispheric asymmetry of movement. Current Opinion in Neurobiology, 6(6), 796800.
Haaland, K.Y., Harrington, D.L., & Knight, R.T. (2000). Neural representations of skilled movement. Brain, 123, 23062313. doi: 10.1093/brain/123.11.2306
Handjaras, G., Bernardi, G., Benuzzi, F., Nichelli, P.F., Pietrini, P., & Ricciardi, E. (2015). A topographical organization for action representation in the human brain. Human Brain Mapping, 36(10), 38323844. doi: 10.1002/hbm.22881
Harrington, D.L., & Haaland, K.Y. (1991). Hemispheric specialization for motor sequencing: Abnormalities in levels of programming. Neuropsychologia, 29(2), 147163.
Harrington, D.L., Rao, S.M., Haaland, K.Y., Bobholz, J.A., Mayer, A.R., Binderx, J.R., & Cox, R.W. (2000). Specialized neural systems underlying representations of sequential movements. Journal of Cognitive Neuroscience, 12(1), 5677.
Hermsdorfer, J., Terlinden, G., Muhlau, M., Goldenberg, G., & Wohlschlager, A.M. (2007). Neural representations of pantomimed and actual tool use: Evidence from an event-related fMRI study. Neuroimage, 36(Suppl 2), T109T118. doi: 10.1016/j.neuroimage.2007.03.037
Ishibashi, R., Pobric, G., Saito, S., & Lambon Ralph, M.A. (2016). The neural network for tool-related cognition: An activation likelihood estimation meta-analysis of 70 neuroimaging contrasts. Cognitive Neuropsychology, 33(3-4), 241256. doi: 10.1080/02643294.2016.1188798
Jacobs, S., Danielmeier, C., & Frey, S.H. (2010). Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool. Journal of Cognitive Neuroscience, 22(11), 25942608. doi: 10.1162/jocn.2009.21372
Jenkinson, M., Beckmann, C.F., Behrens, T.E., Woolrich, M.W., & Smith, S.M. (2012). FSL. Neuroimage, 62(2), 782790. doi: 10.1016/j.neuroimage.2011.09.015
Johnson-Frey, S.H., Newman-Norlund, R., & Grafton, S.T. (2005). A distributed left hemisphere network active during planning of everyday tool use skills. Cerebral Cortex, 15(6), 681695. doi: 10.1093/cercor/bhh169
Kimura, D., & Archibald, Y. (1974). Motor functions of the left hemisphere. Brain, 97(2), 337350. doi: 10.1093/brain/97.1.337
Kourtis, D., & Vingerhoets, G. (2015). Perceiving objects by their function: An EEG study on feature saliency and prehensile affordances. Biological Psychology, 110, 138147.
Kristensen, S., Garcea, F.E., Mahon, B.Z., & Almeida, J. (2016). Temporal Frequency Tuning Reveals Interactions between the Dorsal and Ventral Visual Streams. Journal of Cognitive Neuroscience, 28(9), 12951302. doi: 10.1162/jocn_a_00969
Kroliczak, G., Cavina-Pratesi, C., Goodman, D.A., & Culham, J.C. (2007). What does the brain do when you fake it? An FMRI study of pantomimed and real grasping. Journal of Neurophysiology, 97(3), 24102422. doi: 10.1152/jn.00778.2006
Kroliczak, 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(10), 23962410. doi: 10.1093/cercor/bhn261
Kroliczak, G., McAdam, T.D., Quinlan, D.J., & Culham, J.C. (2008). The human dorsal stream adapts to real actions and 3D shape processing: A functional magnetic resonance imaging study. Journal of Neurophysiology, 100(5), 26272639. doi: 10.1152/jn.01376.2007
Kroliczak, G., Piper, B.J., & Frey, S.H. (2016). Specialization of the left supramarginal gyrus for hand-independent praxis representation is not related to hand dominance. Neuropsychologia. doi: 10.1016/j.neuropsychologia.2016.03.023
Kroliczak, G., Westwood, D.A., & Goodale, M.A. (2006). Differential effects of advance semantic cues on grasping, naming, and manual estimation. Experimental Brain Research, 175(1), 139152. doi: 10.1007/s00221-006-0524-5
Kubiak, A., & Kroliczak, G. (2016). Left extrastriate body area is sensitive to the meaning of symbolic gesture: Evidence from fMRI repetition suppression. Scientific Reports, 6, 31064. doi: 10.1038/srep31064
Li, Y., Randerath, J., Goldenberg, G., & Hermsdorfer, J. (2007). Grip forces isolated from knowledge about object properties following a left parietal lesion. Neuroscience Letters, 426(3), 187191. doi: 10.1016/j.neulet.2007.09.008
Macdonald, S.N., & Culham, J.C. (2015). Do human brain areas involved in visuomotor actions show a preference for real tools over visually similar non-tools? Neuropsychologia, 77, 3541. doi: 10.1016/j.neuropsychologia.2015.08.004
Maki-Marttunen, V., Villarreal, M., & Leiguarda, R.C. (2014). Lateralization of brain activity during motor planning of proximal and distal gestures. Behavioural Brain Research, 272, 226237. doi: 10.1016/j.bbr.2014.06.055
Makoshi, Z., Kroliczak, G., & van Donkelaar, P. (2011). Human supplementary motor area contribution to predictive motor planning. Journal of Motor Behavior, 43(4), 303309. doi: 10.1080/00222895.2011.584085
Marangon, M., Kubiak, A., & Kroliczak, G. (2016). Haptically guided grasping. fMRI shows right-hemisphere parietal stimulus encoding, and bilateral dorso-ventral parietal gradients of object- and action-related processing during grasp execution. Frontiers in Human Neuroscience, 9, 691. doi: 10.3389/fnhum.2015.00691
Michalowski, B., & Kroliczak, G. (2015). Sinistrals are rarely “right”: Evidence from tool-affordance processing in visual half-field paradigms. Frontiers in Human Neuroscience, 9, 166. doi: 10.3389/fnhum.2015.00166
Miezin, F.M., Maccotta, L., Ollinger, J.M., Petersen, S.E., & Buckner, R.L. (2000). Characterizing the hemodynamic response: Effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage, 11(6 Pt 1), 735759. doi: 10.1006/nimg.2000.0568
Mizelle, J.C., Kelly, R.L., & Wheaton, L.A. (2013). Ventral encoding of functional affordances: A neural pathway for identifying errors in action. Brain and Cognition, 82(3), 274282. doi: 10.1016/j.bandc.2013.05.002
Monaco, S., Kroliczak, G., Quinlan, D.J., Fattori, P., Galletti, C., Goodale, M.A., & Culham, J.C. (2010). Contribution of visual and proprioceptive information to the precision of reaching movements. Experimental Brain Research, 202(1), 1532. doi: 10.1007/s00221-009-2106-9
Monaco, S., Sedda, A., Cavina-Pratesi, C., & Culham, J.C. (2015). Neural correlates of object size and object location during grasping actions. European Journal of Neuroscience, 41(4), 454465. doi: 10.1111/ejn.12786
Nichols, T., Brett, M., Andersson, J., Wager, T., & Poline, J.B. (2005). Valid conjunction inference with the minimum statistic. Neuroimage, 25(3), 653660. doi: 10.1016/j.neuroimage.2004.12.005
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97113. doi: 10.1016/0028-3932(71)90067-4
Peeters, R.R., Rizzolatti, G., & Orban, G.A. (2013). Functional properties of the left parietal tool use region. Neuroimage, 78, 8393. doi: 10.1016/j.neuroimage.2013.04.023
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. Quarterly Journal of Experimental Psychology (Hove), 63(11), 21902201. doi: 10.1080/17470218.2010.486903
Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., & Shulman, G.L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676682.
Randerath, J., Goldenberg, G., Spijkers, W., Li, Y., & Hermsdorfer, J. (2010). Different left brain regions are essential for grasping a tool compared with its subsequent use. Neuroimage, 53(1), 171180. doi: 10.1016/j.neuroimage.2010.06.038
Randerath, J., Goldenberg, G., Spijkers, W., Li, Y., & Hermsdorfer, J. (2011). From pantomime to actual use: How affordances can facilitate actual tool-use. Neuropsychologia, 49(9), 24102416. doi: 10.1016/j.neuropsychologia.2011.04.017
Randerath, J., Li, Y., Goldenberg, G., & Hermsdorfer, J. (2009). Grasping tools: Effects of task and apraxia. Neuropsychologia, 47(2), 497505. doi: 10.1016/j.neuropsychologia.2008.10.005
Randerath, J., Valyear, K.F., Hood, A., & Frey, S.H. (2015). Two routes to the same action: An action repetition priming study. Journal of Motor Behavior, 47(2), 142152. doi: 10.1080/00222895.2014.961891
Rao, S.M., Harrington, D.L., Haaland, K.Y., Bobholz, J.A., Cox, R.W., & Binder, J.R. (1997). Distributed neural systems underlying the timing of movements. Journal of Neuroscience, 17(14), 55285535.
Ritterband-Rosenbaum, A., Hermosillo, R., Kroliczak, G., & van Donkelaar, P. (2014). Hand position-dependent modulation of errors in vibrotactile temporal order judgments: The effects of transcranial magnetic stimulation to the human posterior parietal cortex. Experimental Brain Research, 232(6), 16891698. doi: 10.1007/s00221-014-3861-9
Rosenbaum, D.A., Vaughan, J., Barnes, H.J., & Jorgensen, M.J. (1992). Time course of movement planning: Selection of handgrips for object manipulation. Journal of Experimental Psychology: Learning, Memory and Cognition, 18(5), 10581073.
Tarhan, L.Y., Watson, C.E., & Buxbaum, L.J. (2015). Shared and distinct neuroanatomic regions critical for tool-related action production and recognition: evidence from 131 left-hemisphere stroke patients. Journal of Cognitive Neuroscience, 27(12), 24912511. doi: 10.1162/jocn_a_00876
Valyear, K.F., Gallivan, J.P., McLean, D.A., & Culham, J.C. (2012). fMRI repetition suppression for familiar but not arbitrary actions with tools. Journal of Neuroscience, 32(12), 42474259. doi: 10.1523/JNEUROSCI.5270-11.2012
Van Essen, D.C. (2005). A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. Neuroimage, 28(3), 635662. doi: 10.1016/j.neuroimage.2005.06.058
Vannuscorps, G., Dricot, L., & Pillon, A. (2016). Persistent sparing of action conceptual processing in spite of increasing disorders of action production: A case against motor embodiment of action concepts. Cognitive Neuropsychology, 33, 191219. doi: 10.1080/02643294.2016.1186615
Vingerhoets, G. (2008). Knowing about tools: Neural correlates of tool familiarity and experience. Neuroimage, 40(3), 13801391. doi: 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. doi: 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(4), 763777. doi: 10.1002/hbm.21247
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(9), 34263440. doi: 10.1002/hbm.22853
Vingerhoets, G., Nys, J., Honore, P., Vandekerckhove, E., & Vandemaele, P. (2013). Human left ventral premotor cortex mediates matching of hand posture to object use. PLoS One, 8(7), e70480. doi: 10.1371/journal.pone.0070480
Vingerhoets, G., Vandekerckhove, E., Honore, P., Vandemaele, P., & Achten, E. (2011). Neural correlates of pantomiming familiar and unfamiliar tools: Action semantics versus mechanical problem solving? Human Brain Mapping, 32(6), 905918. doi: 10.1002/hbm.21078
Watson, C.E., & Buxbaum, L.J. (2015). A distributed network critical for selecting among tool-directed actions. Cortex, 65, 6582. doi: 10.1016/j.cortex.2015.01.007
Woolrich, M.W., Ripley, B.D., Brady, M., & Smith, S.M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage, 14(6), 13701386. doi: 10.1006/nimg.2001.0931
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