Abstract
It is an open question whether the motor system is involved during understanding of concrete nouns, as it is for concrete verbs. To clarify this issue, we carried out a behavioral experiment using a go-no go paradigm with an early and delayed go-signal delivery. Italian nouns referring to concrete objects (hand-related or foot-related) and abstract entities served as stimuli. Right-handed participants read the stimuli and responded when the presented word was concrete using the left or right hand. At the early go-signal, slower right-hand responses were found for hand-related nouns compared to foot-related nouns. The opposite pattern was found for the left hand. These findings demonstrate an early lateralized modulation of the motor system during noun processing, most likely crucial for noun comprehension.
Similar content being viewed by others
References
Aziz-Zadeh, L., Iacoboni, M., Zaidel, E., Wilson, S., & Mazziotta, J. (2004). Left hemisphere motor facilitation in response to manual action sounds. Eur J Neurosci, 19, 2609–2612.
Barsalou, L. W. (1999). Perceptual symbol systems. Behav Brain Sci, 22, 577–609.
Baumgaertner, A., Buccino, G., Lange, R., McNamara, A., & Binkofski, F. (2007). Polymodal conceptual processing of human biological actions in the left inferior frontal lobe. Eur J Neurosci, 25, 881–889.
Binder, J. R., Frost, J. A., Hammeke, T. A., Rao, S. M., & Cox, R. W. (1996). Function of the left planum temporale in auditory and linguistic processing. Brain, 119, 1239–1247.
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. Eur J Neurosci, 11, 3276–3286.
Borghi, A. M., & Scorolli, C. (2009). Language comprehension and hand motion simulation. Hum Mov Sci, 28, 12–27.
Boulenger, V., Roy, A. C., Paulignan, Y., Deprez, V., Jeannerod, M., & Nazir, T. A. (2006). Cross-talk between language processes and overt motor behavior in the first 200 msec of processing. J Cogn Neurosci, 18, 1607–1615.
Boulenger, V., Silber, B. Y., Roy, A. C., Paulignan, Y., Jeannerod, M., & Nazir, T. A. (2008). Subliminal display of action words interferes with motor planning: a combined EEG and kinematic study. J Physiol Paris, 102, 130–136.
Broca, P. P. (1861). Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bulletin de la Société Anthropologique, 6, 330–357.
Bub, D. N., Masson, M. E. J., & Cree, G. S. (2008). Evocation of functional and volumetric gestural knowledge by objects and words. Cognition, 106, 27–58.
Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L., Fogassi, L., Gallese, V., et al. (2001). Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci, 13, 400–404.
Buccino, G., Riggio, L., Melli, G., Binkofski, F., Gallese, V., & Rizzolatti, G. (2005). Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. Cogn Brain Res, 24, 355–363.
Buccino, G., Sato, M., Cattaneo, L., Rodà, F., & Riggio, L. (2009). Broken affordances, broken objects: a TMS study. Neuropsychologia, 47, 3074–3078.
Cappa, S. F., Sandrini, M., Rossini, P. M., Sosta, K., & Miniussi, C. (2002). The role of the left frontal lobe in action naming: rTMS evidence. Neurology, 59, 720–723.
Cattaneo, Z., Devlin, J. T., Salvini, F., Vecchi, T., & Silvanto, J. (2010). The causal role of category-specific neuronal representations in the left ventral premotor cortex (PMv) in semantic processing. Neuroimage, 49, 2728–2734.
Chao, L. L., & Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. Neuroimage, 12, 478–484.
Chersi, F., Thill, S., Ziemke, T., & Borghi, A. M. (2010). Sentence processing: linking language to motor chains. Front Neurorob, 4, 1–9.
Clerget, E., Winderickx, A., Fadiga, L., & Olivier, E. (2009). Role of Broca’s area in encoding sequential human actions: a virtual lesion study. Neuroreport, 20, 1496–1499.
Dalla Volta, R., Gianelli, C., Campione, G. C., & Gentilucci, M. (2009). Action word understanding and overt motor behavior. Exp Brain Res, 196, 403–412.
di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp Brain Res, 91, 176–180.
Dominey, P. F., Hoen, M., Blanc, J. M., & Lelekov-Boissard, T. (2003). Neurological basis of language and sequential cognition: evidence from simulation, aphasia, and ERP studies. Brain Language, 86, 207–225.
Fadiga, L., Craighero, L., Buccino, G., & Rizzolatti, G. (2002). Speech listening specifically modulates the excitability of tongue muscles: a TMS study. Eur J Neurosci, 15, 399–402.
Fadiga, L., Craighero, L., & D’Ausilio, A. (2009). Broca’s area in language, action, and music. Ann N Y Acad Sci, 1169, 448–458.
Fazio, P., Cantagallo, A., Craighero, L., D’Ausilio, A., Roy, A. C., Pozzo, T., et al. (2009). Encoding of human action in Broca’s area. Brain, 132, 1980–1988.
Ferrari, P. F., Gallese, V., Rizzolatti, G., & Fogassi, L. (2003). Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci, 17, 1703–1714.
Fischer, M. H., & Zwaan, R. A. (2008). Embodied language: a review of the role of the motor system in language comprehension. Q J Exp Psychol, 61, 825–850.
Fodor, J. A. (1975). The language of thought. Cambridge: Harvard University Press.
Gallese, V. (2003). A neuroscientific grasp of concepts: from control to representation. Biol Sci, 358, 1231–1240.
Gallese, V. (2007). Before and below ‘theory of mind’: embodied simulation and the neural correlates of social cognition. Phil Trans R Soc Lond Biol Sci, 362, 659–669.
Gallese, V. (2008). Mirror neurons and the social nature of language: the neural exploitation hypothesis. Social Neurosci, 3, 317–333.
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593–609.
Gallese, V., & Lakoff, G. (2005). The brain’s concepts: the role of the sensory-motor system in reason and language. Cogn Neuropsychol, 22, 455–479.
Gibson, J. J. (1977). The theory of affordances. In R. Shaw & J. Bransford (Eds.), Perceiving, acting and knowing (pp. 67–82). Hillsdale: Erlbaum.
Gibson, J. J. (1979). The ecological approach to visual perception. Boston: Houghton Mifflin.
Glenberg, A. M. (1997). What memory is for. Behav Brain Sci, 20, 1–19.
Glenberg, A. M., & Kaschak, M. P. (2002). Grounding language in action. Psychon Bull Rev, 9, 558–565.
Glover, S., Rosenbaum, D. A., Graham, J., & Dixon, P. (2004). Grasping the meaning of words. Exp Brain Res, 154, 103–108.
Grèzes, J., Armony, J. L., Rowe, J., & Passingham, R. E. (2003a). Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study. Neuroimage, 18, 928–937.
Grèzes, J., & Decety, J. (2002). Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia, 40, 212–222.
Grèzes, J., Tucker, M., Armony, J., Ellis, R., & Passingham, R. E. (2003b). Objects automatically potentiate action: an fMRI study of implicit processing. Eur J Neurosci, 17, 2735–2740.
Hauk, O., Davis, M. H., Ford, M., Pulvermüller, F., & Marslen-Wilson, W. D. (2006). The time course of visual word recognition as revealed by linear regression analysis of ERP data. Neuroimage, 30, 1383–1400.
Hauk, O., Johnsrude, I., & Pulvermüller, F. (2004). Somatotopic representation of action words in human motor and premotor cortex. Neuron, 41, 301–307.
Hauk, O., & Pulvermüller, F. (2004). Neurophysiological distinction of action words in the fronto-central cortex. Hum Brain Mapping, 21, 191–201.
Hepp-Reymond, M.-C., Husler, E. J., Maier, M. A., & Qi, H.-X. (1994). Force related neuronal activity in two regions of the primate ventral premotor cortex. Can J Physiol Pharmacol, 72, 571–579.
Hoenig, K., Sim, E.-J., Bochev, V., Herrnberger, B., & Kiefer, M. (2008). Conceptual flexibility in the human brain: dynamic recruitment of semantic maps from visual, motor, and motion-related areas. J Cogn Neurosci, 20, 1799–1814.
Jeannerod, M., Arbib, M. A., Rizzolatti, G., & Sakata, H. (1995). Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci, 18, 314–320.
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, 681–695.
Kaschak, M. P., & Borreggine, K. L. (2008). Temporal dynamics of the action-sentence compatibility effect. Q J Exp Psychol, 61, 883–895.
Keysers, C., Kohler, E., Umiltà, M. A., Nanetti, L., Fogassi, L., & Gallese, V. (2003). Audiovisual mirror neurons and action recognition. Exp Brain Res, 153, 628–636.
Knecht, S., Dräger, B., Deppe, M., Bobe, L., Lohmann, H., Flöel, A., et al. (2000). Handedness and hemispheric language dominance in healthy humans. Brain, 123, 2512–2518.
Kohler, E., Keysers, C., Umiltà, M. A., Fogassi, L., Gallese, V., & Rizzolatti, G. (2002). Hearing sounds, understanding actions: action representation in mirror neurons. Science, 297, 846–848.
Kurata, K., & Tanji, J. (1986). Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J Neurosci, 6, 403–411.
Lakoff, G. (1987). Women, fire, and dangerous things: what categories reveal about the mind. Chicago and London: University of Chicago Press.
Laudanna, A., Thornton, A., Brown, G., Burani, C., & Marconi, L. (1995). Un corpus dell’italiano scritto contemporaneo dalla parte del ricevente. In S. Bolasco, L. Lebart, & A. Salem (Eds.), III Giornate internazionali di analisi statistica dei dati testuali Vol. 1 (pp. 103–109). Roma: Cisu.
Lindemann, O., Stenneken, P., van Schie, H. T., & Bekkering, H. (2006). Semantic activation in action planning. J Exp Psychol Hum Percept Perform, 32, 633–643.
Mahon, B. Z., & Caramazza, A. (2005). The orchestration of the sensory-motor systems: clues from neuropsychology. Cogn Neuropsychol, 22, 480–494.
Mahon, B. Z., & Caramazza, A. (2008). A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content. J Physiol Paris, 102, 59–70.
Marino, B.F., Gallese, V., Buccino, G., & Riggio, L (2011). Language sensorimotor specificity modulates the motor system. Cortex. doi:10.1016/j.cortex.2010.12.003.
Martin, A. (2007). The representation of object concepts in the brain. Ann Rev Psychol, 58, 25–45.
Meister, G., Wilson, S. M., Deblieck, C., Wu, A. D., & Iacoboni, M. (2007). The essential role of premotor cortex in speech perception. Curr Biol, 17, 1692–1696.
Möttönen, R., & Watkins, K. E. (2009). Motor representations of articulators contribute to categorical perception of speech sounds. J Neurosci, 29, 9819–9825.
Murata, A., Fadiga, L., Fogassi, L., Gallese, V., Raos, V., & Rizzolatti, G. (1997). Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol, 78, 2226–2230.
Myung, J.-Y., Blumstein, S. E., & Sedivy, J. C. (2006). Playing on the typewriter, typing on the piano: manipulation of knowledge of objects. Cognition, 98, 223–243.
Ojemann, G., Ojemann, J., Lettich, E., & Berger, M. (1989). Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg, 71, 316–326.
Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97–113.
Olivieri, M., Finocchiaro, C., Shapiro, K., Gangitano, M., Caramazza, A., & Pascual-Leone, A. (2004). All talk and no action: a transcranial magnetic stimulation study on motor cortex activation during action word production. J Cogn Neurosci, 16, 374–381.
Papeo, L., Vallesi, A., Isaja, A., & Rumiati, R.I. (2009). Effects of TMS on different stages of motor and non-motor verb-processing in the primary motor cortex. PLoS ONE, doi: 10.1371/journal.pone.0004508.
Postle, N., McMahon, K. L., Ashton, R., Meredith, M., & de Zubicaray, G. I. (2008). Action word meaning representations in cytoarchitectonically defined primary and premotor cortices. Neuroimages, 43, 634–644.
Pulvermüller, F. (1999). Words in the brain’s language. Behav Brain Sci, 22, 253–279.
Pulvermüller, F. (2002). The neuroscience of language. Cambridge: Cambridge University Press.
Pulvermüller, F., & Fadiga, L. (2010). Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci, 11, 351–360.
Pulvermüller, F., Härle, M., & Hummel, F. (2001). Walking or talking? Behavioral and neurophysiological correlates of action verb processing. Brain Language, 78, 143–168.
Pulvermüller, F., Hauk, O., Nikulin, V. V., & Ilmoniemi, R. J. (2005a). Functional links between motor and language systems. Eur J Neurosci, 21, 793–797.
Pulvermüller, F., Lutzenberger, W., & Preissl, H. (1999). Nouns and verbs in intact brain: evidence from event-related potentials and high-frequency cortical responses. Cerebral Cortex, 9, 497–506.
Pulvermüller, F., Shtyrov, Y., & Ilmoniemi, R. (2005b). Brain signatures of meaning access in action word recognition. J Cogn Neurosci, 17, 884–892.
Pylyshyn, Z. (1984). Computation and cognition. Toward a foundation for cognitive science. Cambridge: MIT Press.
Raos, V., Umiltà, M. A., Fogassi, L., & Gallese, V. (2006). Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. J Neurophysiol, 95, 709–729.
Rizzolatti, G., & Arbib, M. A. (1998). Language within our grasp. Trends Neurosci, 21, 188–194.
Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., & Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res, 71, 491–507.
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Cogn Brain Res, 3, 131–141.
Rizzolatti, G., Fogassi, L., & Gallese, V. (2004). Cortical mechanisms subserving object grasping, action understanding and imitation. In M. S. Gazzaniga (Ed.), The new cognitive neurosciences, 3rd Edition, Bradford Book (pp. 427–440). Cambridge: MIT Press.
Rizzolatti, G., Scandolara, C., Gentilucci, M., & Camarda, R. (1981). Response properties and behavioral modulation of “mouth” neurons of the postarcuate cortex (area 6) in macaque monkeys. Brain Res, 225, 421–424.
Sakata, H., Taira, M., Mine, S., & Murata, A. (1992). Hand-movement-related neurons of the posterior parietal cortex of the monkey: their role in the visual guidance of hand movements. In R. Caminiti, P. B. Johnson, & Y. Burnod (Eds.), Control of arm movement in space (pp. 185–198). Berlin: Springer.
Sakreida, K., Schubotz, R. I., Wolfensteller, U., & von Cramon, D. Y. (2005). Motion class dependency in observers’ motor areas revealed by functional magnetic resonance imaging. J Neurosci, 25, 1335–1342.
Sato, M., Mengarelli, M., Riggio, L., Gallese, V., & Buccino, G. (2008). Task related modulation of the motor system during language processing. Brain Language, 105, 83–90.
Scorolli, C., & Borghi, A. M. (2007). Sentence comprehension and action: effector specific modulation of the motor system. Brain Res, 1130, 119–124.
Shapiro, K. A., & Caramazza, A. (2003). The representation of grammatical categories in the brain. Trends Cogn Sci, 7, 201–205.
Shapiro, K. A., Moo, L. R., & Caramazza, A. (2006). Cortical signatures of noun and verb production. PNAS, 103, 1644–1649.
Shapiro, K. A., Pascual-Leone, A., Mottaghy, F. M., Gangitano, M., & Caramazza, A. (2001). Grammatical distinctions in the left frontal cortex. J Cogn Neurosci, 13, 713–720.
Taira, M., Mine, S., Georgopulos, A. P., Murata, A., & Sakata, H. (1990). Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res, 83, 29–36.
Taylor, L. J., & Zwaan, R. A. (2008). Motor resonance and linguistic focus. Q J Exp Psychol, 61, 896–904.
Tettamanti, M., Buccino, G., Saccuman, M. C., Gallese, V., Danna, M., Scifo, P., et al. (2005). Listening to action-related sentences activates fronto-parietal motor circuits. J Cogn Neurosci, 17, 273–281.
Tranel, D., Adolphs, R., Damasio, H., & Damasio, A. R. (2001). A neural basis for the retrieval of words for actions. Cogn Neuropsychol, 18, 655–670.
Tucker, M., & Ellis, R. (2004). Action priming by briefly presented objects. Acta Psychol, 116, 185–203.
Tyler, L. K., Bright, P., Fletcher, P., & Stamatakis, E. A. (2004). Neural processing of nouns and verbs: the role of inflectional morphology. Neuropsychologia, 42, 512–523.
Ulrich, R., & Miller, J. (1994). Effects of truncation on reaction time analysis. J Exp Psychol General, 123, 34–80.
Umiltà, M. A., Brochier, T., Spinks, R. L., & Lemon, R. N. (2007). Simultaneous recording of macaque premotor and primary motor cortex neuronal populations reveals different functional contributions to visuomotor grasp. J Neurophysiol, 98, 488–501.
Vigliocco, G., Vinson, D. P., Druks, J., Barber, H., & Cappa, S. F. (2011). Nouns and verbs in the brain: a review of behavioural, electrophysiological, neuropsychological and imaging studies. Neurosci Biobehav Rev, 35, 407–426.
Watkins, K., & Paus, T. (2004). Modulation of motor excitability during speech perception: the role of Broca’s area. J Cogn Neurosci, 16, 978–987.
Wheaton, K. J., Thompson, J. C., Syngeniotis, A., Abbott, D. F., & Puce, A. (2004). Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. Neuroimage, 22, 277–288.
Wilson, S. M., Saygin, A. P., Sereno, M. I., & Iacoboni, M. (2004). Listening to speech activates motor areas involved in speech production. Nat Neurosci, 7, 701–702.
Zwaan, R. A. (2004). The immersed experiencer: toward an embodied theory of language comprehension. In B. H. Ross (Ed.), The psychology of learning and motivation Vol. 44 (pp. 35–62). New York: Academic Press.
Zwaan, R. A., & Taylor, L. J. (2006). Seeing, acting, understanding: motor resonance in language comprehension. J Exp Psychol General, 135, 1–11.
Acknowledgments
This study was supported by the European Community Grant ICT-216125-ROSSI and by MIUR (Ministero Italiano dell’Università e della Ricerca).
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
See Table 1.
Rights and permissions
About this article
Cite this article
Marino, B.F.M., Gough, P.M., Gallese, V. et al. How the motor system handles nouns: a behavioral study. Psychological Research 77, 64–73 (2013). https://doi.org/10.1007/s00426-011-0371-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00426-011-0371-2