Abstract
Although numerous studies have shown that the sensory-motor system is involved in semantic processing of language stimuli, it is still unclear whether comprehension of abstract concepts is embodied, and whether the involvement of the sensory-motor system is context-dependent. Investigation of how the motor system is activated during comprehension of non-literal action languages can help address these issues. So far several studies have reported brain activations during non-literal action language comprehension, but the findings are highly inconsistent because of different types of non-literal action language stimuli. To clarify how the motor system is involved in comprehension of different types of non-literal languages, the current study conducted quantitative meta-analyses on fMRI findings about comprehension of sentences describing fictive motions, metaphoric actions, and idiomatic actions. Results showed that fictive motion sentences elicited activation in the right parahippocampal gyrus, an area important for spatial processing. For metaphoric actions, the left precentral gyrus (BA 6) was strongly activated, suggesting a link between metaphoric and literal meanings. For idiomatic actions, activity was found in the left inferior frontal gyrus (BA 44/45), highlighting semantic selection and inhibition. No premotor or motor activity was found in idiom condition. These results together suggest that the involvement of the sensory-motor system in abstract concepts processing is flexible, depending on semantic features of the language stimuli and links between abstract and literal meanings.
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Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823–829
Aguirre GK, Zarahn E, D’Esposito M (1998) Neural components of topographical representation. Proc Natl Acad Sci USA 95:839–846
Aziz-Zadeh L, Damasio A (2008) Embodied semantics for actions: findings from functional brain imaging. J Physiol Paris 102:35–39. doi:10.1016/j.jphysparis.2008.03.012
Aziz-Zadeh L, Wilson SM, Rizzolatti G, Iacoboni M (2006) Congruent embodied representations for visually presented actions and linguistic phrases describing actions. Curr Biol 16:1818–1823
Barsalou LW (2008) Grounded cognition. Annu Rev Psychol 59:617–645
Boulenger V, Hauk O, Pulvermüller F (2009) Grasping ideas with the motor system: semantic somatotopy in idiom comprehension. Cereb Cortex 19:1905–1914. doi:10.1093/cercor/bhn217
Boulenger V, Shtyrov Y, Pulvermüller F (2012) When do you grasp the idea? MEG evidence for instantaneous idiom understanding. Neuroimage 59:3502–3513. doi:10.1016/j.neuroimage.2011.11.011
Cacciari C, Bolognini N, Senna I, Pellicciari MC, Miniussi C, Papagno C (2011) Literal, fictive and metaphorical motion sentences preserve the motion component of the verb: a TMS study. Brain Lang 119:149–157. doi:10.1016/j.bandl.2011.05.004
Caramazza A, Anzellotti S, Strnad L, Lingnau A (2014) Embodied cognition and mirror neurons: a critical assessment. Annu Rev Neurosci 37:1–15. doi:10.1146/annurev-neuro-071013-013950
Chatterjee A (2010) Disembodying cognition. Lang Cogn 2:79–116
Chen E, Widick P, Chatterjee A (2008) Functional-anatomical organization of predicate metaphor processing. Brain Lang 107:194–202. doi:10.1016/j.bandl.2008.06.007
de Zubicaray G, Postle N, McMahon K, Meredith M, Ashton R (2010) Mirror neurons, the representation of word meaning, and the foot of the third left frontal convolution. Brain Lang 112:77–84
Desai RH, Binder JR, Conant LL, Mano QR, Seidenberg MS (2011) The neural career of sensory-motor metaphors. J Cogn Neurosci 23:2376–2386. doi:10.1162/jocn.2010.21596
Desai RH, Conant LL, Binder JR, Park H, Seidenberg MS (2013) A piece of the action: modulation of sensory-motor regions by action idioms and metaphors. Neuroimage 83:862–869. doi:10.1016/j.neuroimage.2013.07.044
Eichenbaum H, Lipton PA (2008) Towards a functional organization of the medial temporal lobe memory system: role of the parahippocampal and medial entorhinal cortical areas. Hippocampus 18:1314–1324. doi:10.1002/hipo.20500
Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926. doi:10.1002/hbm.20718
Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601
Evans AC, Kamber M, Collins DL, MacDonald D (1994) An MRI based probabilistic atlas of neuroanatomy. In: Shorvon S, Fish D, Andermann F, Bydder GM (eds) Magnetic resonance scanning and epilepsy. Springer, pp 263–274
Fernandino L, Iacoboni M (2010) Are cortical motor maps based on body parts or coordinated actions? Implications for embodied semantics. Brain Lang 112:44–53
Fogassi L, Luppino G (2005) Motor functions of the parietal lobe. Curr Opin Neurobiol 15:626–631
Gallese V, Lakoff G (2005) The Brain’s concepts: the role of the Sensory-motor system in conceptual knowledge. Cogn Neuropsychol 22:455–479. doi:10.1080/02643290442000310
Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878. doi:10.1006/ning.2001.1037
Harvey M, Rossit S (2012) Visuospatial neglect in action. Neuropsychologia 50:1018–1028. doi:10.1016/j.neuropsychologia.2011.09.030
Hauk O, Tschentscher N (2013) The body of evidence: what can neuroscience tell us about embodied semantics? Front Psychol 4:50. doi:10.3389/fpsyg.2013.00050
Hauk O, Johnsrude I, Pulvermüller F (2004) Somatotopic representation of action words in human motor and premotor cortex. Neuron 41:301–307
Hauk O, Shtyrov Y, Pulvermüller F (2008) The time course of action and action-word comprehension in the human brain as revealed by neurophysiology. J Physiol Paris 102:50–58. doi:10.1016/j.jphysparis.2008.03.013
Hétu S, Grégoire M, Saimpont A, Coll MP, Eugène F, Michon PE, Jackson PL (2013) The neural network of motor imagery: an ALE meta-analysis. Neurosci Biobehav Rev 37(5):930–949. doi:10.1016/j.neubiorev.2013.03.017
Hoenig K, Sim EJ, 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. doi:10.1162/jocn.2008.20123
Hötting K, Holzschneider K, Stenzel A, Wolbers T, Röder B (2013) Effects of a cognitive training on spatial learning and associated functional brain activations. BMC Neurosci 14:73. doi:10.1186/1471-2202-14-73
Kemmerer D, Castillo JG, Talavage T, Patterson S, Wiley C (2008) Neuroanatomical distribution of five semantic components of verbs: evidence from fMRI. Brain Lang 107:16–43
Kiefer M, Pulvermüller F (2012) Conceptual representations in mind and brain: theoretical developments, current evidence and future directions. Cortex 48:805–825. doi:10.1016/j.cortex.2011.04.006
Lacey S, Stilla R, Sathian K (2012) Metaphorically feeling: comprehending textural metaphors activates somatosensory cortex. Brain Lang 120:416–421
Laird AR, Fox PM, Price CJ, Glahn DC, Uecker AM, Lancaster JL, Turkeltaub PE, Kochunov P, Fox PT (2005) ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 25:155–164
Lancaster JL, Tordesillas-Gutiérrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205
Lauro LJR, Mattavelli G, Papagno C, Tettamanti M (2013) She runs, the road runs, my mind runs, bad blood runs between us: literal and figurative motion verbs: an fMRI study. Neuroimage 83:361–371. doi:10.1016/j.neuroimage.2013.06.050
Lauro LJR, Tettamanti M, Cappa SF, Papagno C (2008) Idiom comprehension: a prefrontal task? Cereb Cortex 18:162–170
Mahon BZ, 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. doi:10.1016/j.jphysparis.2008.03.004
Mahon BZ, Caramazza A (2009) Concepts and categories: a cognitive neuropsychological perspective. Annu Rev Psychol 60:27–51. doi:10.1146/annurev.psych.60.110707.163532
Matlock T (2004) Fictive motion as cognitive simulation. Mem Cognit 32:1389–1400
McNorgan C (2012) A meta-analytic review of multisensory imagery identifies the neural correlates of modality-specific and modality-general imagery. Front Hum Neurosci 6:285. doi:10.3389/fnhum.2012.00285
Meteyard L, Cuadrado SR, Bahrami B, Vigliocco G (2012) Coming of age: a review of embodiment and the neuroscience of semantics. Cortex 48:788–804. doi:10.1016/j.cortex.2010.11.002
Mundy ME, Downing PE, Dwyer DM, Honey RC, Graham KS (2013) A critical role for the hippocampus and perirhinal cortex in perceptual learning of scenes and faces: complementary findings from amnesia and FMRI. J Neurosci 33:10490–10502. doi:10.1523/JNEUROSCI.2958-12.2013
Nyffeler T, Gutbrod K, Pflugshaupt T, von Wartburg R, Hess CW, Müri RM (2005) Allocentric and egocentric spatial impairments in a case of topographical disorientation. Cortex 41:133–143
O’Reilly RC (2010) The What and How of prefrontal cortical organization. Trends Neurosci 33:355–361. doi:10.1016/j.tins.2010.05.002
Papeo L, Vallesi A, Isaja A, Rumiati RI (2009) Effects of TMS on different stages of motor and non-motor verb processing in the primary motor cortex. PLoS One 4:e4508. doi:10.1371/journal.pone.0004508
Papeo L, Pascual-Leone A, Caramazza A (2013) Disrupting the brain to validate hypotheses on the neurobiology of language. Front Hum Neurosci 7:148. doi:10.3389/fnhum.2013.00148
Papeo L, Lingnau A, Agosta S, Pascual-Leone A, Battelli L, Caramazza A (2014). The origin of word-related motor activity. Cereb Cortex
Penny W, Holmes A (2006) Random effects analysis. In: Friston K, Ashburner J, Kiebel S, Nichols T, Penny W (eds) Statistical parametric mapping: the analysis of functional brain images. Elsevier, London, pp 156–165
Postle N, McMahon KL, Ashton R, Meredith M, de Zubicaray GI (2008) Action word meaning representations in cytoarchitectonically defined primary and premotor cortices. Neuroimage 43:634–644
Pulvermüller F (2005) Brain mechanisms linking language and action. Nat Rev Neurosci 6:576–582
Pulvermüller F, Fadiga L (2010) Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci 11:351–360. doi:10.1038/nrn2811
Raposo A, Moss HE, Stamatakis EA, Tyler LK (2009) Modulation of motor and premotor cortices by actions, action words and action sentences. Neuropsychologia 47:388–396. doi:10.1016/j.neuropsychologia.2008.09.017
Rapp AM, Mutschler DE, Erb M (2012) Where in the brain is nonliteral language? A coordinate-based meta-analysis of functional magnetic resonance imaging studies. Neuroimage 63:600–610. doi:10.1016/j.neuroimage.2012.06.022
Rüschemeyer SA, Brass M, Friederici AD (2007) Comprehending prehending: neural correlates of processing verbs with motor stems. J Cogn Neurosci 19:855–865
Saygin AP, McCullough S, Alac M, Emmorey K (2010) Modulation of BOLD response in motion-sensitive lateral temporal cortex by real and fictive motion sentences. J Cogn Neurosci 22:2480–2490. doi:10.1162/jocn.2009.21388
Schuil KDI, Smits M, Zwaan RA (2013) Sentential context modulates the involvement of the motor cortex in action language processing: an FMRI study. Front Hum Neurosci 7:100. doi:10.3389/fnhum.2013.00100
Shtyrov Y, Hauk O, Pulvermüller F (2004) Distributed neuronal networks for encoding category-specific semantic information: the mismatch negativity to action words. Eur J Neurosci 19:1083–1092
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York
Talmy L (2000) Toward a cognitive semantics (2 voll). MIT Press, Cambridge
Tettamanti M, Buccino G, Saccuman MC, Gallese V, Danna M, Scifo P, Fazio F, Rizzolatti G, Cappa SF, Perani D (2005) Listening to action-related sentences activates fronto-parietal motor circuits. J Cogn Neurosci 17:273–281
Tomasino B, Rumiati RI (2013) At the mercy of strategies: the role of motor representations in language understanding. Front Psychol 4:27. doi:10.3389/fpsyg.2013.00027
Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 16:765–780
Turken AU, Dronkers NF (2011) The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses. Front Syst Neurosci 5:1
van Dam WO, Rüschemeyer SA, Lindemann O, Bekkering H (2010) Context effects in embodied lexical-semantic processing. Front Psychol 1:150. doi:10.3389/fpsyg.2010.00150
van Elk M, van Schie HT, Bekkering H (2008) Semantics in action: an electrophysiological study on the use of semantic knowledge for action. J Physiol Paris 102:95–100. doi:10.1016/j.jphysparis.2008.03.011
van Elk M, van Schie HT, Zwaan RA, Bekkering H (2010) The functional role of motor activation in language processing: motor cortical oscillations support lexical-semantic retrieval. Neuroimage 50:665–677. doi:10.1016/j.neuroimage.2009.12.123
Wallentin M, Lund TE, Ostergaard S, Ostergaard L, Roepstorff A (2005a) Motion verb sentences activate left posterior middle temporal cortex despite static context. Neuroreport 16:649–652
Wallentin M, Ostergaard S, Lund TE, Ostergaard L, Roepstorff A (2005b) Concrete spatial language: see what I mean? Brain Lang 92:221–233
Watson CE, Cardillo ER, Ianni GR, Chatterjee A (2013) Action concepts in the brain: an activation likelihood estimation meta-analysis. J Cogn Neurosci 25:1191–1205. doi:10.1162/jocn-a-00401
Willems RM, Casasanto D (2011) Flexibility in embodied language understanding. Front Psychol 2(116):2011. doi:10.3389/fpsyg.00116
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Yang, J., Shu, H. Involvement of the Motor System in Comprehension of Non-Literal Action Language: A Meta-Analysis Study. Brain Topogr 29, 94–107 (2016). https://doi.org/10.1007/s10548-015-0427-5
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DOI: https://doi.org/10.1007/s10548-015-0427-5