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Brain mechanisms linking language and action

Nature Reviews Neurosciencevolume 6pages576582 (2005) | Download Citation

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Abstract

For a long time the cortical systems for language and actions were believed to be independent modules. However, as these systems are reciprocally connected with each other, information about language and actions might interact in distributed neuronal assemblies. A critical case is that of action words that are semantically related to different parts of the body (for example, 'lick', 'pick' and 'kick'): does the comprehension of these words specifically, rapidly and automatically activate the motor system in a somatotopic manner, and does their comprehension rely on activity in the action system?

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References

  1. 1

    Fodor, J. A. The Modularity of Mind (MIT Press, Cambridge, Massachusetts, USA, 1983).

  2. 2

    Shallice, T. From Neuropsychology to Mental Structure (Cambridge Univ. Press, New York, USA, 1988).

  3. 3

    Lichtheim, L. On aphasia. Brain 7, 433–484 (1885).

  4. 4

    Price, C. J. The anatomy of language: contributions from functional neuroimaging. J. Anat. 197, 335–359 (2000).

  5. 5

    Hebb, D. O. The Organization of Behavior. A Neuropsychological Theory (John Wiley, New York, USA, 1949).

  6. 6

    Palm, G. Neural Assemblies (Springer, Berlin, Germany, 1982).

  7. 7

    Roland, P. E. & Gulyas, B. Visual imagery and visual representation. Trends Neurosci. 17, 281–287; discussion 287–294, 514–516 (1994).

  8. 8

    Braitenberg, V. & Schüz, A. Cortex: Statistics and Geometry of Neuronal Connectivity (Springer, Berlin, Germany, 1998).

  9. 9

    Mesulam, M. M. From sensation to cognition. Brain 121, 1013–1052 (1998).

  10. 10

    Fuster, J. M. Cortex and Mind: Unifying Cognition (Oxford Univ. Press, Oxford, UK, 2003).

  11. 11

    Makris, N. et al. MRI-based topographic parcellation of human cerebral white matter and nuclei II. Rationale and applications with systematics of cerebral connectivity. Neuroimage 9, 18–45 (1999).

  12. 12

    Pandya, D. N. & Yeterian, E. H. in Cerebral Cortex. Vol. 4 (eds Peters, A. & Jones, E. G.) 3–61 (Plenum, London, UK, 1985).

  13. 13

    Romanski, L. M. et al. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nature Neurosci. 2, 1131–1136 (1999).

  14. 14

    Rizzolatti, G. & Luppino, G. The cortical motor system. Neuron 31, 889–901 (2001).

  15. 15

    Young, M. P., Scannell, J. W., Burns, G. & Blakemore, C. Analysis of connectivity: neural systems in the cerebral cortex. Rev. Neurosci. 5, 227–249 (1994).

  16. 16

    Gardner, H. & Zurif, E. Bee but not Be: oral reading of single words in aphasia and alexia. Neuropsychologia 13, 181–190 (1975).

  17. 17

    Miceli, G., Silveri, M., Villa, G. & Caramazza, A. On the basis of agrammatics' difficulty in producing main verbs. Cortex 20, 207–220 (1984).

  18. 18

    Daniele, A., Giustolisi, L., Silveri, M. C., Colosimo, C. & Gainotti, G. Evidence for a possible neuroanatomical basis for lexical processing of nouns and verbs. Neuropsychologia 32, 1325–1341 (1994).

  19. 19

    Warrington, E. K. & McCarthy, R. A. Categories of knowledge: further fractionations and an attempted integration. Brain 110, 1273–1296 (1987).

  20. 20

    Pulvermüller, F. Words in the brain's language. Behav. Brain Sci. 22, 253–336 (1999).

  21. 21

    Plaut, D. C. & Shallice, T. Deep dyslexia: a case study of connectionist neuropsychology. Cogn. Neuropsychol. 10, 377–500 (1993).

  22. 22

    Pulvermüller, F. & Preissl, H. A cell assembly model of language. Network Comput. Neural Syst. 2, 455–468 (1991).

  23. 23

    Kiefer, M. & Spitzer, M. The limits of a distributed account of conceptual knowledge. Trends Cogn. Sci. 5, 469–471 (2001).

  24. 24

    Humphreys, G. W. & Forde, E. M. Hierarchies, similarity, and interactivity in object recognition: 'category-specific' neuropsychological deficits. Behav. Brain Sci. 24, 453–509 (2001).

  25. 25

    Zatorre, R. J., Evans, A. C., Meyer, E. & Gjedde, A. Lateralization of phonetic and pitch discrimination in speech processing. Science 256, 846–849 (1992).

  26. 26

    Pulvermüller, F., Shtyrov, Y. & Ilmoniemi, R. J. Spatio-temporal patterns of neural language processing: an MEG study using minimum-norm current estimates. Neuroimage 20, 1020–1025 (2003).

  27. 27

    Wilson, S. M., Saygin, A. P., Sereno, M. I. & Iacoboni, M. Listening to speech activates motor areas involved in speech production. Nature Neurosci. 7, 701–702 (2004).

  28. 28

    Paus, T., Perry, D. W., Zatorre, R. J., Worsley, K. J. & Evans, A. C. Modulation of cerebral blood flow in the human auditory cortex during speech: role of motor-to-sensory discharges. Eur. J. Neurosci. 8, 2236–2246 (1996).

  29. 29

    Liberman, A. M., Cooper, F. S., Shankweiler, D. P. & Studdert-Kennedy, M. Perception of the speech code. Psychol. Rev. 74, 431–461 (1967).

  30. 30

    Liberman, A. M. & Whalen, D. H. On the relation of speech to language. Trends Cogn. Sci. 4, 187–196 (2000).

  31. 31

    Fowler, C. A. An event approach to the study of speech perception from a direct realist perspective. J. Phonetics 14, 3–28 (1987).

  32. 32

    Fowler, C. A., Brown, J. M., Sabadini, L. & Weihing, J. Rapid access to speech gestures in perception: evidence from choice and simple response time tasks. J. Mem. Lang. 49, 396–413 (2003).

  33. 33

    Fadiga, L., Craighero, L., Buccino, G. & Rizzolatti, G. Speech listening specifically modulates the excitability of tongue muscles: a TMS study. Eur. J. Neurosci. 15, 399–402 (2002).

  34. 34

    Horwitz, B. & Braun, A. R. Brain network interactions in auditory, visual and linguistic processing. Brain Lang. 89, 377–384 (2004).

  35. 35

    Rizzolatti, G. & Craighero, L. The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192 (2004).

  36. 36

    Penfield, W. & Rasmussen, T. The Cerebral Cortex of Man (Macmillan, New York, USA, 1950).

  37. 37

    He, S. Q., Dum, R. P. & Strick, P. L. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J. Neurosci. 13, 952–980 (1993).

  38. 38

    Matelli, M., Camarda, R., Glickstein, M. & Rizzolatti, G. Afferent and efferent projections of the inferior area 6 in the macaque monkey. J. Comp. Neurol. 251, 281–298 (1986).

  39. 39

    Elbert, T., Pantev, C., Wienbruch, C., Rockstroh, B. & Taub, E. Increased cortical representation of the fingers of the left hand in string players. Science 270, 305–307 (1995).

  40. 40

    Graziano, M. S., Taylor, C. S. & Moore, T. Complex movements evoked by microstimulation of precentral cortex. Neuron 34, 841–851 (2002).

  41. 41

    Hauk, O., Johnsrude, I. & Pulvermüller, F. Somatotopic representation of action words in the motor and premotor cortex. Neuron 41, 301–307 (2004).

  42. 42

    Tettamanti, M. et al. Listening to action-related sentences activates fronto-parietal motor circuits. J. Cogn. Neurosci. 17, 273–281 (2005).

  43. 43

    Buccino, G. et al. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur. J. Neurosci. 13, 400–404 (2001).

  44. 44

    Holcomb, P. J. & Neville, H. J. Auditory and visual semantic priming in lexical decision: a comparision using event-related brain potentials. Lang. Cognit. Process. 5, 281–312 (1990).

  45. 45

    Sereno, S. C., Rayner, K. & Posner, M. I. Establishing a time line for word recognition: evidence from eye movements and event-related potentials. Neuroreport 13, 2195–2200 (1998).

  46. 46

    Pulvermüller, F., Härle, M. & Hummel, F. Neurophysiological distinction of verb categories. Neuroreport 11, 2789–2793 (2000).

  47. 47

    Hauk, O. & Pulvermüller, F. Neurophysiological distinction of action words in the fronto-central cortex. Hum. Brain Mapp. 21, 191–201 (2004).

  48. 48

    Shtyrov, Y., Hauk, O. & Pulvermüller, F. Distributed neuronal networks for encoding category-specific semantic information: the mismatch negativity to action words. Eur. J. Neurosci. 19, 1083–1092 (2004).

  49. 49

    Pulvermüller, F., Shtyrov, Y. & Ilmoniemi, R. J. Brain signatures of meaning access in action word recognition. J. Cogn. Neurosci. (in the press).

  50. 50

    Näätänen, R., Tervaniemi, M., Sussman, E., Paavilainen, P. & Winkler, I. 'Primitive intelligence' in the auditory cortex. Trends Neurosci. 24, 283–288 (2001).

  51. 51

    Pulvermüller, F., Hauk, O., Nikulin, V. V. & Ilmoniemi, R. J. Functional links between motor and language systems. Eur. J. Neurosci. 21, 793–797 (2005).

  52. 52

    Buccino, G. et al. Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. Cogn. Brain Res. (in the press).

  53. 53

    Patterson, K. & Hodges, J. R. in International Encyclopaedia of the Social and Behavioural Sciences (eds Thompson, R. F. & McClelland, J. L.) 3401–3405 (Pergamon, New York, USA, 2001).

  54. 54

    Scott, S. K. & Johnsrude, I. S. The neuroanatomical and functional organization of speech perception. Trends Neurosci. 26, 100–107 (2003).

  55. 55

    Posner, M. I. & Pavese, A. Anatomy of word and sentence meaning. Proc. Natl Acad. Sci. USA 95, 899–905 (1998).

  56. 56

    Chao, L. L., Haxby, J. V. & Martin, A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neurosci. 2, 913–919 (1999).

  57. 57

    Pulvermüller, F., Lutzenberger, W. & Preissl, H. Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. Cereb. Cortex 9, 497–506 (1999).

  58. 58

    Bird, H., Lambon-Ralph, M. A., Patterson, K. & Hodges, J. R. The rise and fall of frequency and imageability: noun and verb production in semantic dementia. Brain Lang. 73, 17–49 (2000).

  59. 59

    Humphreys, G. W. & Riddoch, M. J. On telling your fruit from your vegetables: a consideration of category-specific deficits after brain-damage. Trends Neurosci. 10, 145–148 (1987).

  60. 60

    Tyler, L. K., Moss, H. E., Durrant-Peatfield, M. R. & Levy, J. P. Conceptual structure and the structure of concepts: a distributed account of category-specific deficits. Brain Lang. 75, 195–231 (2000).

  61. 61

    McClelland, J. L. & Rogers, T. T. The parallel distributed processing approach to semantic cognition. Nature Rev. Neurosci. 4, 310–322 (2003).

  62. 62

    Bak, T. H., O'Donovan, D. G., Xuereb, J. H., Boniface, S. & Hodges, J. R. Selective impairment of verb processing associated with pathological changes in Brodmann areas 44 and 45 in the motor neurone disease-dementia-aphasia syndrome. Brain 124, 103–120 (2001).

  63. 63

    Neininger, B. & Pulvermüller, F. Word-category specific deficits after lesions in the right hemisphere. Neuropsychologia 41, 53–70 (2003).

  64. 64

    Pulvermüller, F. & Mohr, B. The concept of transcortical cell assemblies: a key to the understanding of cortical lateralization and interhemispheric interaction. Neurosci. Biobehav. Rev. 20, 557–566 (1996).

  65. 65

    Liberman, A. M. & Mattingly, I. G. The motor theory of speech perception revised. Cognition 21, 1–36 (1985).

  66. 66

    Braitenberg, V. & Schüz, A. in Language Origin: A Multidisciplinary Approach (eds Wind, J., Chiarelli, B., Bichakjian, B. H., Nocentini, A. & Jonker, A.) 89–102 (Kluwer, Dordrecht, Germany, 1992).

  67. 67

    Baddeley, A. Working memory: looking back and looking forward. Nature Rev. Neurosci. 4, 829–839 (2003).

  68. 68

    Fadiga, L., Fogassi, L., Pavesi, G. & Rizzolatti, G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73, 2608–2611 (1995).

  69. 69

    Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593–609 (1996).

  70. 70

    Rizzolatti, G., Fadiga, L., Gallese, V. & Fogassi, L. Premotor cortex and the recognition of motor actions. Brain Res. Cogn. Brain Res. 3, 131–141 (1996).

  71. 71

    Jeannerod, M. Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14, S103–S109 (2001).

  72. 72

    Hari, R. et al. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc. Natl Acad. Sci. USA 95, 15061–15065 (1998).

  73. 73

    Barsalou, L. W. Perceptual symbol systems. Behav. Brain Sci. 22, 577–609; discussion 610–660 (1999).

  74. 74

    Barsalou, L. W., Kyle Simmons, W., Barbey, A. K. & Wilson, C. D. Grounding conceptual knowledge in modality-specific systems. Trends Cogn. Sci. 7, 84–91 (2003).

  75. 75

    Lakoff, G. & Johnson, M. Philosophy in the Flesh: the Embodied Mind and its Challenge to Western Thought (Basic Books, New York, USA, 1999).

  76. 76

    Shastri, L., Grannes, D., Narayana, S. & Feldman, J. in Hybrid Information Processing in Adaptive Autonomous Vehicles (eds Kraetzschmar, G. K. & Palm, G.) (Springer, Berlin, Germany, 2005).

  77. 77

    Pulvermüller, F., Mohr, B. & Schleichert, H. Semantic or lexico–syntactic factors: what determines word-class specific activity in the human brain? Neurosci. Lett. 275, 81–84 (1999).

  78. 78

    Wittgenstein, L. Philosophical Investigations (Blackwell, Oxford, UK, 1953).

  79. 79

    Hommel, B., Musseler, J., Aschersleben, G. & Prinz, W. The theory of event coding (TEC): a framework for perception and action planning. Behav. Brain Sci. 24, 849–878; discussion 878–937 (2001).

  80. 80

    Wermter, S. et al. Towards multimodal neural network robot learning. Rob. Auton. Syst. 47, 171–175 (2004).

  81. 81

    Wermter, S., Weber, C., Elshaw, M., Gallese, V. & Pulvermüller, F. in Biomimetic Learning for Neural Robots (eds Wermter, S., Palm, G. & Elshaw, M.) (Springer, Berlin, Germany, in the press).

  82. 82

    Knoblauch, A., Markert, H. & Palm, G. in International Work-Conference on the Interplay Between Natural and Artificial Computation 2005 (eds Mira, J. & Alvarez, J. R.) 405–414 (Springer, Berlin, Germany, 2005).

  83. 83

    Pulvermüller, F., Hummel, F. & Härle, M. Walking or talking?: Behavioral and neurophysiological correlates of action verb processing. Brain Lang. 78, 143–168 (2001).

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Acknowledgements

This work was supported by the Medical Research Council (UK) and by the European Community under the Information Society Technologies Programme. For discussions related to this work, I am grateful to R. Assadollahi, T. Bak, V. Gallese, R. Ilmoniemi, O. Hauk, M. Kiefer, A. Knoblauch, W. Marslen-Wilson, B. Mohr, B. Neininger, G. Palm, K. Patterson, G. Rizzolatti, Y. Shtyrov and S. Wermter.

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  1. the Medical Research Council Cognition and Brain Sciences Unit, Cambridge, CB2 2EF, UK

    • Friedemann Pulvermüller

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