Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque

Nature Neuroscience

Volumn 9, Issue 8, 2006, Pages 1064-1070

  Gil Da Costa, Ricardo ^a,b,c,d   Martin, Alex ^b   Lopes, Marco A ^a   Mũoz, Monica ^e   Fritz, Jonathan B ^f   Braun, Allen R ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c HARVARD UNIVERSITY   (United States)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN 15;

ACOUSTICS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; EVOLUTION; FEASIBILITY STUDY; FEMALE; HEARING; LANGUAGE; MACACA; MALE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SPECIES DIFFERENCE; SUPRASYLVIAN GYRUS; TELENCEPHALON; VOCALIZATION; WERNICKE AREA;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; CEREBRAL CORTEX; EVOLUTION; FEMALE; HUMANS; LANGUAGE; MACACA; MAGNETIC RESONANCE IMAGING; MALE; POSITRON-EMISSION TOMOGRAPHY; RANDOM ALLOCATION; SPECIES SPECIFICITY; VOCALIZATION, ANIMAL;

EID: 33747593338     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1741     Document Type: Article

References (49)

1. Hauser, M.D., Chomsky, N. & Fitch, W.T. The faculty of language: what is it, who has it, and how did it evolve? Science 298, 1569-1579 (2002).
2. Seyfarth, R.M., Cheney, D.L. & Bergman, T.J. Primate social cognition and the origins of language. Trends Cogn. Sci. 9, 264-266 (2005).
3. Seyfarth, R.M. & Cheney, D.L. Signalers and receivers in animal communication. Annu. Rev. Psychol. 54, 145-173 (2003).
4. Ghazanfar, A.A. & Santos, L.R. Primate brains in the wild: the sensory bases for social interactions. Nature Rev. Neurosci. 5, 603-616 (2004).
5. Fitch, W.T. Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J. Acoust. Soc. Am. 102, 1213-1222 (1997).
6. Poremba, A. et al. Species-specific calls evoke asymmetric activity in the monkey's temporal poles. Nature 427, 448-451 (2004).
7. Rauschecker, J.P., Tian, B. & Hauser, M.D. Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268, 111-114 (1995).
8. Gil-da-Costa, R. et al. Toward an evolutionary perspective on conceptual representation: species-specific calls activate visual and affective processing systems in the macaque. Proc. Natl. Acad. Sci. USA. 101, 17516-17521 (2004).
9. Gifford, G.W., MacLean, K.A., Hauser, M.D. & Cohen, Y.E. The neurophysiology of functionally meaningful categories: macaque ventrolateral prefrontal cortex plays a critical role in spontaneous categorization of species-specific vocalizations. J. Cogn. Neurosci. 17, 1471-1482 (2005).
10. Romanski, L.M. & Goldman-Rakic, P.S. An auditory domain in primate prefrontal cortex. Nat. Neurosci. 5, 15-16 (2002).
11. Caplan, D. Neurolinguistics and Linguistic Aphasiology (Cambridge Univ. Press, Cambridge, UK, 1987).
12. Galaburda, A.M. & Pandya, D.N. The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey. J. Comp. Neurol. 221, 169-184 (1983).
13. Preuss, T.M. & Goldman-Rakic, P.S. Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca. J. Comp. Neurol. 310, 475-506 (1991).
14. Deacon, T.W. The neural circuitry underlying primate calls and human language. Hum. Evol. 4, 367-401 (1989).
15. Kohler, E. et al. Hearing sounds, understanding actions: action representation in mirror neurons. Science 297, 846-848 (2002).
16. Geyer, S., Matelli, M., Luppino, G. & Zilles, K. Functional neuroanatomy of the primate isocortical motor system. Anat. Embryol. (Berl.) 202, 443-474 (2000).
17. Rizzolatti, G. & Arbib, M.A. Language within our grasp. Trends Neurosci. 21, 188-194 (1998).
18. Picard, N. & Strick, P.L. Imaging the premotor areas. Curr. Opin. Neurobiol. 11, 663-672 (2001).
19. Petrides, M. & Pandya, D.N. Comparative cytoarchitectonic analysis of the human and macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur. J. Neurosci. 16, 291-310 (2002).
20. Petrides, M., Cadoret, G. & Mackey, S. Orofacial somatomotor responses in the macaque monkey homologue of Broca's area. Nature 435, 1235-1238 (2005).
21. Ulanovsky, N., Las, L. & Nelken, I. Processing of low-probability sounds by cortical neurons. Nat. Neurosci. 6, 391-398 (2003).
22. Leinonen, L., Hyvarinen, J. & Sovijarvi, A.R. Functional properties of neurons in the temporo-parietal association cortex of awake monkey. Exp. Brain Res. 39, 203-215 (1980).
23. Binder, J.R. et al. Human temporal lobe activation by speech and nonspeech sounds. Cereb. Cortex 10, 512-528 (2000).
24. Warren, J.D. & Griffiths, T.D. Distinct mechanisms for processing spatial sequences and pitch sequences in the human auditory brain. J. Neurosci. 23, 5799-5804 (2003).
25. Geschwind, N. & Levitsky, W. Human brain: left-right asymmetries in temporal speech regions. Science 161, 186-187 (1968).
26. Belin, P., Zatorre, R., Lafaille, P., Ahad, P. & Pike, B. Voice-selective areas in human auditory cortex. Nature 403, 309-312 (2000).
27. Papathanassiou, D. et al. A common language network for comprehension and production: a contribution to the definition of language epicenters with PET. Neuroimage 11, 347-357 (2000).
28. Passingham, R.E. The specialization of the human neocortex. in Comparative Neuropsychology (ed. Milner. D.) Ch. 15 271-298 (Oxford Univ. Press, Oxford, 1998).
29. Damasio, A.R. & Geschwind, N. The neural basis of language. Annu. Rev. Neurosci. 7, 127-147 (1984).
30. Catani, M., Jones, D.K. & Ffytche, D.H. Perisylvian language networks of the human brain. Ann. Neurol. 57, 8-16 (2005).
31. Sereno, M.I. Language and the primate brain. in Proceedings Thirteenth Annual Conference of the Cognitive Science Society, 79-84 (Lawrence Erlbaum Associates, Hillsdale, New Jersey, 1991).
32. Rizzolatti, G. & Luppino, G. The cortical motor system. Neuron 31, 889-901 (2001).
33. Romanski, L.M., Averbeck, B.B. & Diltz, M. Neural representation of vocalizations in the primate ventral prefrontal cortex. J. Neurophysiol. 93, 734-747 (2004).
34. Price, C.J. et al. Hearing and saying. The functional neuro-anatomy of auditory word processing. Brain 119, 919-931 (1996).
35. Poeppel, D. et al. Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex. Neuropsychologia 42, 183-200 (2004).
36. Jurgens, U. Neural pathways underlying vocal control. Neurosci. Biobehav. Rev. 26, 235-258 (2002).
37. Wise, S.P. The evolution of ventral premotor cortex and the primate way of reaching. in Evolution of Primate Nervous Systems: A Comprehensive Reference Vol. 4, (ed. Kaas. J.H.) Ch. 11 (in the press).
38. Gemba, H., Miki, N. & Sasaki, K. Cortical field potentials preceding vocalization and influences of cerebellar hemispherectomy upon them in monkeys. Brain Res. 697, 143-151 (1995).
39. Hast, M.H., Fischer, J.M., Wetzel, A.B. & Thompson, V.E. Cortical motor representation of the laryngeal muscles in Macaca mulatta. Brain Res. 73, 229-240 (1974).
40. Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593-609 (1996).
41. Thompson-Schill, S.L., Bedny, M. & Goldberg, R.F. The fronal lobes and the regulation of mental activity. Curr. Opin. Neurobiol. 15, 219-224 (2005).
42. Fogassi, L. et al. Parietal lobe: from action organization to intention understanding. Science 308, 662-667 (2005).
43. Gannon, P.J., Holloway, R.L., Broadfield, D.C. & Braun, A.R. Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. Science 279, 220-222 (1998).
44. Barsalou, L.W. Continuity of the conceptual system across species. Trends Cogn. Sci. 9, 309-311 (2005).
45. Gouzoules, H. & Gouzoules, S. Agonistic screams differ among four species of macaques: the significance of motivation-structural rules. Anim. Behav. 59, 501-512 (2000).
46. Chi, T., Ru, P. & Shamma, S. Multiresolution spectrotemporal analysis of complex sounds. J. Acoust. Soc. Am. 118, 887-906 (2005).
47. Paxinos, G., Huang, X. & Toga, A.W. The Rhesus Monkey Brain in Stereotaxic Coordinates (Academic Press, San Diego, 2000).
48. Pandya, D.N. & Sanides, F. Architectonic parcelation of the temporal operculum in rhesus monkey and its projection pattern. Z. Anat. Entwicklungsgesch 139, 127-61 (1973).
49. Seltzer, B. & Pandya, D.N. Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res. 149, 1-24 (1978).