Two distinct auditory-motor circuits for monitoring speech production as revealed by content-specific suppression of auditory cortex

Cerebral Cortex

Volumn 25, Issue 6, 2015, Pages 1576-1586

  Ylinen, Sari ^a,b   Nora, Anni ^a,c   Leminen, Alina ^a   Hakala, Tero ^a   Huotilainen, Minna ^a,d,e   Shtyrov, Yury ^f,g,h   Mäkelä, Jyrki P ^b   Service, Elisabet ^a,i  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c AALTO UNIVERSITY   (Finland)

^d UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^e FINNISH INSTITUTE OF OCCUPATIONAL HEALTH   (Finland)

^f AARHUS UNIVERSITY   (Denmark)

^g LUND UNIVERSITY   (Sweden)

^h MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

ⁱ MCMASTER UNIVERSITY   (Canada)

Author keywords

asymmetric speech monitoring; efference copy; forward prediction; magnetoencephalography (MEG); phonological working memory

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; AUDITORY FEEDBACK; AUDITORY MOTOR CIRCUIT; AUDITORY RESPONSE; AUDITORY STIMULATION; BRAIN CORTEX; BRAIN MAPPING; CONSONANT; FEMALE; HUMAN; LEFT HEMISPHERE; MALE; NORMAL HUMAN; PHONETICS; PRIORITY JOURNAL; RIGHT HANDEDNESS; RIGHT HEMISPHERE; SPEECH; SPEECH PERCEPTION; VISUAL STIMULATION; VOWEL; WORKING MEMORY; ANALYSIS OF VARIANCE; HEMISPHERIC DOMINANCE; INHIBITION (PSYCHOLOGY); MAGNETOENCEPHALOGRAPHY; NERVE TRACT; PHOTOSTIMULATION; PHYSIOLOGY; SPEECH ANALYSIS; YOUNG ADULT;

ACOUSTIC STIMULATION; ADULT; ANALYSIS OF VARIANCE; AUDITORY CORTEX; BRAIN MAPPING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETOENCEPHALOGRAPHY; MALE; NEURAL PATHWAYS; PHOTIC STIMULATION; SPEECH; SPEECH PERCEPTION; SPEECH PRODUCTION MEASUREMENT; YOUNG ADULT;

EID: 84930355265     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht351     Document Type: Article

References (55)

1. Abrams DA, Nicol T, Zecker S, Kraus N. 2008. Right-hemisphere auditory cortex is dominant for coding syllable patterns in speech. J Neurosci. 28:3958-3965.
2. Ahveninen J, Jääskeläinen IP, Raij T, Bonmassar G, Devore S, Hämäläinen M, Levänen S, Lin FH, Sams M, Shinn-Cunningham BG et al. 2006. Task-modulated "what" and "where" pathways in human auditory cortex. Proc Natl Acad Sci USA. 103:14608-14613.
3. Alho K, Vorobyev VA, Medvedev SV, Pakhomov SV, Roudas MS, Tervaniemi M, van Zuijen T, Näätänen R. 2003. Hemispheric lateralization of cerebral blood-flow changes during selective listening to dichotically presented continuous speech. Brain Res Cogn Brain Res. 17:201-211.
4. Aliu SO, Houde JF, Nagarajan SS. 2009. Motor-induced suppression of the auditory cortex. J Cogn Neurosci. 21:791-802.
5. Baddeley AD. 1986.Working memory. Oxford (UK): Clarendon Press.
6. Baddeley AD, Hitch G. 1974. Working memory. In: Bower GH, editor. The psychology of learning and motivation: advances in research and theory. New York (NY): Academic Press. p. 47-89.
7. Boemio A, Fromm S, Braun A, Poeppel D. 2005. Hierarchical and asymmetric temporal sensitivity in human auditory cortices. Nat Neurosci. 8:389-395.
8. Boersma P, Weenink D. 2008. Praat: doing phonetics by computer [Computer program]. Version 5.0.40. Available from: http://www. praat.org/ (retrieved 17 November 2008).
9. Chang EF, Niziolek CA, Knight RT, Nagarajan SS, Houde JF. 2013. Human cortical sensorimotor network underlying feedback control of vocal pitch. Proc Natl Acad Sci USA. 110:2653-2658.
10. Curio G, Neuloh G, Numminen J, Jousmäki V, Hari R. 2000. Speaking modifies voice-evoked activity in the human auditory cortex. Hum Brain Mapp. 9:183-191.
11. Davachi L, Maril A, Wagner AD. 2001. When keeping in mind supports later bringing to mind: neural markers of phonological rehearsal predict subsequent remembering. J Cogn Neurosci. 13: 1059-1070.
12. Ellis N, Beaton A. 1993. Factors affecting the learning of foreign language vocabulary: imagery keyword mediators and phonological short-term memory. Q J Exp Psychol A. 46:533-558.
13. Friston K. 2005. A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci. 360:815-836.
14. Gagnepain P, Henson RN, Davis MH. 2012. Temporal predictive codes for spoken words in auditory cortex. Curr Biol. 22:615-621.
15. Giraud AL, Poeppel D. 2012. Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci. 15:511-517.
16. Grill-Spector K, Henson R, Martin A. 2006. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci. 10:14-23.
17. Guenther FH. 1995. Speech sound acquisition, coarticulation, and rate effects in a neural network model of speech production. Psychol Rev. 102:594-621.
18. Guenther FH, Ghosh SS, Tourville JA. 2006. Neural modeling and imaging of the cortical interactions underlying syllable production. Brain Lang. 96:280-301.
19. Heinks-Maldonado TH, Nagarajan SS, Houde JF. 2006. Magnetoencephalographic evidence for a precise forward model in speech production. Neuroreport. 17:1375-1379.
20. Hickok G. 2012. Computational neuroanatomy of speech production. Nat Rev Neurosci. 13:135-145.
21. Hickok G, Houde J, Rong F. 2011. Sensorimotor integration in speech processing: computational basis and neural organization. Neuron. 69:407-422.
22. Hickok G, Poeppel D. 2007. The cortical organization of speech processing. Nat Rev Neurosci. 8:393-402.
23. Hillyard SA, Hink RF, Schwent VL, Picton TW. 1973. Electrical signs of selective attention in the human brain. Science. 182:177-180.
24. Houde JF, Nagarajan SS. 2011. Speech production as state feedback control. Front Hum Neurosci. 5:82.
25. Houde JF, Nagarajan SS, Sekihara K, Merzenich MM. 2002. Modulation of the auditory cortex during speech: an MEG study. J Cogn Neurosci. 14:1125-1138.
26. Jääskeläinen IP, Ojanen V, Ahveninen J, Auranen T, Levänen S, Möttönen R, Tarnanen I, Sams M. 2004. Adaptation of neuromagnetic N1 responses to phonetic stimuli by visual speech in humans. Neuroreport. 15:2741-2744.
27. Jacquemot C, Scott SK. 2006. What is the relationship between phonological short-term memory and speech processing? Trends Cogn Sci. 10:480-486.
28. Kauramäki J, Jääskeläinen IP, Hari R, Möttönen R, Rauschecker JP, Sams M. 2010. Lipreading and covert speech production similarly modulate human auditory-cortex responses to pure tones. J Neurosci. 30:1314-1321.
29. Klucharev V, Möttönen R, Sams M. 2003. Electrophysiological indicators of phonetic and non-phonetic multisensory interactions during audiovisual speech perception. Brain Res Cogn Brain Res. 18:65-75.
30. Kujala A, Alho K, Valle S, Sivonen P, Ilmoniemi RJ, Alku P, Näätänen R. 2002. Context modulates processing of speech sounds in the right auditory cortex of human subjects. Neurosci Lett. 331:91-94.
31. Levelt WJM. 1989. Speaking: from intention to articulation. Cambridge (MA): MIT Press.
32. Mäkelä JP. 2007. Chapter 25: Magnetoencephalography (auditory evoked fields). In: Burkard RF, Eggermont JJ, Don M, editors. Auditory evoked potentials. Philadelphia (PA): Lippincott Williams & Wilkins. p. 525-545.
33. McGettigan C, Scott SK. 2012. Cortical asymmetries in speech perception: what's wrong, what's right and what's left? Trends Cogn Sci. 16:269-276.
34. Niziolek CA, Nagarajan SS, Houde JF. 2013. What does motor efference copy represent? Evidence from speech production. J Neurosci. 33:16110-16116.
35. Numminen J, Curio G. 1999. Differential effects of overt, covert and replayed speech on vowel-evoked responses of the human auditory cortex. Neurosci Lett. 272:29-32.
36. Pardo PJ, Mäkelä JP, Sams M. 1999. Hemispheric differences in processing tone frequency and amplitude modulations. Neuroreport. 10:3081-3086.
37. Paulesu E, Frith CD, Frackowiak RS. 1993. The neural correlates of the verbal component of working memory. Nature. 362:342-345.
38. Poeppel D. 2003. The analysis of speech in different temporal integration windows: cerebral lateralization as "asymmetric campling in time". Speech Commun. 41:245-255.
39. Price CJ, Crinion JT, MacSweeney M. 2011. A generative model of speech production in Broca's and Wernicke's areas. Front Psychol. 2:237.
40. Rauschecker JP, Scott SK. 2009. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci. 12:718-724.
41. Sams M, Hari R, Rif J, Knuutila J. 1993. The human auditory sensory memory trace persists about 10s: neuromagnetic evidence. J Cogn Neurosci. 5:363-370.
42. Sams M, Möttönen R, Sihvonen T. 2005. Seeing and hearing others and oneself talk. Brain Res Cogn Brain Res. 23:429-435.
43. Schwartz J, Tallal P. 1980. Rate of acoustic change may underlie hemispheric specialization for speech perception. Science. 207:1380-1381.
44. Scott M. 2013. Corollary discharge provides the sensory content of inner speech. Psychol Sci. 24:1824-1830.
45. Scott M, Yeung HH, Gick B, Werker JF. 2013. Inner speech captures the perception of external speech. J Acoust Soc Am. 133: EL286-EL292.
46. Sperry RW. 1950. Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol. 43:482-489.
47. Taulu S, Simola J. 2006. Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Phys Med Biol. 51:1759-1768.
48. Tian X, Poeppel D. 2013. The effect of imagination on stimulation: the functional specificity of efference copies in speech processing. J Cogn Neurosci. 25:1020-1036.
49. Tian X, Poeppel D. 2010. Mental imagery of speech and movement implicates the dynamics of internal forward models. Front Psychol. 1:166.
50. Tian X, Poeppel D. 2012. Mental imagery of speech: linking motor and perceptual systems through internal simulation and estimation. Front Hum Neurosci. 6:314.
51. Tourville JA, Guenther FH. 2011. The DIVA model: a neural theory of speech acquisition and production. Lang Cogn Process. 26:952-981.
52. Ventura MI, Nagarajan SS, Houde JF. 2009. Speech target modulates speaking induced suppression in auditory cortex. BMC Neurosci. 10:58.
53. von Holst E, Mittelstaedt H. 1950. Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Die Naturwissenschaften. 37:464-476.
54. Wacongne C, Labyt E, van Wassenhove V, Bekinschtein T, Naccache L, Dehaene S. 2011. Evidence for a hierarchy of predictions and prediction errors in human cortex. Proc Natl Acad Sci USA. 108:20754-20759.
55. Zatorre RJ, Belin P, Penhune VB. 2002. Structure and function of auditory cortex: music and speech. Trends Cogn Sci. 6:37-46.