Speech prosodic characteristics recorded by functional magnetic resonance imaging in healthy volunteers
https://doi.org/10.14412/2074-2711-2017-4-17-25
Abstract
Many mechanisms for the brain organization of speech processes remain poorly understood now.
Objective: to assess the structural and functional organization of speech prosody, by applying functional magnetic resonance imaging (fMRI). This technique allows non-invasive studies of the organization of the speech system.
Patients and methods. Using their proposed three paradigms, the authors evaluated speech prosody in healthy volunteers. The first paradigm was aimed to determine the intonation characteristics of a sentence; the second paradigm is to study the given accentuated and non-accentuated rhythms, and the third to recognize melodies.
Results and discussion. In the first paradigm, there was bilateral activation of Wernicke's speech area (Brodmann's Area 22) that significantly prevailed in volume and intensity in the right hemisphere of the brain. Also, the right hemisphere predominantly showed activation of the supplementary motor region included in cytoarchitectonical Brodmann's Area 6. There was a significant activation Brodmann's Area 9 when a rhythm was determined in the right hemisphere and in Brodmann's Area 46 when melodies were recognized. The cerebellum, limbic system, subcortical structures, etc. were noted to be activated, which permits speech function to be regarded as a whole brain process.
Conclusion. The investigation has confirmed that different regions of both hemispheres of the brain are involved in the systemic organization of speech, which enables the authors to speak about the codominance of the hemispheres in respect of this function. The presented paradigms fully meet the objectives of the study and can be used to map the prosodic characteristics of speech.
About the Authors
V. A. KarlovRussian Federation
Department of Nervous System Diseases, Faculty of General Medicine
20, Delegatskaya St., Build. 1, Moscow 127473
V. M. Shklovsky
Russian Federation
23, Malyi Kropotkinsky Lane, Moscow 119991
R. N. Konovalov
Russian Federation
80, Volokolamskoe Shosse, Moscow 125367
A. G. Petrushevsky
Russian Federation
23, Malyi Kropotkinsky Lane, Moscow 119991
V. S. Zolovkina
Russian Federation
Department of Nervous System Diseases, Faculty of General Medicine
20, Delegatskaya St., Build. 1, Moscow 127473
References
1. Карлов ВА, Шкловский ВМ, Золовкина ВС. Развитие представлений об организации речевой системы. Журнал неврологии и психиатрии им. С.С. Корсакова. 2017;(5): 4-8. [Karlov VA, Shklovskii VM, Zolovkina VS. The development of ideas about the organization of the speech system. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2017;(5):4-8. (In Russ.)].
2. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006 Dec 16;368(9553):2167-78.
3. Vingerhoets G, Berckmoes C, Stroobant N. Cerebral Hemodynamics During Discrimination of Prosodic and Semantic Emotion in Speech Studied by Transcranial Doppler Ultrasonography. Neuropsychology. 2003 Jan;17(1):93-9.
4. Filippi M. fMRI techniques and protocols. Humana press; 2009. 25 p.
5. Майорова ЛА, Мартынова ОВ, Федина ОН, Петрушевский АГ. ФМРТ-исследование нарушения постинсультной сенсорной афазией. Журнал высшей нервной деятельности. 2013;(3):328-37. [Maiorova LA, Martynova OV, Fedina ON, Petrushevskii AG. An FMRI study of violations of post-stroke sensory aphasia. Zhurnal vysshei nervnoi deyatel'nosti. 2013;(3):328-37. (In Russ.)].
6. Кремнева ЕИ, Коновалов РН, Кротенкова МВ и др. Функциональная асимметрия речевых структур у здоровых людей, выявляемая при помощи функциональной магнитно-резонансной томографии (фМРТ). Сборник материалов конференции «Современные направления исследований функциональной межполушарной асимметрии и пластичности мозга». Москва; 2010. С. 173-7. [Kremneva EI, Konovalov RN, Krotenkova MV, et al. Funktsional'naya asimmetriya rechevykh struktur u zdorovykh lyudei, vyyavlyaemaya pri pomoshchi funktsional'noi magnitno-rezonansnoi tomografii (fMRT). Sbornik materialov konferentsii «Sovremennye napravleniya issledovanii funktsional'noi mezhpolusharnoi asimmetrii i plastichnosti mozga» [Functional asymmetry of speech structures in healthy individuals, detected with functional magnetic resonance imaging (fMRI). The collection of materials of conference «Modern directions of research of the functional interhemispheric asymmetry and plasticity of the brain»]. Moscow; 2010. P. 173-7.]
7. Власова РМ. Мозговые механизмы номинативной функции речи: нейропсихологический и нейровизуализационный подход. Дисс. канд. психол. наук. Москва; 2013. 144 с. [Vlasova RM. Brain mechanisms of nominative function of speech: neuropsychological and neuroimaging approach. Diss. cand. psychol. sci. Moscow; 2013. 144 p.]
8. Стрельников КН. Функциональная асимметрия мозга при восприятии интонационных характеристик речи в норме и при шизофрении. Автореф. дисс. канд. мед. наук. Санкт-Петербург; 2003. 23 с. [Strel'nikov KN. Functional brain asymmetry in the perception of intonational characteristics of speech in norm and at schizophrenia. Autoref. diss. cand. med. sci. Saint-Petersburg; 2003. 23 p.]
9. Шабетник ОИ. Особенности нарушения высших психических функций и их восстановление при поражениях правого полушария мозга. Дисс. канд. пед. наук. Москва; 2011. 153 с. [Shabetnik OI. Features of disorders of higher mental functions and their recovery in patients with lesions of the right hemisphere of the brain. Diss. cand. ped. sci. Moscow; 2011. 153 p.]
10. Friston KJ, Holmes AP, Worsley KJ, et al. Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping. 1995;2(4):189-210. doi: 10.1002/hbm.460020402
11. Сепп ЕК. История развития нервной системы позвоночных. 1949. 424 с. [Sepp EK. Istoriya razvitiya nervnoi sistemy pozvonochnykh [The history of the development of the nervous system of vertebrates]. 1949. 424 p.].
12. Карлов ВА. Детская неврология как инструмент познания развивающегося мозга. Журнал неврологии и психиатрии им. С.С. Корсакова. 2002;(4):5-6. [Karlov VA. Pediatric neurology as a tool for understanding the developing brain. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2002;(4):5-6. (In Russ.)].
13. Лурия АР. Высшие корковые функции и их нарушение при локальных поражениях мозга. Москва: Просвещение; 1989. 244 с. [Luriya AR. Vysshie korkovye funktsii i ikh narushenie pri lokal'nykh porazheniyakh mozga [Higher cortical functions and their impairment in local lesions of the brain]. Moscow: Prosveshchenie; 1989. 244 p.]
14. Лурия АР, Юдович ФЯ. Речь и развитие психических процессов у ребенка. Москва; 1956. [Luriya AR, Yudovich FYa. Rech' i razvitie psikhicheskikh protsessov u rebenka [Speech and development of mental processes in the child]. Moscow; 1956.]
15. Бадалян ЛО. Детская неврология. Москва; 2001. [Badalyan LO. Detskaya nevrologiya [Pediatric neurology]. Moscow; 2001.]
16. Исенина ЕИ. Психолингвистические закономерности речевого онтогенеза (дословесный период). Иваново; 1983. [Isenina EI. Psikholingvisticheskie zakonomernosti rechevogo ontogeneza (doslovesnyiy period) [Psycholinguistic regularities of speech ontogenesis (prespeech period)]. Ivanovo; 1983.]
17. Babiloni C, Ferretti A, Del Gratta C, et al. Human cortical responses during one-bit delayed-response tasks: an fMRI study. Brain Res Bull. 2005 May 15;65(5):383-90.
18. Kü bler A, Dixon V, Garavan H. Automaticity and reestablishment of executive control-an fMRI study. J Cogn Neurosci. 2006 Aug;18(8):1331-42. doi: 10.1162/jocn.2006.18.8.1331.
19. Abrahams S, Goldstein LH, Simmons A, et al. Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses. Hum Brain Mapp. 2003 Sep;20(1): 29-40. doi: 10.1002/hbm.10126
20. Nakai T, Kato C, Matsuo K. An FMRI study to investigate auditory attention: a model of the cocktail party phenomenon. Magn Reson Med Sci. 2005;4(2):75-82. doi: 10.2463/mrms.4.7
21. Knauff M, Mulack T, Kassubek J, et al. Spatial imagery in deductive reasoning: a functional MRI study. Brain Research. Brain Res Cogn Brain Res. 2002 Apr;13(2):203-12. doi: 10.1016/S0926-6410(01)00116-1
22. Shallice T, Stuss DT, Alexander MP, et al. The multiple dimensions of sustained attention. Cortex. 2008 Jul-Aug;44(7):794-805. doi: 10.1016/j.cortex.2007.04.002. Epub 2007 Dec 23.
23. Slotnic SD, Moo LR. Prefrontal cortex hemispheric specialization for categorical and coordinate visual spatial memory. Neuropsychologia. 2006;44(9):1560-8. Epub 2006 Mar 3. doi: 10.1016/j.neuropsychologia.2006.01.018
24. Leung HC, Gore JC, Goldman-Rakic PS. Sustained mnemonic response in the human middle frontal gyrus during on-line storage of spatial memoranda. J Cogn Neurosci. 2002 May 15;14(4):659-71. doi: 10.1162/08989290260045882
25. Zhang JX, Leung HC, Johnson MK. Frontal activations associated with accessing and evaluating information in working memory: an fMRI study. Neuroimage. 2003 Nov;20(3): 1531-9. doi: 10.1016/j.neuroimage.2003.07.016
26. Pochon JB, Levy R, Fossati P, et al. The neural system that bridges reward and cognition in humans: an fMRI study. Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5669-74. doi: 10.1073/pnas.082111099
27. Raye CL, Johnson MK, Mitchell KJ, et al. Neuroimaging a single thought: dorsolateral PFC activity associated with refreshing justactivated information. Neuroimage. 2002 Feb; 15(2):447-53. doi: 10.1006/nimg.2001.0983
28. Xie S, Xiao J, Jiang X. The fMRI study of the calculation tasks in normal aged volunteers. Beijing Da Xue Xue Bao. 2003 Jun 18;35(3):311-3.
29. Rickard TC, Romero SG, Basso G, et al. The calculating brain: an fMRI study. Neuropsychologia. 2000;38(3):325-35. doi: 10.1016/S0028-3932(99)00068-8
30. Bermpohl F, Pascual-Leone A, Amedi A, et al. Attentional modulation of emotional stimulus processing: an fMRI study using emotional expectancy. Human Hum Brain Mapp. 2006 Aug;27(8):662-77. doi: 10.1002/hbm.20209
31. Royet JP, Koenig O, Gregoire MC, et al. Functional anatomy of perceptual and semantic processing for odors. J Cogn Neurosci. 1999 Jan;11(1):94-109. doi: 10.1162/089892999563166
32. Benton AL. Differential behavioral effects of frontal lobe disease. Neuropsychologia. 1968;6(1):53-60.
33. Wapner W, Hamby S, Gardner H. The role of the right hemisphere in the apprehension of complex linguistic materials. Brain Lang. 1981 Sep;14(1):15-33.
34. Stemmer B, Giroux F, Joanette Y. Production and evaluation of requests by right hemisphere brain-damage individuals. Brain Lang. 1994 Jul;47(1):1-31.
35. Winner E, Gardner H. The comprehension of metaphor in brain-damaged patients. Brain. 1977 Dec;100(4):717-29.
36. Черниговская ТВ, Деглин ВЛ. Метафорическое и силлогическое мышление как проявление функциональной асимметрии мозга. Ученые записки Тартуского Университета. Труды по знаковым системам. 1986;(19):68-84. [Chernigovskaya TV, Deglin VL. Syllogisme and metaphorical thinking as a manifestation of functional asymmetry of the brain. Uchenye zapiski Tartuskogo Universiteta, Trudy po znakovym sistemam. 1986;(19):68- 84.]
37. Lundgren K, Brownell H, Roy S, Cayer-Meade C. A metaphor comprehension intervention for patients with right hemmisphere brain damage: A pilot study. Brain Lang. 2006;99(1-2): 69-70.
38. Vanhalle C, Lemieux S, Joubert S, et al. Processing of speech acts by right hemisphere brain-damaged patients: an ecological approach. Aphasiology. 2000;14(11):1127-41.
39. Myers PS. Toward a definition of RHD syndrome. Aphasiology. 2001;15:913-8.
40. La Pointe L, Murdoch B, Stierwalt JA. Brain-based communication disorders. San Diego: Plural Publishing; 2010.
41. Chantraine Y, Joanette Y, Ska B. Conversational abilities in patients with right hemisphere damage. Journal of Neurolinguistics. 1998;(11):21–32.
42. Glosser G. Discourse patterns in neurologically impaired and aged populations. In: Brownell HH, Joanette Y, editors. Narrative discourse in neurologically impaired and normal aging adults. San Diego: Singular; 1993.P. 191–212.
43. Tompkins CA, Fassbinder W, Lehman Blake M, et al. Inference generation during text comprehension by adults with right hemisphere brain damage: Activation failure versus multiple activation. J Speech Lang Hear Res. 2004 Dec; 47(6):1380-95.
44. Blake ML. Perspectives on treatment for communication deficits associated with right hemisphere brain damage. Am J Speech Lang Pathol. 2007 Nov;16(4):331-42.
45. Shook A, Marian V, Bartolotti J, Schroeder SR. Musical experience influences statistical learning of a novel language. Am J Psychol. 2013 Spring;126(1):95-104.
46. Amunts K, Schlaug G, Jä ncke L, et al. Motor cortex and hand motor skills: structural compliance in the human brain. Hum Brain Mapp. 1997;5(3):206-15. doi: 10.1002/(SICI)1097- 0193(1997)5:3<206::AID-HBM5>3.0.CO;2-7.
47. Pantev C, Oostenveld R., Engelien A, et al. Increased auditory cortical representation in musicians. Nature. 1998 Apr 23;392(6678):811-4.
48. Musacchia G, Sams M, Skoe E, Kraus N. Musicians have enhanced subcortical auditory and audiovisual processing of speech and music. Proc Natl Acad Sci U S A. 2007 Oct 2;104(40): 15894-8. Epub 2007 Sep 26.
49. Bengtsson S, Nagy Z, Skare S, et al. Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci. 2005 Sep;8(9):1148-50. Epub 2005 Aug 7.
50. Kleber B, Veit R, Birbaumer N, et al. The brain of opera singers: experience-dependent changes in functional activation. Cereb Cortex. 2010 May;20(5):1144-52. doi: 10.1093/cercor/bhp177. Epub 2009 Aug 19.
51. Ellis RJ, Norton AC, Overy K, et al. Differentiating maturational and training influences on fMRI activation during music processing. Neuroimage. 2012 Apr 15;60(3):1902-12. doi: 10.1016/j.neuroimage.2012.01.138. Epub 2012 Feb 9.
52. Ohnishi T, Matsuda H, Asada T, et al. Functional anatomy of musical perception in musicians. Cereb Cortex. 2001 Aug;11(8): 754-60.
53. Sluming V, Barrick T, Howard M, et al. Voxel-based morphometry reveals increased gray matter density in Broca's area in male symphony orchestra musicians. Neuroimage. 2002 Nov;17(3):1613-22.
54. Hutchinson S, Lee LH, Gaab N, Schlaug G. Cerebellar volume of musicians. Cereb Cortex. 2003 Sep;13(9):943-9.
55. Foster NE, Zatorre RJ. Cortical structure predicts success in performing musical transformation judgments. Neuroimage. 2010 Oct 15; 53(1):26-36. doi: 10.1016/j.neuroimage.2010.06.042. Epub 2010 Jun 23.
56. Elmer S, Meyer M, Jä ncke L. Neurofunctional and behavioral correlates of phonetic and temporal categorization in musically trained. Cereb Cortex. 2012 Mar;22(3):650-8. doi: 10.1093/cercor/bhr142. Epub 2011 Jun 16.
57. Keenan JP, Thangaraj V, Halpern AR, Schlaug G. Absolute pitch and planum temporale. Neuroimage. 2001 Dec;14(6):1402-8.
58. Norton A, Winner E, Cronin K, et al. Are there pre-existing neural, cognitive, or motoric markers for musical ability? Brain Cogn. 2005 Nov;59(2):124-34. Epub 2005 Jul 28.
59. Schlaug G, Norton A, Overy K, Winner E. Effects of music training on the child's brain and cognitive development. Ann N Y Acad Sci. 2005 Dec;1060:219-30.
60. Schlaug G, Forgeard M, Zhu L, et al. Training-induced neuroplasticity in young children. Ann N Y Acad Sci. 2009 Jul;1169:205-8. doi: 10.1111/j.1749-6632.2009.04842.x.
61. Ellis RJ, Norton AC, Overy K, et al. Differentiating maturational and training influences on fMRI activation during music processing. Neuroimage. 2012 Apr 15;60(3):1902-12. doi: 10.1016/j.neuroimage.2012.01.138. Epub 2012 Feb 9.
62. Mavridis IN, Pyrgelis ES. Brain Activation During Singing: «Clef de Sol Activation» Is the «Concert» of the Human Brain. Med Probl Perform Art. 2016;31(1):45-50.
63. Afif A, Minotti L, Kahane P, Hoffmann D. Anatomofunctional organization of the insular cortex: A study using intracerebral electrical stimulation in epileptic patients. Epilepsia. 2010;51(11):2305-2315. doi: 10.1111/j.1528-1167.2010.02755.x.
64. Augustine J. The insular lobe in primates including humans. Neurol Res. 1985 Mar;7(1): 2-10.
65. Shelley B, Trimble M. The Insular Lobe of Reil–its Anatamico-Functional, Behavioural and Neuropsychiatric Attributes in Humans. World J Biol Psychiatry. 2004;5(4):176-200. doi: 10.1080/15622970410029933.
66. Sö rö s P, Hachinski V. Cardiovascular and neurological causes of sudden death after ischaemic stroke. Lancet Neurol. 2012 Feb; 11(2):179-88. doi: 10.1016/S1474-4422(11)70291-5.
67. Chen Q, Zhang Y, Hou H, et al. Neural correlates of the popular music phenomenon: evidence from functional MRI and PET imaging. Eur J Nucl Med Mol Imaging. 2017 Jun; 44(6):1033-1041. doi: 10.1007/s00259-017-3614-7. Epub 2017 Jan 12.
68. Gordon HW. Left hemisphere dominance for rhythmic elements in dichotomically presented melodies. Cortex. 1978 Mar;14(1):58-70.
69. Parkin AJ, Williamson P. Cerebral Lateralisation at different stages of facial processing. Cortex. 1987 Mar;23(1):99-110.
70. Ротенберг В. Мозг. Стратегия полушарий. Метафора в свете гештальт-подхода. Екатеринбург: ЛИТУР; 2001. 320 с. [Rotenberg V. Mozg. Strategiya polusharii. Metafora v svete geshtal't-podkhoda [Brain. Strategy hemispheres. Metaphor in the light of the gestalt approach]. Ekaterinburg: LITUR; 2001. 320 p.]
Review
For citations:
Karlov V.A., Shklovsky V.M., Konovalov R.N., Petrushevsky A.G., Zolovkina V.S. Speech prosodic characteristics recorded by functional magnetic resonance imaging in healthy volunteers. Neurology, Neuropsychiatry, Psychosomatics. 2017;9(4):17-25. (In Russ.) https://doi.org/10.14412/2074-2711-2017-4-17-25