From Hearing Sounds to Recognizing Phonemes: Primary Auditory Cortex is A Truly Perceptual Language Area

Byron Bernal, Alfredo Ardila

1 Radiology Department/Brain Institute, Nicklaus Children’s Hospital, Miami, FL, USA;
2 Department of Communication Sciences and Disorders, Florida International University, Miami, Florida, USA

Received: , Accepted: , Published:

Topical Section: Communication and Language: Theoretical Advances in Explaining Brain Mechanisms

References

1. Dejerine J (1914) Semiologie des affections du systeme nerveux. Paris: Masson.

2. Goldstein K (1948) Language and language disturbances. New York: Grune & Stratton

3. Head H (1926) Aphasia and kindred disorders of speech. London: Cambridge University Press.

4. Pick A (1931) Aphasia. Springfiedl, Ill: Charles C. Thomas.

5. Luria AR (1962) Higher Cortical Functions in Man. Moscow University Press.

6. Luria AR (1970) Traumatic Aphasia: Its Syndromes, Psychology, and Treatment. Mouton de Gruyter.

7. Luria AR (1973) The Working Brain. Basic Books.

8. Luria AR (1976) Basic Problems in Neurolinguistics. New York: Mouton.

9. Penfield W, Rasmussen T (1952) The cerebral cortex of man. MacMillan Company.

10. Penfield W, Jaspers HH (1954) Epilepsy and the functional anatomy of the human brain. Boston: Little Brown

11. Ojemann GA (1983) Brain organization for language from the perspective of electrical stimulation mapping. Behav Brain Sci 6: 189-206.    

12. Price CJ (2010) The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 1191: 62-88.    

13. Gernsbacher MA, Kaschak MP (2003) Neuroimaging studies of language production and comprehension. An Rev Psychol 54: 91

14. Ardila A (2014) Aphasia Handbook. Miami, FL: Florida International University

15. Benson DF (1979) Aphasia, alexia and agraphia. New York: Churchill Livingstone.

16. Bogen JE, Bogen GM (1976) Wernicke’s Region–where is it? Ann N Y Acad Sci 280: 834-843.    

17. DeWitt I, Rauschecker JP (2013) Wernicke’s area revisited: parallel streams and word processing. Brain Lang 127: 181-191.    

18. Dronkers NF, Redfern BB, Knight RT (2000) The neural architecture of language disorders. New Cogn Neurosci 2: 949-958.

19. Dronkers NF, Plaisant O, Iba-Zizen MT, Cabanis EA (2007) Paul Broca’s historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain 130: 1432-1441.    

20. Grodzinsky Y, Santi A (2008) The battle for Broca’s region. Trends Cogn Sci 12: 474-480.    

21. Bernal B, Ardila A, Rosselli M (2015) Broca’s area network in language function: A pooling-data connectivity study. Front Psycho 6: 687.

22. Ardila A, Bernal B, Rosselli M (2014) Participation of the insula in language revisited: A meta-analytic connectivity study. J Neuroling 29: 31-41.    

23. Ardila A, Bernal B, Rosselli M (2015) Language and visual perception associations: Meta-analytic connectivity modeling of Brodmann area 37. Behav Neurol 2015: 565871

24. Ardila A, Bernal B, Rosselli M (2016) How localized are language brain areas? A review of Brodmann areas involvement in language. Arch Clin Neuropsychol 31: 112-122.

25. Brannon EM, Cabeza R, Huettel SA, et al. (2008) Principles of cognitive. Neuroscience 3: 757. Sunderland, MA: Sinauer Associates.

26. Pulvermüller F, Fadiga L (2010) Active perception: sensorimotor circuits as a cortical basis for language. Nature Rev Neurosci 11: 351-360.    

27. Clark J, Yallop C (1995) An Introduction to Phonetics and Phonology. Blackwell

28. Cammoun L, Thiran J P, Griffa A, et al. (2014) Intrahemispheric cortico-cortical connections of the human auditory cortex. Brain Struct Funct 220: 3537-3553.

29. Upadhyay J, Silver A, Knaus TA, et al. (2008) Effective and structural connectivity in the human auditory cortex. J Neurosc 28: 3341-3349.    

30. Bitan T, Lifshitz A, Breznitz Z, et al. (2010) Bidirectional connectivity between hemispheres occurs at multiple levels in language processing but depends on sex. J Neurosci 30: 11576-11585.    

31. Patel RS, Bowman FD, Rilling JK (2006) Determining hierarchical functional networks from auditory stimuli fMRI. Hum Brain Map 27: 462-470.    

32. Eckert MA, Kamdar NV, Chang CE, et al. (2008) A cross‐modal system linking primary auditory and visual cortices: Evidence from intrinsic fMRI connectivity analysis. Hum Brain Map 29: 848-857.    

33. Shams L, Ma WJ, Beierholm U (2005) Sound-induced flash illusion as an optimal percept. Neuroreport 16: 1923-1927.    

34. Balz J, Keil J, Romero YR, et al. (2016) GABA concentration in superior temporal sulcus predicts gamma power and perception in the sound-induced flash illusion. NeuroImage 125: 724-730.    

35. Bilecen D, Scheffler K, Schmid N, et al. (1998) Tonotopic organization of the human auditory cortex as detected by BOLD-FMRI. Hear Res 126: 19-27.    

36. Da Costa S, Saenz M, Clarke S, et al. (2015) Tonotopic gradients in human primary auditory cortex: concurring evidence from high-resolution 7 T and 3 T fMRI. Brain Top 28: 66-69.    

37. Humphries C, Liebenthal E, Binder JR (2010) Tonotopic organization of human auditory cortex. Neuroimage 50: 1202-1211.    

38. Dorsaint-Pierre R, Penhune VB, Watkins KE, et al. (2006) Asymmetries of the planum temporale and Heschl’s gyrus: relationship to language lateralization. Brain 129: 1164-1176.    

39. Zatorre RJ (2001) Neural specializations for tonal processing. Ann N Y Acad Sci 930: 193-210.

40. Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Ce Cortex 11: 946-953.    

41. Zatorre RJ, Belin P, Penhune VB (2002) Structure and function of auditory cortex: music and speech. Trends Cogn Scien 6: 37-46.    

42. Schomers MR, Pulvermüller F (2016) Is the sensorimotor cortex relevant for speech perception and understanding? An integrative review. Front Hum Neurosc 10.

43. Glick H, Sharma A (2016) Cross-modal Plasticity in Developmental and Age-Related Hearing Loss: Clinical Implications. Hear Res.

44. Specht K, Baumgartner F, Stadler J, et al. (2014). Functional asymmetry and effective connectivity of the auditory system during speech perception is modulated by the place of articulation of the consonant-A 7T fMRI study. Front Psychol 5.

45. Menéndez-Colino LM, Falcón C, Traserra J, et al. (2007) Activation patterns of the primary auditory cortex in normal-hearing subjects: a functional magnetic resonance imaging study. Acta oto-laryngol 127: 1283-1291.    

46. Lasota KJ, Ulmer JL, Firszt JB, et al. (2003) Intensity-dependent activation of the primary auditory cortex in functional magnetic resonance imaging. J Comp Assist Tom 27: 213-218.    

47. Yetkin FZ, Wolberg SC, Temlett JA, et al. (1990) Pure word deafness. South Afric Med J 78: 668-670.

48. Stefanatos GA, Joe WQ, Aguirre GK, et al. (2008) Activation of human auditory cortex during speech perception: effects of monaural, binaural, and dichotic presentation. Neuropsychologia 46: 301-315.    

49. Alain C, Reinke K, McDonald KL, et al. (2005) Left thalamo-cortical network implicated in successful speech separation and identification. Neuroimage 26: 592-599.    

50. Liebenthal E, Binder JR, Spitzer SM et al. (2005) Neural substrates of phonemic perception. Cereb Cortex 15: 1621-1631.    

51. Hall DA, Johnsrude IS, Haggard MP, et al. (2002) Spectral and temporal processing in human auditory cortex. Cereb Cortex 12: 140-149.    

52. Hart HC, Hall DA, Palmer AR (2003) The sound-level-dependent growth in the extent of fMRI activation in Heschl’s gyrus is different for low-and high-frequency tones. Hear Res 179: 104-112.    

53. Patterson RD, Uppenkamp S, Johnsrude IS, et al. (2002) The processing of temporal pitch and melody information in auditory cortex. Neuron 36: 767-776.    

54. Obleser J, Boecker H, Drzezga A, et al. (2006) Vowel sound extraction in anterior superior temporal cortex. Hum Brain Map 27: 562-571.    

55. Izumi S, Itoh K, Matsuzawa H, et al. (2011) Functional asymmetry in primary auditory cortex for processing musical sounds: temporal pattern analysis of fMRI time series. Neuroreport 22: 470-473.    

56. Da Costa S, van der Zwaag W, Miller LM et al. (2013) Tuning in to sound: frequency-selective attentional filter in human primary auditory cortex. J Neurosc 33: 1858-1863.    

57. Calvert G, Campbell R (2003) Reading speech from still and moving faces: the neural substrates of visible speech. Cogn Neurosci J 15: 57-70.    

58. Wiegand K, Gutschalk A (2012) Correlates of perceptual awareness in human primary auditory cortex revealed by an informational masking experiment. Neuroimage 61: 62-69.    

59. Benoit MM, Raij T, Lin FH, et al. (2010) Primary and multisensory cortical activity is correlated with audiovisual percepts. Hum Brain Map 31: 526-538.

60. Friederici AD, Meyer M, von Cramon DY (2000) Auditory language comprehension: an event-related fMRI study on the processing of syntactic and lexical information. Brain Lang 74: 289-300.    

61. Deschamps I, Tremblay P (2014) Sequencing at the syllabic and supra-syllabic levels during speech perception: an fMRI study. Front Hum Neurosci 8.

62. Stoppelman N, Harpaz T, Ben‐Shachar M (2013) Do not throw out the baby with the bath water: choosing an effective baseline for a functional localizer of speech processing. Brain Behav 3: 211-222.    

63. Belin P, Zatorre RJ, Ahad P (2002) Human temporal-lobe response to vocal sounds. Cogn Brain Res 13: 17-26.    

64. Conant LL, Liebenthal E, Desai A, et al. (2014) FMRI of phonemic perception and its relationship to reading development in elementary-to middle-school-age children. Neuroimage 89: 192-202.

65. Ardila A (1993) Toward a model of phoneme perception. Int J Neurosc 70: 1-12.    

66. Nygaard C, Pisoni DB (1995) Speech Perception: New Directions in Research and Theory. In JL Miller, PD Eimas. Handbook of Perception and Cognition: Speech, Language, and Communication. San Diego: Academic Press.

67. Lin CY, Wang HC (2011) Automatic estimation of voice onset time for word-initial stops by applying random forest to onset detection. J Acooust Soc Amer 130: 514-525.    

68. Zaehle T, Jancke L, Meyer M (2007) Electrical brain imaging evidences left auditory cortex involvement in speech and non-speech discrimination based on temporal features. Behav Brain Funct 3: 63.    

69. Boatman D, Hart J, Lesser RP, et al. (1998) Right hemisphere speech perception revealed by amobarbital injection and electrical interference. Neurology 51: 458-464.    

70. Specht K (2014) Neuronal basis of speech comprehension. Hear Res 307: 121-135.    

71. Basso A (2003) Aphasia and its therapy. New York: Oxford University Press.

72. Ardila, A (2010) A proposed reinterpretation and reclassification of aphasic syndromes. Aphasiology 24: 363-394.    

73. Benson DF, Ardila A (1996) Aphasia: A clinical perspective. New York: Oxford University Press.

74. Gandour J, Dzemidzic M, Wong D, et al. (2003) Temporal integration of speech prosody is shaped by language experience: An fMRI study. Brain Lang 84: 318-336.    

75. Ulrich G (1978) Interhemispheric functional relationships in auditory agnosia: an analysis of the preconditions and a conceptual model. Brain Lang 5: 286-300.    

76. Ackermann H, Mathiak K (1999) Symptomatologie, pathologischanatomische Grundlaqen und Pathomechanismen zentraler Hörstörungen (reine Worttaubheit, auditive Agnosie, Rindentaubheit). Fortschritte Neurole·Psychiatr 67: 509-523.

77. Poeppel D (2001) Pure word deafness and the bilateral processing of the speech code. Cogn Sci 25: 679-693.    

78. Takahashi N, Kawamura M, Shinotou H. et al. (1992) Pure word deafness due to left hemisphere damage. Cortex 28: 295-303.

79. Kussmaul A (1877) Disturbances of speech. In H. von Ziemssen (Ed.), Enyclopedia of the practice of medicine. New York: William Wood.

80. Auerbach SH, Allard T, Naeser M, et al. (1982) Pure word deafness. Analysis of a case with bilateral lesions and a defect at the prephonemic level. Brain 105: 271-300.

81. Feldmann H (2004) 200 years testing hearing disorders with speech, 50 years German speech audiometry—a review. Laryngo-rhino-otologie 83: 735-742.    

82. Brody RM, Nicholas BD, Wolf MJ, et al. (2013) Cortical deafness: a case report and review of the literature. Otol Neurotol 34: 1226-1229.    

83. Caramazza A, Berndt RS, Basili AG (1983) The selective impairment of phonological processing: A case study. Brain Lang 18: 128-174.    

84. Molfese DL, Molfese VJ, Espy KA (1999) The predictive use of event-related potentials in language development and the treatment of language disorders. Dev Neuropsychol 16: 373-377.    

85. Eimas PD (1999) Segmental and syllabic representations in the perception of speech by young infants. J Acoust Soc Amer 105: 1901-1911.    

86. Vannest JJ, Karunanayaka PR, Altaye M, et al. (2009) Comparison of fMRI data from passive listening and active—response story processing tasks in children. J Magn Res Imaging 29: 971-976.    

87. Ashtari M, Lencz T, Zuffante P, et al. (2004) Left middle temporal gyrus activation during a phonemic discrimination task. Neuroreport 15: 389-393.    

88. Dean III DC, Dirks H, O’Muircheartaigh J, et al. (2014) Pediatric neuroimaging using magnetic resonance imaging during non-sedated sleep. Ped Radiol 44: 64-72.    

89. Dehaene-Lambertz G, Dehaene S, Hertz-Pannier L (2002) Functional neuroimaging of speech perception in infants. Science 298: 2013-2015.    

90. Altman NR, Bernal B (2001) Brain Activation in Sedated Children: Auditory and Visual Functional MR Imaging 1. Radiology 221: 56-63.    

91. Gemma M, de Vitis A, Baldoli C, et al. (2009) Functional magnetic resonance imaging (fMRI) in children sedated with propofol or midazolam. J Neurosurg Anesthesiol 21: 253-258.    

92. Dobrunz UEG, Jaeger K, Vetter G (2007) Memory priming during light anaesthesia with desflurane and remifentanil anaesthesia. Br J Anaesthesia 98: 491-496.    

93. Ford JM, Dierks T, Fisher DJ, et al. (2012) Neurophysiological studies of auditory verbal hallucinations. Schiz Bull 38: 715-723. www.fmriconsulting.com/brodmannconn/index.php?q=BA_41    

94. Taylor RL, Campbell GT (1976) Sensory interaction: Vision is modulated by hearing. Perception 5: 467.    

95. Poirier C, Collignon O, DeVolder AG, et al. (2005) Specific activation of the V5 brain area by auditory motion processing: an fMRI study. Cogn Brain Res 25: 650-658.    

96. Poirier C, Collignon O, Scheiber C, et al. (2006) Auditory motion perception activates visual motion areas in early blind subjects. Neuroimage 31: 279-285.    

97. Collignon O, Dormal G, Albouy G, et al. (2013) Impact of blindness onset on the functional organization and the connectivity of the occipital cortex. Brain 136: 2769-2783.    

98. De Volder AG, Toyama H, Kimura Y, et al. (2001) Auditory triggered mental imagery of shape involves visual association areas in early blind humans. Neuroimage 14: 129-139.    

99. Finney EM, Fine I, Dobkins KR (2001) Visual stimuli activate auditory cortex in the deaf. Nature Neurosci 4: 1171-1173.    

100. Shiell MM, Champoux F, Zatorre RJ (2015) Reorganization of auditory cortex in early-deaf people: Functional connectivity and relationship to hearing aid use. J Cogn Neurosci 27: 150-163.    

101. Flemming ES (2013) Auditory representations in phonology. Routledge.

102. McGurk H, MacDonald J (1976) Hearing lips and seeing voices. Nature 264: 746-748.

103. Burton MW, LoCasto PC, Krebs-Noble D, et al. (2005) A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing. Neuroimage 26: 647-661.    

104. Longoni F, Grande M, Hendrich V, et al. (2005) An fMRI study on conceptual, grammatical, and morpho-phonological processing. Brain Cogn 57: 131-134.    

105. Cammoun L, Thiran JP, Griffa A, et al. (2014) Intrahemispheric cortico-cortical connections of the human auditory cortex. Brain Struct Function: 1-17.

106. Upadhyay J, Ducros M, Knaus TA, et al. (2007) Function and connectivity in human primary auditory cortex: a combined fMRI and DTI study at 3 Tesla. Cereb Cortex 17: 2420-2432.    

107. Saur D, Kreher BW, Schnell S, et al. (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci U S A 105: 18035-18040.    

108. Ardila A (2011) There are two different language systems in the brain. J Behav Brain Sci 1: 23.    

109. Ardila A (2012) Interaction between lexical and grammatical language systems in the brain. Phys Life Rev 9: 198-214.    

110. Duffau H, Gatignol P, Mandonnet E, et al. (2008) Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 109: 461-471.    

111. Bernal B, Ardila A (2009) The role of the arcuate fasciculus in conduction aphasia. Brain 132: 2309-2316.    

112. Brewer AA, Barton B (2016) Maps of the Auditory Cortex. An Rev Neurosci 39: 385-407.

113. Manca AD, Grimaldi M (2016) Vowels and Consonants in the Brain: Evidence from Magnetoencephalographic Studies on the N1m in Normal-Hearing Listeners. Front Psychol 7.

114. Caclin A, Fonlupt P (2006) Functional and effective connectivity in an Fmri study of an auditory‐related task. Eur J Neurosc 23: 2531-2537.    

115. Binder JR, Frost JA, Hammeke TA et al. (2000) Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex 10: 512-528.    

116. Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8: 393-402.

117. Vigneau M, Beaucousin V, Herve PY, et al. (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30: 1414-1432.    

118. Tervaniemi M, Hugdahl K (2003) Lateralization of auditory-cortex functions. Brain Res Rev 43: 231-246.    

119. Zhang L, Xi J, Xu G, et al. (2011) Cortical dynamics of acoustic and phonological processing in speech perception. PloS one 6: e20963.    

120. Bernal B, Ardila A (2014) Bilateral representation of language: A critical review and analysis of some unusual cases. J Neuroling 28: 63-80.    

Copyright Info: © 2016, Alfredo Ardila, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)