Brain Structure and Function

, Volume 219, Issue 4, pp 1369–1383 | Cite as

Mapping phonemic processing zones along human perisylvian cortex: an electro-corticographic investigation

  • Sophie Molholm
  • Manuel R. Mercier
  • Einat Liebenthal
  • Theodore H. Schwartz
  • Walter Ritter
  • John J. Foxe
  • Pierfilippo De Sanctis
Original Article

Abstract

The auditory system is organized such that progressively more complex features are represented across successive cortical hierarchical stages. Just when and where the processing of phonemes, fundamental elements of the speech signal, is achieved in this hierarchy remains a matter of vigorous debate. Non-invasive measures of phonemic representation have been somewhat equivocal. While some studies point to a primary role for middle/anterior regions of the superior temporal gyrus (STG), others implicate the posterior STG. Differences in stimulation, task and inter-individual anatomical/functional variability may account for these discrepant findings. Here, we sought to clarify this issue by mapping phonemic representation across left perisylvian cortex, taking advantage of the excellent sampling density afforded by intracranial recordings in humans. We asked whether one or both major divisions of the STG were sensitive to phonemic transitions. The high signal-to-noise characteristics of direct intracranial recordings allowed for analysis at the individual participant level, circumventing issues of inter-individual anatomic and functional variability that may have obscured previous findings at the group level of analysis. The mismatch negativity (MMN), an electrophysiological response elicited by changes in repetitive streams of stimulation, served as our primary dependent measure. Oddball configurations of pairs of phonemes, spectro-temporally matched non-phonemes, and simple tones were presented. The loci of the MMN clearly differed as a function of stimulus type. Phoneme representation was most robust over middle/anterior STG/STS, but was also observed over posterior STG/SMG. These data point to multiple phonemic processing zones along perisylvian cortex, both anterior and posterior to primary auditory cortex. This finding is considered within the context of a dual stream model of auditory processing in which functionally distinct ventral and dorsal auditory processing pathways may be engaged by speech stimuli.

Keywords

ECog Phoneme Superior temporal gyrus Auditory Speech processing Intracranial 

Notes

Acknowledgments

The authors wish to express their sincere appreciation to the participants who kindly donated their time to this project, to Mr. Jason Adler for his contribution to the analysis of data, and to Ms. Edel Flynn for assistance with manuscript formatting. SM and JJF received support from NIMH (MH 85322) and a grant from the Nathan Gancher Foundation, and MM from the Swiss National Science Foundation (PBELP3-123067).

Supplementary material

429_2013_574_MOESM1_ESM.tif (419 kb)
Supplementary material 1 (TIFF 419 kb)

References

  1. Abdul-Kareem IA, Sluming V (2008) Heschl gyrus and its included primary auditory cortex: structural MRI studies in healthy and diseased subjects. J Magn Reson Imaging 28(2):287–299PubMedCrossRefGoogle Scholar
  2. Allison T, Puce A et al (1999) Electrophysiological studies of human face perception. I: potentials generated in occipitotemporal cortex by face and non-face stimuli. Cereb Cortex 9(5):415–430PubMedCrossRefGoogle Scholar
  3. Amenedo E, Escera C (2000) The accuracy of sound duration representation in the human brain determines the accuracy of behavioral perception. Eur J Neurosci 12(7):2570–2574PubMedCrossRefGoogle Scholar
  4. Beauchamp MS (2005) See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex. Curr Opin Neurobiol 15(2):145–153PubMedCrossRefGoogle Scholar
  5. Butler JS, Molholm S et al (2011) Common or redundant neural circuits for duration processing across audition and touch. J Neurosci 31(9):3400–3406PubMedCentralPubMedCrossRefGoogle Scholar
  6. Calvert GA, Thesen T (2004) Multisensory integration: methodological approaches and emerging principles in the human brain. J Physiol Paris 98(1–3):191–205PubMedCrossRefGoogle Scholar
  7. Chang EF, Rieger JW, Johnson K, Berger MS, Barbaro NM, Knight RT (2010) Categorical speech representation in human superior temporal gyrus. Nat Neurosci 13(11):1428–1432PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chevillet M, Riesenhuber M et al (2011) Functional correlates of the anterolateral processing hierarchy in human auditory cortex. J Neurosci 31(25):9345–9352PubMedCentralPubMedCrossRefGoogle Scholar
  9. De Sanctis P, Molholm S et al (2009) Right hemispheric contributions to fine auditory temporal discriminations: high-density electrical mapping of the duration mismatch negativity (MMN). Front Integr Neurosci 3:5PubMedCentralPubMedCrossRefGoogle Scholar
  10. Desai R, Liebenthal E et al (2005) Volumetric vs. surface-based alignment for localization of auditory cortex activation. Neuroimage 26(4):1019–1029PubMedCrossRefGoogle Scholar
  11. Desai R, Liebenthal E et al (2008) Left posterior temporal regions are sensitive to auditory categorization. J Cogn Neurosci 20(7):1174–1188PubMedCentralPubMedCrossRefGoogle Scholar
  12. DeWitt I, Rauschecker JP (2012) Phoneme and word recognition in the auditory ventral stream. Proc Natl Acad Sci USA 109(8):E505–E514PubMedCentralPubMedCrossRefGoogle Scholar
  13. Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601PubMedCrossRefGoogle Scholar
  14. Fedorenko E, Kanwisher N (2011) Some regions within Broca’s area do respond more strongly to sentences than to linguistically degraded stimuli: a comment on Rogalsky and Hickok (2011). J Cogn Neurosci 23(10):2632–2635CrossRefGoogle Scholar
  15. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47PubMedCrossRefGoogle Scholar
  16. Fishman YI, Steinschneider M (2010) Neural correlates of auditory scene analysis based on inharmonicity in monkey primary auditory cortex. J Neurosci 30(37):12480–12494PubMedCentralPubMedCrossRefGoogle Scholar
  17. Flinker A, Chang EF et al (2011) Sub-centimeter language organization in the human temporal lobe. Brain Lang 117(3):103–109PubMedCentralPubMedCrossRefGoogle Scholar
  18. Guthrie D, Buchwald JS (1991) Significance testing of difference potentials. Psychophysiology 28(2):240–244PubMedCrossRefGoogle Scholar
  19. Hackett TA (2011) Information flow in the auditory cortical network. Hear Res 271(1–2):133–146PubMedCentralPubMedCrossRefGoogle Scholar
  20. Hasson U, Levy I et al (2002) Eccentricity bias as an organizing principle for human high-order object areas. Neuron 34(3):479–490PubMedCrossRefGoogle Scholar
  21. Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402PubMedCrossRefGoogle Scholar
  22. Ide A, Rodriguez E et al (1996) Bifurcation patterns in the human sylvian fissure: hemispheric and sex differences. Cereb Cortex 6(5):717–725PubMedCrossRefGoogle Scholar
  23. Kang X, Bertrand O et al (2004) Local landmark-based mapping of human auditory cortex. Neuroimage 22(4):1657–1670PubMedCrossRefGoogle Scholar
  24. Kanwisher N, McDermott J et al (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17(11):4302–4311PubMedGoogle Scholar
  25. Leavitt VM, Molholm S et al (2011) “What” and “where” in auditory sensory processing: a high-density electrical mapping study of distinct neural processes underlying sound object recognition and sound localization. Front Integr Neurosci 5:23PubMedCentralPubMedCrossRefGoogle Scholar
  26. Leech R, Holt LL et al (2009) Expertise with artificial nonspeech sounds recruits speech-sensitive cortical regions. J Neurosci 29(16):5234–5239PubMedCentralPubMedCrossRefGoogle Scholar
  27. Liebenthal E, Binder JR et al (2005) Neural substrates of phonemic perception. Cereb Cortex 15(10):1621–1631PubMedCrossRefGoogle Scholar
  28. Liebenthal E, Desai R et al (2010) Specialization along the left superior temporal sulcus for auditory categorization. Cereb Cortex 20(12):2958–2970PubMedCentralPubMedCrossRefGoogle Scholar
  29. Lucan JN, Foxe JJ et al (2010) Tactile shape discrimination recruits human lateral occipital complex during early perceptual processing. Hum Brain Mapp 31(11):1813–1821PubMedGoogle Scholar
  30. McKeeff TJ, McGugin RW et al (2010) Expertise increases the functional overlap between face and object perception. Cognition 117(3):355–360PubMedCentralPubMedCrossRefGoogle Scholar
  31. Molholm S, Martinez A et al (2005) The neural circuitry of pre-attentive auditory change-detection: an fMRI study of pitch and duration mismatch negativity generators. Cereb Cortex 15(5):545–551PubMedCrossRefGoogle Scholar
  32. Näätänen R (1992) Attention and brain function. Lawrence Erlbaum Associates, NJ, HillsdaleGoogle Scholar
  33. Naatanen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24(4):375–425PubMedCrossRefGoogle Scholar
  34. Näätänen R, Paavilainen P et al (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118(12):2544–2590PubMedCrossRefGoogle Scholar
  35. Obleser J, Eisner F (2009) Pre-lexical abstraction of speech in the auditory cortex. Trends Cogn Sci 13(1):14–19PubMedCrossRefGoogle Scholar
  36. Obleser J, Zimmerman J et al (2007) Multiple stages of auditory speech perception reflected in event-related FMRI. Cereb Cortex 17(10):2251–2257PubMedCrossRefGoogle Scholar
  37. Obleser J, Leaver AM et al (2010) Segregation of vowels and consonants in human auditory cortex: evidence for distributed hierarchical organization. Front Psychol 1:232PubMedCentralPubMedCrossRefGoogle Scholar
  38. Okada K, Rong F et al (2010) Hierarchical organization of human auditory cortex: evidence from acoustic invariance in the response to intelligible speech. Cereb Cortex 20(10):2486–2495PubMedCentralPubMedCrossRefGoogle Scholar
  39. Oostenveld R, Fries P et al (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869PubMedCentralPubMedCrossRefGoogle Scholar
  40. Orlov T, Makin TR et al (2010) Topographic representation of the human body in the occipitotemporal cortex. Neuron 68(3):586–600PubMedCrossRefGoogle Scholar
  41. Osnes B, Hugdahl K et al (2011) Increased activation in superior temporal gyri as a function of increment in phonetic features. Brain Lang 116(2):97–101PubMedCrossRefGoogle Scholar
  42. Peelle JE, Johnsrude IS et al (2010) Hierarchical processing for speech in human auditory cortex and beyond. Front Hum Neurosci 4:51PubMedCentralPubMedGoogle Scholar
  43. Picton TW, Alain C et al (2000) Mismatch negativity: different water in the same river. Audiol Neurootol 5(3–4):111–139PubMedCrossRefGoogle Scholar
  44. Pourtois G, Peelen MV et al (2007) Direct intracranial recording of body-selective responses in human extrastriate visual cortex. Neuropsychologia 45(11):2621–2625PubMedCrossRefGoogle Scholar
  45. Pourtois G, Spinelli L et al (2010) Modulation of face processing by emotional expression and gaze direction during intracranial recordings in right fusiform cortex. J Cogn Neurosci 22(9):2086–2107PubMedCrossRefGoogle Scholar
  46. Rademacher J, Burgel U et al (2002) Stereotaxic localization, intersubject variability, and interhemispheric differences of the human auditory thalamocortical system. Neuroimage 17(1):142–160PubMedCrossRefGoogle Scholar
  47. Raizada RD, Poldrack RA (2007) Selective amplification of stimulus differences during categorical processing of speech. Neuron 56(4):726–740PubMedCrossRefGoogle Scholar
  48. Rauschecker JP (1998) Cortical processing of complex sounds. Curr Opin Neurobiol 8(4):516–521PubMedCrossRefGoogle Scholar
  49. Rauschecker JP (2012) Ventral and dorsal streams in the evolution of speech and language. Front Evolut Neurosci 4:7Google Scholar
  50. Ritter W, Paavilainen P et al (1992) Event-related potentials to repetition and change of auditory stimuli. Electroencephalogr Clin Neurophysiol 83(5):306–321PubMedCrossRefGoogle Scholar
  51. Roland PE, Zilles K (1998) Structural divisions and functional fields in the human cerebral cortex. Brain Res Brain Res Rev 26(2–3):87–105PubMedCrossRefGoogle Scholar
  52. Saint-Amour D, De Sanctis P et al (2007) Seeing voices: high-density electrical mapping and source-analysis of the multisensory mismatch negativity evoked during the McGurk illusion. Neuropsychologia 45(3):587–597PubMedCentralPubMedCrossRefGoogle Scholar
  53. Scott SK, Johnsrude IS (2003) The neuroanatomical and functional organization of speech perception. Trends Neurosci 26(2):100–107PubMedCrossRefGoogle Scholar
  54. Sehatpour P, Molholm S et al (2008) A human intracranial study of long-range oscillatory coherence across a frontal-occipital-hippocampal brain network during visual object processing. Proc Natl Acad Sci USA 105(11):4399–4404PubMedCentralPubMedCrossRefGoogle Scholar
  55. Steinschneider M, Nourski KV et al (2011) Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex 21(10):2332–2347PubMedCentralPubMedCrossRefGoogle Scholar
  56. Turkeltaub PE, Coslett HB (2010) Localization of sublexical speech perception components. Brain Lang 114(1):1–15PubMedCentralPubMedCrossRefGoogle Scholar
  57. Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. J Neurosurg 106(6):1117–1133CrossRefGoogle Scholar
  58. Wise RJ, Scott SK et al (2001) Separate neural subsystems within ‘Wernicke’s area’. Brain 124(Pt 1):83–95PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Sophie Molholm
    • 1
    • 2
  • Manuel R. Mercier
    • 1
  • Einat Liebenthal
    • 3
  • Theodore H. Schwartz
    • 4
  • Walter Ritter
    • 1
  • John J. Foxe
    • 1
    • 2
  • Pierfilippo De Sanctis
    • 1
  1. 1.The Sheryl and Daniel R. Tishman Cognitive Neurophysiology Laboratory, Departments of Pediatrics and NeuroscienceChildren’s Evaluation and Rehabilitation Center (CERC), Albert Einstein College of MedicineBronxUSA
  2. 2.The Cognitive Neurophysiology LaboratoryThe Nathan S. Kline Institute for Psychiatric ResearchOrangeburgUSA
  3. 3.Department of NeurologyMedical College of WisconsinMilwaukeeUSA
  4. 4.Department of Neurological SurgeryWeill Cornell Medical College, New York Presbyterian HospitalNew YorkUSA

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