Skip to main content
Top
Published in: Brain Structure and Function 4/2014

01-07-2014 | Original Article

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

Authors: Sophie Molholm, Manuel R. Mercier, Einat Liebenthal, Theodore H. Schwartz, Walter Ritter, John J. Foxe, Pierfilippo De Sanctis

Published in: Brain Structure and Function | Issue 4/2014

Login to get access

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.
Appendix
Available only for authorised users
Footnotes
1
We reanalyzed our data without the low-pass filter and found no differences between filtered (30 Hz) and unfiltered data with regard to the statistical results for the MMNs. Data from the original analyses are presented.
 
Literature
go back to reference 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):287–299PubMedCrossRef 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):287–299PubMedCrossRef
go back to reference 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):415–430PubMedCrossRef 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):415–430PubMedCrossRef
go back to reference 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):2570–2574PubMedCrossRef 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):2570–2574PubMedCrossRef
go back to reference Beauchamp MS (2005) See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex. Curr Opin Neurobiol 15(2):145–153PubMedCrossRef Beauchamp MS (2005) See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex. Curr Opin Neurobiol 15(2):145–153PubMedCrossRef
go back to reference Calvert GA, Thesen T (2004) Multisensory integration: methodological approaches and emerging principles in the human brain. J Physiol Paris 98(1–3):191–205PubMedCrossRef Calvert GA, Thesen T (2004) Multisensory integration: methodological approaches and emerging principles in the human brain. J Physiol Paris 98(1–3):191–205PubMedCrossRef
go back to reference 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):1428–1432PubMedCentralPubMedCrossRef 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):1428–1432PubMedCentralPubMedCrossRef
go back to reference Chevillet M, Riesenhuber M et al (2011) Functional correlates of the anterolateral processing hierarchy in human auditory cortex. J Neurosci 31(25):9345–9352PubMedCentralPubMedCrossRef Chevillet M, Riesenhuber M et al (2011) Functional correlates of the anterolateral processing hierarchy in human auditory cortex. J Neurosci 31(25):9345–9352PubMedCentralPubMedCrossRef
go back to reference 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 3:5PubMedCentralPubMedCrossRef 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 3:5PubMedCentralPubMedCrossRef
go back to reference Desai R, Liebenthal E et al (2005) Volumetric vs. surface-based alignment for localization of auditory cortex activation. Neuroimage 26(4):1019–1029PubMedCrossRef Desai R, Liebenthal E et al (2005) Volumetric vs. surface-based alignment for localization of auditory cortex activation. Neuroimage 26(4):1019–1029PubMedCrossRef
go back to reference Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601PubMedCrossRef Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601PubMedCrossRef
go back to reference 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):2632–2635CrossRef 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):2632–2635CrossRef
go back to reference Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47PubMedCrossRef Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47PubMedCrossRef
go back to reference Fishman YI, Steinschneider M (2010) Neural correlates of auditory scene analysis based on inharmonicity in monkey primary auditory cortex. J Neurosci 30(37):12480–12494PubMedCentralPubMedCrossRef Fishman YI, Steinschneider M (2010) Neural correlates of auditory scene analysis based on inharmonicity in monkey primary auditory cortex. J Neurosci 30(37):12480–12494PubMedCentralPubMedCrossRef
go back to reference Guthrie D, Buchwald JS (1991) Significance testing of difference potentials. Psychophysiology 28(2):240–244PubMedCrossRef Guthrie D, Buchwald JS (1991) Significance testing of difference potentials. Psychophysiology 28(2):240–244PubMedCrossRef
go back to reference Hasson U, Levy I et al (2002) Eccentricity bias as an organizing principle for human high-order object areas. Neuron 34(3):479–490PubMedCrossRef Hasson U, Levy I et al (2002) Eccentricity bias as an organizing principle for human high-order object areas. Neuron 34(3):479–490PubMedCrossRef
go back to reference Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402PubMedCrossRef Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402PubMedCrossRef
go back to reference Ide A, Rodriguez E et al (1996) Bifurcation patterns in the human sylvian fissure: hemispheric and sex differences. Cereb Cortex 6(5):717–725PubMedCrossRef Ide A, Rodriguez E et al (1996) Bifurcation patterns in the human sylvian fissure: hemispheric and sex differences. Cereb Cortex 6(5):717–725PubMedCrossRef
go back to reference Kang X, Bertrand O et al (2004) Local landmark-based mapping of human auditory cortex. Neuroimage 22(4):1657–1670PubMedCrossRef Kang X, Bertrand O et al (2004) Local landmark-based mapping of human auditory cortex. Neuroimage 22(4):1657–1670PubMedCrossRef
go back to reference 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):4302–4311PubMed 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):4302–4311PubMed
go back to reference 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 5:23PubMedCentralPubMedCrossRef 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 5:23PubMedCentralPubMedCrossRef
go back to reference Liebenthal E, Binder JR et al (2005) Neural substrates of phonemic perception. Cereb Cortex 15(10):1621–1631PubMedCrossRef Liebenthal E, Binder JR et al (2005) Neural substrates of phonemic perception. Cereb Cortex 15(10):1621–1631PubMedCrossRef
go back to reference Lucan JN, Foxe JJ et al (2010) Tactile shape discrimination recruits human lateral occipital complex during early perceptual processing. Hum Brain Mapp 31(11):1813–1821PubMed Lucan JN, Foxe JJ et al (2010) Tactile shape discrimination recruits human lateral occipital complex during early perceptual processing. Hum Brain Mapp 31(11):1813–1821PubMed
go back to reference 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):545–551PubMedCrossRef 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):545–551PubMedCrossRef
go back to reference Näätänen R (1992) Attention and brain function. Lawrence Erlbaum Associates, NJ, Hillsdale Näätänen R (1992) Attention and brain function. Lawrence Erlbaum Associates, NJ, Hillsdale
go back to reference 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):375–425PubMedCrossRef 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):375–425PubMedCrossRef
go back to reference Näätänen R, Paavilainen P et al (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118(12):2544–2590PubMedCrossRef Näätänen R, Paavilainen P et al (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118(12):2544–2590PubMedCrossRef
go back to reference Obleser J, Eisner F (2009) Pre-lexical abstraction of speech in the auditory cortex. Trends Cogn Sci 13(1):14–19PubMedCrossRef Obleser J, Eisner F (2009) Pre-lexical abstraction of speech in the auditory cortex. Trends Cogn Sci 13(1):14–19PubMedCrossRef
go back to reference Obleser J, Zimmerman J et al (2007) Multiple stages of auditory speech perception reflected in event-related FMRI. Cereb Cortex 17(10):2251–2257PubMedCrossRef Obleser J, Zimmerman J et al (2007) Multiple stages of auditory speech perception reflected in event-related FMRI. Cereb Cortex 17(10):2251–2257PubMedCrossRef
go back to reference Obleser J, Leaver AM et al (2010) Segregation of vowels and consonants in human auditory cortex: evidence for distributed hierarchical organization. Front Psychol 1:232PubMedCentralPubMedCrossRef Obleser J, Leaver AM et al (2010) Segregation of vowels and consonants in human auditory cortex: evidence for distributed hierarchical organization. Front Psychol 1:232PubMedCentralPubMedCrossRef
go back to reference 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):2486–2495PubMedCentralPubMedCrossRef 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):2486–2495PubMedCentralPubMedCrossRef
go back to reference Oostenveld R, Fries P et al (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869PubMedCentralPubMedCrossRef Oostenveld R, Fries P et al (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869PubMedCentralPubMedCrossRef
go back to reference Orlov T, Makin TR et al (2010) Topographic representation of the human body in the occipitotemporal cortex. Neuron 68(3):586–600PubMedCrossRef Orlov T, Makin TR et al (2010) Topographic representation of the human body in the occipitotemporal cortex. Neuron 68(3):586–600PubMedCrossRef
go back to reference 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):97–101PubMedCrossRef 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):97–101PubMedCrossRef
go back to reference Peelle JE, Johnsrude IS et al (2010) Hierarchical processing for speech in human auditory cortex and beyond. Front Hum Neurosci 4:51PubMedCentralPubMed Peelle JE, Johnsrude IS et al (2010) Hierarchical processing for speech in human auditory cortex and beyond. Front Hum Neurosci 4:51PubMedCentralPubMed
go back to reference Picton TW, Alain C et al (2000) Mismatch negativity: different water in the same river. Audiol Neurootol 5(3–4):111–139PubMedCrossRef Picton TW, Alain C et al (2000) Mismatch negativity: different water in the same river. Audiol Neurootol 5(3–4):111–139PubMedCrossRef
go back to reference Pourtois G, Peelen MV et al (2007) Direct intracranial recording of body-selective responses in human extrastriate visual cortex. Neuropsychologia 45(11):2621–2625PubMedCrossRef Pourtois G, Peelen MV et al (2007) Direct intracranial recording of body-selective responses in human extrastriate visual cortex. Neuropsychologia 45(11):2621–2625PubMedCrossRef
go back to reference 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):2086–2107PubMedCrossRef 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):2086–2107PubMedCrossRef
go back to reference Rademacher J, Burgel U et al (2002) Stereotaxic localization, intersubject variability, and interhemispheric differences of the human auditory thalamocortical system. Neuroimage 17(1):142–160PubMedCrossRef Rademacher J, Burgel U et al (2002) Stereotaxic localization, intersubject variability, and interhemispheric differences of the human auditory thalamocortical system. Neuroimage 17(1):142–160PubMedCrossRef
go back to reference Raizada RD, Poldrack RA (2007) Selective amplification of stimulus differences during categorical processing of speech. Neuron 56(4):726–740PubMedCrossRef Raizada RD, Poldrack RA (2007) Selective amplification of stimulus differences during categorical processing of speech. Neuron 56(4):726–740PubMedCrossRef
go back to reference Rauschecker JP (2012) Ventral and dorsal streams in the evolution of speech and language. Front Evolut Neurosci 4:7 Rauschecker JP (2012) Ventral and dorsal streams in the evolution of speech and language. Front Evolut Neurosci 4:7
go back to reference Ritter W, Paavilainen P et al (1992) Event-related potentials to repetition and change of auditory stimuli. Electroencephalogr Clin Neurophysiol 83(5):306–321PubMedCrossRef Ritter W, Paavilainen P et al (1992) Event-related potentials to repetition and change of auditory stimuli. Electroencephalogr Clin Neurophysiol 83(5):306–321PubMedCrossRef
go back to reference Roland PE, Zilles K (1998) Structural divisions and functional fields in the human cerebral cortex. Brain Res Brain Res Rev 26(2–3):87–105PubMedCrossRef Roland PE, Zilles K (1998) Structural divisions and functional fields in the human cerebral cortex. Brain Res Brain Res Rev 26(2–3):87–105PubMedCrossRef
go back to reference 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):587–597PubMedCentralPubMedCrossRef 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):587–597PubMedCentralPubMedCrossRef
go back to reference Scott SK, Johnsrude IS (2003) The neuroanatomical and functional organization of speech perception. Trends Neurosci 26(2):100–107PubMedCrossRef Scott SK, Johnsrude IS (2003) The neuroanatomical and functional organization of speech perception. Trends Neurosci 26(2):100–107PubMedCrossRef
go back to reference 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):4399–4404PubMedCentralPubMedCrossRef 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):4399–4404PubMedCentralPubMedCrossRef
go back to reference Steinschneider M, Nourski KV et al (2011) Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex 21(10):2332–2347PubMedCentralPubMedCrossRef Steinschneider M, Nourski KV et al (2011) Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex 21(10):2332–2347PubMedCentralPubMedCrossRef
go back to reference Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. J Neurosurg 106(6):1117–1133CrossRef Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. J Neurosurg 106(6):1117–1133CrossRef
go back to reference Wise RJ, Scott SK et al (2001) Separate neural subsystems within ‘Wernicke’s area’. Brain 124(Pt 1):83–95PubMedCrossRef Wise RJ, Scott SK et al (2001) Separate neural subsystems within ‘Wernicke’s area’. Brain 124(Pt 1):83–95PubMedCrossRef
Metadata
Title
Mapping phonemic processing zones along human perisylvian cortex: an electro-corticographic investigation
Authors
Sophie Molholm
Manuel R. Mercier
Einat Liebenthal
Theodore H. Schwartz
Walter Ritter
John J. Foxe
Pierfilippo De Sanctis
Publication date
01-07-2014
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 4/2014
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-013-0574-y

Other articles of this Issue 4/2014

Brain Structure and Function 4/2014 Go to the issue