Abstract
This study investigated methodological (task, stimulus) and intersubject variability in the cortical representation of auditory processing of complex sounds, including speech. Subjects were adult seizure patients undergoing left hemisphere electrocortical mapping (ECM). We tested auditory discrimination of complex sounds, including frequency-modulated tones and speech syllables (digitized, synthesized) contrasted by phonetic features and lexical status. To measure task effects, auditory comprehension was also tested. Within- and across-patient differences in the distribution of deficits induced by ECM were modeled statistically using the recently developed method of Template Mixture Modeling. Cortical representations of auditory discrimination were smaller, more localized, and less variable across subjects than auditory comprehension. Stimulus effects were observed only for speech-tone contrasts. When tasks and stimuli were held constant, two auditory discrimination centers were identified in the posterior temporal lobe. There was also an interaction between task and intersubject effects, with more intersubject variability in cortical maps of auditory comprehension than auditory discrimination. These results demonstrate the utility of using the statistical modeling approach of Template Mixture Modeling to quantify sources of variability in cortical functional organization.
Similar content being viewed by others
References
Basso A, Casati G, Vignolo L (1977) Phonemic identification defect in aphasia. Cortex 13:84–95
Benson R, Whalen D, Richardson M, Swainson B, Clark V, Lai S, Liberman A (2001) Parametrically dissociating speech and nonspeech perception in the brain using fMRI. Brain Lang 78:364–396
Bhatnagar S, Mandybur G, Buckingham H, Andy O (2000) Language representation in the human brain: evidence from cortical mapping. Brain Lang 74:238–259
Binder J, Frost J, Hammeke T, Bellgowan P, Springer J, Kaufman J, Possing E (2000) Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex 10:512–528
Boatman D, Hall C, Goldstein M, Lesser R, Gordon B (1997) Neuroperceptual differences in consonant and vowel discrimination, as revealed by direct cortical electrical interference. Cortex 33:83–98
Boatman D, Hart J, Lesser R, Honeycutt N, Anderson N, Miglioretti D, Gordon B (1998) Right hemisphere speech perception as revealed by amobarbital injection and electrical interference. Neurology 51:458–464
Boatman D, Gordon G, Hart J, Selnes O, Miglioretti D, Lenz F (2000) Transcortical sensory aphasia: revisited and revised. Brain 123:1634–1642
Bookheimer S, Zeffiro T, Blaxton T, Malow B, Gaillard W, Sato S, Kufta C, Fedio P, Theodore W (1997) A direct comparison of PET activation and electrocortical stimulation mapping for language localization. Neurology 47:1056–1065
Burton M, Small S, Blumstein S (2000) The role of segmentation in phonological processing: an fMRI investigation. J Cogn Neurosci 12:679–690
Celsis P, Boulanouar K, Doyon B, Ranjeva J, Berry I, Nespoulous J, Chollet F (1999) Differential fMRI responses in the left posterior superior temporal gyrus and left supramarginal gyrus to habituation and change detection in syllables and tones. Neuroimage 9:135–144
Corina D, McBurney S, Dodrill C, Hinshaw K, Brinkley J, Ojemann G (1999) Functional roles of Broca’s area and SMG: evidence from cortical stimulation mapping in a deaf signer. Neuroimage 10:570–581
De Renzi E, Vignolo L (1969) The Token test: a sensitive test to detect receptive disturbances in aphasics. Brain 85:665–678
Demonet J-F, Chollet F, Ramsay S, Cardebat D, Nespoulous J, Wise R, Rascol A, Frackowiak R (1992) The anatomy of phonological and semantic processing in normal subjects. Brain 115:1753–1768
Gelman A, Carlin J, Stern H, Rubin D (1995) Bayesian data analysis. Chapman and Hall, London, p 34
Green P (1995) Reversible jump Markov chain Monte Carlo computation and Bayesian model determination. Biometrika 82:711–732
Humphries C, Willard K, Buchsbaum B, Hickok G (2001) Role of anterior temporal cortex in auditory sentence comprehension: an fMRI study. Neuroreport 12:1749–1752
Johnsrude I, Zatorre R, Milner B, Evans A (1997) Left-hemisphere specialization for the processing of acoustic transients. Neuroreport 8:1761–1765
Klatt D (1980) Software for a cascade/parallel formant synthesizer. J Acoust Soc Am 67:971–995
Lesser R, Lueders H, Klem G, Dinner D, Hahn J, Cohen L (1984) The localization of speech and writing functions in the frontal language area: results of extraoperative cortical stimulation. Brain 107:275–291
Lurito J, Lowe M, Sartorius C, Mathews V (2000) Comparison of fMRI and intraoperative direct cortical stimulation in localization of receptive language areas. J Comp Assist Tomogr 24:99–105
Mazoyer B, Tzourio N, Frak V, Syrota A, Murayama N, Levrier O, Salamon G, Dehaene S, Cohen L, Mehler J (1993) The cortical representation of speech. J Cogn Neurosci 5:467–479
McCullagh C, Nelder J (1989) Generalized linear models. Chapman and Hall, London
Miceli G, Caltagirone C, Gainotti G, Payer-Rigo (1978) Discrimination of voice versus place contrasts in aphasia. Brain Lang 6:47–51
Miglioretti D, McCulloch C, Zeger S (2000) Template mixture models for direct cortical electrical interference data. Biostatistics 1:1–19
Miglioretti D, McCulloch C, Zeger S (2002) Combining images across multiple subjects: a study of direct cortical electrical interference. J Am Statist Assoc 97:125–135
Nathan S, Sinha S, Gordon B, Lesser R, Thakor N (1993) Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalogr Clin Neurophysiol 88:183–192
Ojemann G (1979) Individual variability in cortical organization of language. J Neurosurg 50:164–169
Ojemann G (1983) Brain organization for language from the perspective of electrical stimulation mapping. Behav Brain Sci 6:189–230
Ojemann G, Mateer C (1979) Human language cortex: localization of memory, syntax, and sequential motor-phoneme identification systems. Science 205:1401–1403
Poeppel D (1996) A critical review of PET studies in phonological processing. Brain Lang 55:317–351
Price C, Wise R, Warburton E, Moore C, Howard D, Patterson K, Frackowiak R, Friston K (1996) Hearing and saying: the functional neuro-anatomy of auditory word processing. Brain 119:919–931
Pugh K, Shaywitz B, Shaywitz S, Fulbright R, Byrd D, Skudlarski P, Shankweiler D, Katz L, Constable R, Fletcher J, Lacadie C, Marchione K, Gores J (1996) Auditory selective attention: an fMRI investigation. Neuroimage 4:159–173
SAS Institute Inc. (2000) SAS OnlineDoc®, Version 8
Scott S, Blank C, Rosen S, Wise R (2000) Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123:2400–2406
Toga A, Jones A, Rothfield J, Woods R, Payne B, Huang C, Mazziotta J, Cai R (1993) Anatomic variability as measured with a 3D reconstructed Talairach atlas. In: Uemura K, Lassen N, Jones T, Kanno I (eds) Quantification of brain function. Elsevier Science, New York, pp 449–456
Vouloumanos A, Kiehl K, Werker J, Liddle P (2001) Detection of sounds in the auditory stream: event-related fMRI evidence for differential activation to speech and nonspeech. J Cogn Neurosci 13:994–1005
Wise R, Chollet F, Hadar U, Friston K, Hoffner E, Frackowiak R (1991) Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain 114:1803–1817
Zatorre R, Evans A, Meyer E, Gjedde A (1992) Lateralization of phonetic and pitch discrimination in speech processing. Science 256:846–849
Acknowledgements
This study was supported by NIDCD grant R01-DC005645. We thank G. Qian and N. Bardhan for technical assistance; Drs. B. Gordon, S. Zeger, C. McCulloch, and S. Reich for helpful discussion; and the reviewers for thoughtful comments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Miglioretti, D.L., Boatman, D. Modeling variability in cortical representations of human complex sound perception. Exp Brain Res 153, 382–387 (2003). https://doi.org/10.1007/s00221-003-1703-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-003-1703-2