No AccessJournal of Speech, Language, and Hearing ResearchResearch Article29 Aug 2019

Functional Parcellation of the Speech Production Cortex

    Neuroimaging has revealed a core network of cortical regions that contribute to speech production, but the functional organization of this network remains poorly understood.


    We describe efforts to identify reliable boundaries around functionally homogenous regions within the cortical speech motor control network in order to improve the sensitivity of functional magnetic resonance imaging (fMRI) analyses of speech production and thus improve our understanding of the functional organization of speech production in the brain.


    We used a bottom-up, data-driven approach by pooling data from 12 previously conducted fMRI studies of speech production involving the production of monosyllabic and bisyllabic words and pseudowords that ranged from single vowels and consonant–vowel pairs to short sentences (163 scanning sessions, 136 unique participants, 39 different speech conditions). After preprocessing all data through the same pipeline and registering individual contrast maps to a common surface space, hierarchical clustering was applied to contrast maps randomly sampled from the pooled data set in order to identify consistent functional boundaries across subjects and tasks. Boundary completion was achieved by applying adaptive smoothing and watershed segmentation to the thresholded population-level boundary map. Hierarchical clustering was applied to the mean within–functional region of interest (fROI) response to identify networks of fROIs that respond similarly during speech.


    We identified highly reliable functional boundaries across the cortical areas involved in speech production. Boundary completion resulted in 117 fROIs in the left hemisphere and 109 in the right hemisphere. Clustering of the mean within-fROI response revealed a core sensorimotor network flanked by a speech motor planning network. The majority of the left inferior frontal gyrus clustered with the visual word form area and brain regions (e.g., anterior insula, dorsal anterior cingulate) associated with detecting salient sensory inputs and choosing the appropriate action.


    The fROIs provide insight into the organization of the speech production network and a valuable tool for studying speech production in the brain by improving within-group and between-groups comparisons of speech-related brain activity.

    Supplemental Material


    • Basilakos, A., Smith, K. G., Fillmore, P., Fridriksson, J., & Fedorenko, E. (2017). Functional characterization of the human speech articulation network.Cerebral Cortex, 28, 1816–1830.
    • Beal, D. S., Segawa, J. A., Tourville, J. A., Cai, S., & Guenther, F. H. (2012). Speech motor sequence learning difficulties in persistent developmental stuttering: An fMRI study (Program No. 681.0). Meeting Planner, 42nd Annual Meeting of the Society for Neuroscience, New Orleans, LA.
    • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing.Journal of the Royal Statistical Society. Series B (Methodological), 57, 289–300.
    • Bohland, J. W., Bullock, D., & Guenther, F. H. (2010). Neural representations and mechanisms for the performance of simple speech sequences.Journal of Cognitive Neuroscience, 22(7), 1504–1529.
    • Bohland, J. W., & Guenther, F. H. (2006). An fMRI investigation of syllable sequence production.NeuroImage, 32(2), 821–841.
    • Brown, S., Ingham, R. J., Ingham, J. C., Laird, A. R., & Fox, P. T. (2005). Stuttered and fluent speech production: An ALE meta-analysis of functional neuroimaging studies.Human Brain Mapping, 25(1), 105–117.
    • Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network: Anatomy, function, and relevance to disease.Annals of the New York Academy of Sciences, 1124(1), 1–38.
    • Cai, S., Tourville, J. A., Beal, D. S., Perkell, J. S., Guenther, F. H., & Ghosh, S. S. (2014). Diffusion imaging of cerebral white matter in persons who stutter: Evidence for network-level anomalies.Frontiers in Human Neuroscience, 8, 54.
    • Caviness, V. S., Jr., Meyer, J., Makris, N., & Kennedy, D. N. (1996). MRI-based topographic parcellation of human neocortex: An anatomically specified method with estimate of reliability.Journal of Cognitive Neuroscience, 8(6), 566–587.
    • Cohen, A. L., Fair, D. A., Dosenbach, N. U., Miezin, F. M., Dierker, D., Van Essen, D. C., … Petersen, S. E. (2008). Defining functional areas in individual human brains using resting functional connectivity MRI.NeuroImage, 41(1), 45–57.
    • Costafreda, S. G. (2009). Pooling fMRI data: Meta-analysis, mega-analysis and multi-center studies.Frontiers in Neuroinformatics, 3, 33.
    • Daniel, T. A., Katz, J. S., & Robinson, J. L. (2016). Delayed match-to-sample in working memory: A BrainMap meta-analysis.Biological Psychology, 120, 10–20.
    • Dehaene, S., & Cohen, L. (2011). The unique role of the visual word form area in reading.Trends in Cognitive Sciences, 15(6), 254–262.
    • Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., … Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.NeuroImage, 31(3), 968–980.
    • Dosenbach, N. U., Visscher, K. M., Palmer, E. D., Miezin, F. M., Wenger, K. K., Kang, H. C., … Petersen, S. E. (2006). A core system for the implementation of task sets.Neuron, 50(5), 799–812.
    • Duvernoy, H. M. (1999). The human brain: Surface, blood supply, and three dimensional Anatomy (2nd ed.). New York, NY: Springer-Verlag.
    • Efron, B. (1982). The jackknife, the bootstrap, and other resampling plans. CBMS-NSF Regional Conference Series in Applied Mathematics, Monograph 38, Philadelphia, PA.
    • Eickhoff, S. B., Bzdok, D., Laird, A. R., Roski, C., Caspers, S., Zilles, K., & Fox, P. T. (2011). Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation.NeuroImage, 57(3), 938–949.
    • Eickhoff, S. B., Heim, S., Zilles, K., & Amunts, K. (2009). A systems perspective on the effective connectivity of overt speech production.Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences, 367(1896), 2399–2421.
    • Fischl, B. (2012). FreeSurfer.NeuroImage, 62(2), 774–781.
    • Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system.NeuroImage, 9(2), 195–207.
    • Fu, C. H., Vythelingum, G. N., Brammer, M. J., Williams, S. C., Amaro, E., Jr., Andrew, C. M., … McGuire, P. K. (2005). An fMRI study of verbal self-monitoring: Neural correlates of auditory verbal feedback.Cerebral Cortex, 16(7), 969–977.
    • Gagnon, L., Sakadžić, S., Lesage, F., Musacchia, J. J., Lefebvre, J., Fang, Q., … Boas, D. A. (2015). Quantifying the microvascular origin of BOLD-fMRI from first principles with two-photon microscopy and an oxygen-sensitive nanoprobe.The Journal of Neuroscience, 35(8), 3663–3675.
    • Ghosh, S. S., Tourville, J. A., & Guenther, F. H. (2008). A neuroimaging study of premotor lateralization and cerebellar involvement in the production of phonemes and syllables.Journal of Speech, Language, and Hearing Research, 51(5), 1183–1202.
    • Golfinopoulos, E., & Guenther, F. H. (2011). Prominence in English spoken utterances: fMRI evidence for left hemisphere cortical recruitment. Poster presented at the 17th Annual Meeting of the Organization on Human Brain Mapping. Québec City, Canada.
    • Golfinopoulos, E., Tourville, J. A., Bohland, J. W., Ghosh, S. S., Nieto-Castañón, A., & Guenther, F. H. (2011). fMRI investigation of unexpected somatosensory feedback perturbation during speech.NeuroImage, 55(3), 1324–1338.
    • Guenther, F. H. (2016). Neural control of speech. Cambridge, MA: MIT Press.
    • Guenther, F. H., Ghosh, S. S., & Tourville, J. A. (2006). Neural modeling and imaging of the cortical interactions underlying syllable production.Brain and Language, 96(3), 280–301.
    • Hagler, D. J., Jr., Saygin, A. P., & Sereno, M. I. (2006). Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data.NeuroImage, 33(4), 1093–1103.
    • Hayasaka, S., & Nichols, T. E. (2003). Validating cluster size inference: Random field and permutation methods.NeuroImage, 20(4), 2343–2356.
    • Heim, S., Opitz, B., & Friederici, A. D. (2003). Distributed cortical networks for syntax processing: Broca's area as the common denominator.Brain and Language, 85(3), 402–408.
    • Hickok, G., Houde, J., & Rong, F. (2011). Sensorimotor integration in speech processing: Computational basis and neural organization.Neuron, 69(3), 407–422.
    • Hickok, G., & Poeppel, D. (2007). The cortical organization of speech processing.Nature Reviews Neuroscience, 8(5), 393–402.
    • Hinds, O. P., Rajendran, N., Polimeni, J. R., Augustinack, J. C., Wiggins, G., Wald, L. L., … Fischl, B. (2008). Accurate prediction of V1 location from cortical folds in a surface coordinate system.NeuroImage, 39(4), 1585–1599.
    • Houde, J. F., & Nagarajan, S. S. (2011). Speech production as state feedback control.Frontiers in Human Neuroscience, 5, 82.
    • Indefrey, P. (2011). The spatial and temporal signatures of word production components: A critical update.Frontiers in Psychology, 2, 255.
    • Kim, J.-H., Lee, J.-M., Jo, H. J., Kim, S. H., Lee, J. H., Kim, S. T., … Ziad, S. S. (2010). Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity-based parcellation method.NeuroImage, 49(3), 2375–2386.
    • Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., … Fox, P. T. (2000). Automated Talairach atlas labels for functional brain mapping.Human Brain Mapping, 10(3), 120–131.
    • Lee, M. H., Smyser, C. D., & Shimony, J. S. (2013). Resting-state fMRI: A review of methods and clinical applications.American Journal of Neuroradiology, 34(10), 1866–1872.
    • Menon, R. S. (2012). The great brain versus vein debate.NeuroImage, 62(2), 970–974.
    • Menon, V. (2015). Salience network.In A. W. Toga (Ed.), Brain mapping: An encyclopedic reference (Vol. 2, pp. 597–611). Cambridge, MA: Academic Press.
    • Nieto-Castañón, A., Ghosh, S. S., Tourville, J. A., & Guenther, F. H. (2003). Region of interest based analysis of functional imaging data.NeuroImage, 19(4), 1303–1316.
    • Niziolek, C. A., & Guenther, F. H. (2013). Vowel category boundaries enhance cortical and behavioral responses to speech feedback alterations.The Journal of Neuroscience, 33(29), 12090–12098.
    • Overduin, S. A., & Guenther, F. H. (2009). Brain structures differentially responsible for controlling overt and covert speech [Abstract]. Chicago, IL: Society for Neuroscience.
    • Park, H., Park, Y.-H., Cha, J., Seo, S. W., Na, D. L., & Lee, J.-M. (2017). Agreement between functional connectivity and cortical thickness-driven correlation maps of the medial frontal cortex.PLOS ONE, 12(3), e0171803.
    • Peeva, M. G., Guenther, F. H., Tourville, J. A., Nieto-Castañón, A., Anton, J.-L., Nazarian, B., & Alario, F.-X. (2010). Distinct representations of phonemes, syllables, and supra-syllabic sequences in the speech production network.NeuroImage, 50(2), 626–638.
    • Petrides, M. (2014). Neuroanatomy of language regions of the human brain. London, United Kingdom: Academic Press.
    • Poldrack, R. A. (2007). Region of interest analysis for fMRI.Social Cognitive and Affective Neuroscience, 2(1), 67–70.
    • Power, J. D., Cohen, A. L., Nelson, S. M., Wig, G. S., Barnes, K. A., Church, J. A., … Petersen, S. E. (2011). Functional network organization of the human brain.Neuron, 72(4), 665–678.
    • Rademacher, J., Galaburda, A. M., Kennedy, D. N., Filipek, P. A., & Caviness, V. S., Jr. (1992). Human cerebral cortex: Localization, parcellation, and morphometry with magnetic resonance imaging.Journal of Cognitive Neuroscience, 4(4), 352–374.
    • Rottschy, C., Langner, R., Dogan, I., Reetz, K., Laird, A. R., Schulz, J. B., … Eickhoff, S. B. (2012). Modelling neural correlates of working memory: A coordinate-based meta-analysis.NeuroImage, 60(1), 830–846.
    • Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., … Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control.The Journal of Neuroscience, 27(9), 2349–2356.
    • Segawa, J. A., Tourville, J. A., Beal, D. S., & Guenther, F. H. (2013). The representation of syllabic frame structures and phonological content in the brain. Poster presented at the 19th Annual Meeting of the Organization for Human Brain Mapping, Seattle, WA.
    • Segawa, J. A., Tourville, J. A., Beal, D. S., & Guenther, F. H. (2015). The neural correlates of speech motor sequence learning.The Journal of Cognitive Neuroscience, 27(4), 819–831.
    • Seghier, M. L., & Price, C. J. (2009). Dissociating functional brain networks by decoding the between-subject variability.NeuroImage, 45(2), 349–359.
    • Simonyan, K., Ackermann, H., Chang, E. F., & Greenlee, J. D. (2016). New developments in understanding the complexity of human speech production.The Journal of Neuroscience, 36(45), 11440–11448.
    • Sörös, P., Sokoloff, L. G., Bose, A., McIntosh, A. R., Graham, S. J., & Stuss, D. T. (2006). Clustered functional MRI of overt speech production.NeuroImage, 32(1), 376–387.
    • Takai, O., Brown, S., & Liotti, M. (2010). Representation of the speech effectors in the human motor cortex: Somatotopy or overlap.Brain and Language, 113(1), 39–44.
    • Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system: An approach to cerebral imaging. New York, NY: Thieme.
    • Thirion, B., Varoquaux, G., Dohmatob, E., & Poline, J.-B. (2014). Which fMRI clustering gives good brain parcellations.Frontiers in Neuroscience, 8, 167.
    • Tourville, J., & Guenther, F. H. (2012). Automatic cortical labeling system for neuroimaging studies of normal and disordered speech (Program No. 681.06). Meeting Planner, 42nd Annual Meeting of the Society for Neuroscience, New Orleans, LA.
    • Tourville, J. A., & Guenther, F. H. (2011). The DIVA model: A neural theory of speech acquisition and production.Language and Cognitive Processes, 26(7), 952–981.
    • Tourville, J. A., Reilly, K. J., & Guenther, F. H. (2008). Neural mechanisms underlying auditory feedback control of speech.NeuroImage, 39(3), 1429–1443.
    • Toyomura, A., Koyama, S., Miyamaoto, T., Terao, A., Omori, T., Murohashi, H., & Kuriki, S. (2007). Neural correlates of auditory feedback control in human.Neuroscience, 146(2), 499–503.
    • Turkeltaub, P. E., Eden, G. F., Jones, K. M., & Zeffiro, T. A. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation.NeuroImage, 16(3), 765–780.
    • Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., … Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.NeuroImage, 15(1), 273–289.
    • Van Essen, D. C., Drury, H. A., Joshi, S., & Miller, M. I. (1998). Functional and structural mapping of human cerebral cortex: Solutions are in the surfaces.Proceedings of the National Academy of Sciences of the United States of America, 95(3), 788–795.
    • Viessmann, O. M., Bianciardi, M., Scheffler, K., Wald, L. L., & Polimeni, J. R. (2018). The EPI rs-fMRI signal shows an orientation effect with respect to B0 and phase-encode axis across cortical depth. Joint Annual Meeting ISMRM-ESMRMB 2018, Paris, France.
    • Vigneau, M., Beaucousin, V., Hervé, P.-Y., Duffau, H., Crivello, F., Houdé, O., … Tzourio-Mazoyer, N. (2006). Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing.NeuroImage, 30(4), 1414–1432.
    • Ward, J. H., Jr. (1963). Hierarchical grouping to optimize an objective function.Journal of the American Statistical Association, 58(301), 236–244.
    • Whitfield-Gabrieli, S., & Nieto-Castañón, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks.Brain Connectivity, 2(3), 125–141.
    • Wilson, S. M. (2014). The impact of vascular factors on language localization in the superior temporal sulcus.Human Brain Mapping, 35(8), 4049–4063.
    • Wise, R. J., Greene, J., Büchel, C., & Scott, S. K. (1999). Brain regions involved in articulation.The Lancet, 353(9158), 1057–1061.
    • Yousry, T., Schmid, U. D., Alkadhi, H., Schmidt, D., Peraud, A., Buettner, A., & Winkler, P. (1997). Localization of the motor hand area to a knob on the precentral gyrus: A new landmark.Brain, 120(1), 141–157.
    • Zilles, K., & Amunts, K. (2010). Centenary of Brodmann's map—Conception and fate.Nature Reviews Neuroscience, 11, 139–145.

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