Brain Correlates of Stuttering and Syllable Production: Gender Comparison and Replication
Publication: Journal of Speech, Language, and Hearing Research
Volume 47, Number 2
Pages 321-341
Abstract
This article reports a gender replication study of the P. T. Fox et al. (2000) performance correlation analysis of neural systems that distinguish between normal and stuttered speech in adult males. Positron-emission tomographic (PET) images of cerebral blood flow (CBF) were correlated with speech behavior scores obtained during PET imaging for 10 dextral female stuttering speakers and 10 dextral, age- and sex-matched normally fluent controls. Gender comparisons were made between the total number of voxels per region significantly correlated with speech performance (as in P. T. Fox et al., 2000) plus total voxels per region that were significantly correlated with stutter rate and not with syllable rate.
Stutter-rate regional correlates were generally right-sided in males, but bilateral in the females. For both sexes the positive regional correlates for stuttering were in right (R) anterior insula and the negative correlates were in R Brodmann area 21/22 and an area within left (L) inferior frontal gyrus. The female stuttering speakers displayed additional positive correlates in L anterior insula and in basal ganglia (L globus pallidus, R caudate), plus extensive right hemisphere negative correlates in the prefrontal area and the limbic and parietal lobes. The male stuttering speakers were distinguished by positive correlates in L medial occipital lobe and R medial cerebellum. Regions that positively correlated with syllable rate (essentially stutter-free speech) in stuttering speakers and controls were very similar for both sexes.
The findings strengthen claims that chronic developmental stuttering is functionally related to abnormal speech-motor and auditory region interactions. The gender differences may be related to differences between the genders with respect to susceptibility (males predominate) and recovery from chronic stuttering (females show higher recovery rates during childhood).
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References
Abbey, E. (1975). The monkey wrench gang. New York: Avon Books.
Abwender, D. A., Trinidad, K. S., Jones, K. R., Como, P. G., Hymes, E., & Kurlan, R. (1998). Features resembling Tourette’s syndrome in developmental stutterers. Brain and Language, 62, 455–464.
Belin, P., Zatorre, R. J., Lafaille, P., Ahad, P., & Pike, B.(2000). Voice-selective areas in human auditory cortex. Nature, 403, 309–312.
Blood, G. W., & Blood, I. M. (1989). Laterality preferences in female and male stutterers. Journal of Fluency Disorders, 14, 1–10.
Bloodstein, O. (1995). A handbook on stuttering. San Diego, CA: Singular.
Boecker, H., Dagher, A., Ceballos-Baumann, A. O., Passingham, R. E., Samuel, M., Friston, K. J., et al.(1998). Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: Investigations with H215O PET. Journal of Neurophysiology, 79, 1070–1080.
Boring, E. G. (1950). A history of experimental psychology. New York: Appleton.
Braun, A. R., Varga, M., Stager, S., Schulz, G., Selbie, S., Maisog, J. M., Carson, R. E., & Ludlow, C. L.(1997). Altered patterns of cerebral activity during speech and language production in developmental stuttering: An H215O positron emission tomography study. Brain, 120, 761–784.
Buckner, R. L., Raichle, M. E., & Petersen, S. E. (1995). Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups.Journal of Neurophysiology, 74, 2163–2173.
Comings, D. E., & Comings, B. G. (1994). TS, learning,and speech problems. Journal of the American Academy of Child and Adolescent Psychiatry, 33, 429–430.
De Nil, L. F., Kroll, R. M., Kapur, S., & Houle, S. (2000).A positron emission tomography study of silent and oral single word reading in stuttering and nonstuttering adults. Journal of Speech, Language, and Hearing Research, 43, 1038–1053.
Dronkers, N. F. (1996). A new brain region for coordinating speech articulation. Nature, 384, 159–161.
Fiez, J. A., & Petersen, S. E. (1998). Neuroimaging studies of word reading. Proceedings of the National Academy of Sciences, USA, 95, 914–921.
Foundas, A. L., Bollich, A. M., Corey, D. M., Hurley, M., & Heilman, K. M. (2001). Anomalous anatomy of speech-language areas in adults with persistent developmental stuttering. Neurology 57, 207–215.
Fox, P. T., Ingham, R. J., Ingham, J. C., Zamarripa, F., Xiong, J.-H., & Lancaster, J. (2000). Brain correlates of stuttering and syllable production: A PET performance-correlation analysis. Brain, 123, 1985–2004.
Fox, P. T., Ingham, R. J., Ingham, J. C., Hirsch, T., Downs, J. H., Martin, C., et al. (1996). A PET study of the neural systems of stuttering. Nature, 382, 158–162.
Fox, P. T., & Lancaster, J. L. (1996). Un atlas du cerveau sur Internet [A brain atlas on the Internet]. Recherche, 289, 49–51.
Fox, P. T., & Raichle, M. E. (1984). Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. Journal of Neurophysiology, 51, 1109–1120.
Fox, P. T., & Raichle, M. E. (1985). Stimulus rate determines regional brain blood flow in striate cortex. Annals of Neurology, 17, 303–305.
Frost, J. A., Binder, J. R., Springer, J. A., Hammeke, T. A., Bellgowan, P. S., Rao, S. M., & Cox, R. W. (1999). Language processing is strongly left lateralized in both sexes: Evidence from functional MRI. Brain, 122, 199–208.
Fujiki, N., Naito, Y., Hirano, S., Kojima, H., Shiomi, Y., Nishizawa, S., et al. (1999). Correlation between rCBF and speech perception in cochlear implant users.Auris Nasus Larynx, 26, 229–236.
Good, C. D., Johnsrude, I., Ashburner, J., Henson,R. N. A., Friston, K. J., & Frackowiak, R. S. J. (2001). Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage, 14, 685–700.
Griffiths, T. D., Bench, C. J., & Frackowiak, R. S.(1994). Human cortical areas selectively activated by apparent sound movement. Current Biology, 4, 892–895.
Harasty, J., Double, K. L., Halliday, G. M., Kril, J. J., & McRitchie, D. A. (1997). Language-associated cortical regions are proportionally larger in the female brain. Archives of Neurology, 54, 171–176.
Indefrey, P., & Levelt, W. J. M. (2000). The neural correlates of language production. In M. S. Gazzaniga (Ed.), The new cognitive neurosciences (2nd ed., pp. 845–866). Cambridge, MA: MIT Press.
Ingham, R. J. (1988). Speech naturalness and stuttering research: A review. In S. E. Gerber & G. T. Mencher (Eds.) International perspectives on communication disorders (pp. 168–180). Washington, DC: Gallaudet University Press.
Ingham, R. J. (1998). On learning from speech-motor control research on stuttering. In A. K. Cordes & R. J. Ingham (Eds.), Treatment efficacy for stuttering: A search for empirical bases (pp. 67–101). San Diego, CA: Singular.
Ingham, R. J. (2001). Brain imaging studies of developmental stuttering. Journal of Communication Disorders, 34, 493–516.
Ingham, R. J., Bakker, K., Kilgo, M., & Moglia, R.(1999). Stuttering Measurement System (SMS). Santa Barbara: University of California. Retrieved March 31, 2004, fromhttp://www.speech.ucsb.edu/
Ingham, R. J., Cordes, A. K., & Gow, M. L. (1993). Time interval measurement of stuttering: Modifying interjudge agreement. Journal of Speech and Hearing Research, 36, 503–515.
Ingham, R. J., Fox, P. T., Ingham, J. C., & Zamarripa, F. (2000). Is overt speech a prerequisite for the neural activations associated with chronic developmental stuttering ? Brain and Language, 75, 163–194.
Ingham, R. J., & Packman, A. (1979). A further evaluation of the speech of stutterers during chorus- and nonchorusreading conditions. Journal of Speech and Hearing Research, 22, 784–793.
Jaeger, J. J., Lockwood, A. H., Van Valin, R. D., Jr., Kemmerer, D. L., Murphy, B. W., & Wack, D. S. (1998). Sex differences in brain regions activated by grammatical and reading tasks. Neuroreport, 9, 2803–2807.
Kansaku, K., Yamaura, A., & Kitazawa, S. (2000). Sex differences in lateralization revealed in the posterior language areas. Cerebral Cortex, 10, 866–872.
Kidd, K. K., Heimbuch, R. C., & Records, M. A. (1981). Vertical transmission of susceptibility to stuttering with sex-modified expression. Proceedings of the National Academy of Sciences, USA, 78, 606–610.
Lancaster, J. L., Glass, T. G., Lankipalli, B. R., Downs, H., Mayberg, H., & Fox, P. T. (1995). A modality-independent approach to spatial normalization of tomographic images of the human brain. Human Brain Mapping, 3, 209–223.
Lancaster, J. L., Rainey, L. H., Summerlin, J. L., Frietas, C. S., Fox, P. T., Evans, A. C., et al. (1997). Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward-transform method. Human Brain Mapping, 4, 238–242.
Lewis, D., & Sherman, D. (1951). Measuring the severity of stuttering. Journal of Speech and Hearing Disorders, 16, 320–326.
Martin, R. R., Haroldson, S. K., & Triden K. A. (1984). Stuttering and speech naturalness. Journal of Speech and Hearing Disorders, 49, 53–58.
McGlone, J. (1980). Sex differences in human brain asymmetry: A critical survey. Behavioral and Brain Sciences, 3, 216–263.
Mesulam, M. M., & Mufson, E. J. (1985). The insula of Reil in man and monkey. In A. Peters &E. Jones (Eds.), Cerbral cortex (pp. 179–226). New York: Plenum Press.
Moore, W. H., Jr. (1993). Hemisphere processing research. In E. Boberg (Ed.), Neuropsychology of stuttering (pp. 39–72). Edmonton, Alberta, Canada: University of Alberta Press.
Müller, R. A., Rothermel, R. D., Behen, M. E., Muzik, O., Mangner, T. J., & Chugani, H. T. (1997). Receptive and expressive language activations for sentences: A PET study. Neuroreport, 8, 3767–3770.
Murphy, K., Corfield, D. R., Guz, A., Fink, G. R., Wise, R. J., Harrison, J., & Adams, L. (1997). Cerebral areas associated with motor control of speech in humans. Journal of Applied Physiology, 83, 1438–1447.
Nuck, M. E., Blood, G. W., & Blood, I. M. (1987). Fluent and disfluent normal speakers’ responses on a synthetic sentence identification (SSI) task. Journal of Communication Disorders, 20, 161–169.
Pakkenberg, B., & Gundersen, H. J. G. (1997). Neocortical neuron number in humans: Effect of sex and age. Journal of Comparative Neurology, 384, 312–320.
Paulesu, E., Frith, C. D., & Frackowiak, R. S. (1993).The neural correlates of the verbal component of working memory. Nature, 362, 342–345.
Petersen, S. E., van Mier, H., Fiez, J. A., & Raichle, M. E. (1998). The effects of practice on the functional anatomy of task performance. Proceedings of the National Academy of Sciences, USA, 95, 853–860.
Phillips, M. D., Lowe, M. J., Lurito, J. T., Dzemidzic, M., & Mathews, V. P. (2001). Temporal lobe activation demonstrates sex-based differences during passive listening. Radiology, 220, 202–207.
Price, C. J., Green, D. W., & von Studnitz, R. (1999).A functional imaging study of translation and language switching. Brain, 122, 2207–2208.
Pugh, K. R., Shaywitz, B. A., Shaywitz, S. E., Constable, R. T., Skudlarski, P., Fulbright, R., et al.(1996). Cerebral organization of component processes in reading. Brain, 119, 1221–1238.
Raichle, M. E., Fiez, J. A., Videen, T. O., Mac Leod, A. M., Pardo, J. V., Fox, P. T., & Petersen, S. E. (1994). Practice-related changes in human brain functional anatomy during nonmotor learning. Cerebral Cortex, 4, 8–26.
Rosenfield, D. B., & Jerger, J. (1984). Stuttering and auditory function. In R. F. Curlee& W. H. Perkins(Eds.),Nature and treatment of stuttering: New directions (pp. 73–87). San Diego, CA: College-Hill Press.
Salmelin, R., Schnitzler, A., Schmitz, F., & Freund, H. J. (2000). Single word reading in developmental stutterers and fluent speakers. Brain, 123, 1184–1202.
Salmelin, R., Schnitzler, A., Schmitz, F., Jäncke, L., Witte, O. W., & Freund, H. J. (1998). Functional organization of the auditory cortex is different in stutterers and fluent speakers. Neuroreport, 9, 2225–2229.
Shaywitz, B. A., Shaywitz, S. E., Pugh, K. R., Constable, R. T., Skudlarski, P., Fulbright, R., et al.(1995). Sex differences in the functional organization of the brain for language. Nature, 373, 607–609.
Sidtis, J. J., Strother, S. C., Anderson, J. R., & Rottenberg, D. A. (1999). Are brain functions really additive ? Neuroimage, 9, 490–496.
Silbersweig, D. A., Stern, E., Frith, C., Cahill, C., Holmes, A., Grootoonk, S., et al. (1995). A functional neuroanatomy of hallucinations in schizophrenia. Nature, 378, 176–179.
Sommer, M., Koch, M. A., Paulus, W., Weiller, C., & Buchel, C. (2002). Disconnection of speech-relevant brain areas in persistent developmental stuttering. Lancet, 360, 380–383.
Stern, E., Silbersweig, D. A., Chee, K. Y., Holmes, A., Robertson, M. M., Trimble, M., et al. (2000). A functional neuroanatomy of tics in Tourette syndrome. Archives of General Psychiatry, 57, 741–748.
Stromsta, C. (1972). Interaural phase disparity of stutterers and nonstutterers. Journal of Speech and Hearing Research, 15, 771–780.
Stromsta, C. (1986). Elements of stuttering. Oshtemo, MI: Atsmorts.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.
Travis, L. E. (1978). The cerebral dominance theory of stuttering: 1931-1978. Journal of Speech and Hearing Disorders, 43, 278–281.
Van Riper, C., & Hull C. J. (1955). The quantitative measurement of the effect of certain situations on stuttering. In W. Johnson & R. R. Leutenegger (Eds.),Stuttering in children and adults (pp. 199–206) Minneapolis: University of Minnesota Press.
Webster, W. G. (1988). Neural mechanisms underlying stuttering: Evidence from bimanual handwriting performance. Brain and Language, 33, 226–244.
Webster, W. G. (1993). Hurried hands and tangled tongues. In E. Boberg (Ed.), Neuropsychology of stuttering (pp. 73–127). Edmonton, Alberta, Canada: University of Alberta Press.
Wertz, R. T., Lapointe, L. L., & Rosenbek, J. C. (1991).Apraxia of speech: The disorder and its management. San Diego, CA: Singular.
Wildgruber, D., Ackermann, H., & Grodd, W. (2001). Differential contributions of motor cortex, basal ganglia, and cerebellum to speech motor control: Effects of syllable repetition rate evaluated by fMRI. Neuroimage, 13, 101–109.
Wise, R. J. S., Greene, J., Buchel, C., & Scott, S. K.(1999). Brain regions involved in articulation. Lancet, 353, 1057–1061.
Witelson, S. F., & Kigar, D. L. (1992). Sylvian fissure morphology and asymmetry in men and women: Bilateral differences in relation to handedness in men. Journal of Comparative Neurology, 323, 326–340.
Wood, F., Stump, D., McKeehan, A., Sheldon, S., & Proctor, J. (1980). Patterns of regional cerebral blood flow during attempted reading aloud by stutterers both on and off haloperidol medication: Evidence for inadequate left frontal activation during stuttering. Brain and Language, 9, 141–144.
Wu, J. C., Maguire, G., Riley, G., Fallon, J., LaCase, L., Chin, S., et al. (1995). A positron emission tomography (F-18) deoxyglucose study of developmental stuttering. Neuroreport, 6, 501–505.
Xiong, J.-H., Gao, J., Lancaster, J. L., & Fox, P. T.(1995). Clustered pixels analysis for functional MRI activation studies in the human brain. Human Brain Mapping, 3, 287–301.
Xiong, J., Rao, S., Jerabek, P., Woldorff, M., & Fox, P. T.(2000). Inter-subject variability in cortical activations during a complex language task. Neuroimage, 12, 326–339.
Yairi, E., Ambrose, N., & Cox, N. (1996). Genetics of stuttering: A critical review. Journal of Speech and Hearing Research, 39, 771–784.
Yates, A. J. (1963). Recent empirical and theoretical approaches to the experimental manipulation of speech in normal subjects and in stammerers. Behaviour Research and Therapy, 1, 95–119.
Zald, D. H., & Pardo, J. V. (1999). The functional neuroanatomy of voluntary swallowing. Annals of Neurology, 46, 281–286.
Zatorre, R. J., Meyer, E., Gjedde, A., & Evans, A. C. (1996). PET studies of phonetic processing of speech: Review, replication, and reanalysis. Cerebral Cortex, 6, 21–30.
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Copyright © 2004 American Speech-Language-Hearing Association.
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- Received: May 16, 2003
- Accepted: Aug 8, 2003
- Published in issue: Apr 1, 2004
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