Evidence of Left Inferior Frontal-premotor Structural and Functional Connectivity Deficits in Adults Who Stutter

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2011 Apr 8

PMID 21471556

Citations 72

Authors

Soo-Eun Chang

Barry Horwitz

John Ostuni

Richard Reynolds

Christy L Ludlow

Affiliations

Soon will be listed here.

Abstract

The neurophysiological basis for stuttering may involve deficits that affect dynamic interactions among neural structures supporting fluid speech processing. Here, we examined functional and structural connectivity within corticocortical and thalamocortical loops in adults who stutter. For functional connectivity, we placed seeds in the left and right inferior frontal Brodmann area 44 (BA44) and in the ventral lateral nucleus (VLN) of the thalamus. Subject-specific seeds were based on peak activation voxels captured during speech and nonspeech tasks using functional magnetic resonance imaging. Psychophysiological interaction (PPI) was used to find brain regions with heightened functional connectivity with these cortical and subcortical seeds during speech and nonspeech tasks. Probabilistic tractography was used to track white matter tracts in each hemisphere using the same seeds. Both PPI and tractrography supported connectivity deficits between the left BA44 and the left premotor regions, while connectivity among homologous right hemisphere structures was significantly increased in the stuttering group. No functional connectivity differences between BA44 and auditory regions were found between groups. The functional connectivity results derived from the VLN seeds were less definitive and were not supported by the tractography results. Our data provide strongest support for deficient left hemisphere inferior frontal to premotor connectivity as a neural correlate of stuttering.

Citing Articles

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A comparison of structural morphometry in children and adults with persistent developmental stuttering.

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References

Eden G, Joseph J, Brown H, Brown C, Zeffiro T . Utilizing hemodynamic delay and dispersion to detect fMRI signal change without auditory interference: the behavior interleaved gradients technique. Magn Reson Med. 1999; 41(1):13-20. DOI: 10.1002/(sici)1522-2594(199901)41:1<13::aid-mrm4>3.0.co;2-t. View

Hashimoto Y, Sakai K . Brain activations during conscious self-monitoring of speech production with delayed auditory feedback: an fMRI study. Hum Brain Mapp. 2003; 20(1):22-8. PMC: 6871912. DOI: 10.1002/hbm.10119. View

Fox P, Ingham R, Ingham J, Hirsch T, Downs J, Martin C . A PET study of the neural systems of stuttering. Nature. 1996; 382(6587):158-61. DOI: 10.1038/382158a0. View

Riley G . A stuttering severity instrument for children and adults. J Speech Hear Disord. 1972; 37(3):314-22. DOI: 10.1044/jshd.3703.314. View

Salmelin R, Schnitzler A, Schmitz F, Freund H . Single word reading in developmental stutterers and fluent speakers. Brain. 2000; 123 ( Pt 6):1184-202. DOI: 10.1093/brain/123.6.1184. View

Schmahmann J, Pandya D . Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: a WGA-HRP and fluorescent tracer study. J Comp Neurol. 1990; 295(2):299-326. DOI: 10.1002/cne.902950212. View

Smits-Bandstra S, De Nil L . Sequence skill learning in persons who stutter: implications for cortico-striato-thalamo-cortical dysfunction. J Fluency Disord. 2007; 32(4):251-78. DOI: 10.1016/j.jfludis.2007.06.001. View

Eickhoff S, Stephan K, Mohlberg H, Grefkes C, Fink G, Amunts K . A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005; 25(4):1325-35. DOI: 10.1016/j.neuroimage.2004.12.034. View

Cykowski M, Fox P, Ingham R, Ingham J, Robin D . A study of the reproducibility and etiology of diffusion anisotropy differences in developmental stuttering: a potential role for impaired myelination. Neuroimage. 2010; 52(4):1495-504. PMC: 4135434. DOI: 10.1016/j.neuroimage.2010.05.011. View

10.

Lu C, Peng D, Chen C, Ning N, Ding G, Li K . Altered effective connectivity and anomalous anatomy in the basal ganglia-thalamocortical circuit of stuttering speakers. Cortex. 2009; 46(1):49-67. DOI: 10.1016/j.cortex.2009.02.017. View

11.

Alm P . Stuttering and the basal ganglia circuits: a critical review of possible relations. J Commun Disord. 2004; 37(4):325-69. DOI: 10.1016/j.jcomdis.2004.03.001. View

12.

Civier O, Tasko S, Guenther F . Overreliance on auditory feedback may lead to sound/syllable repetitions: simulations of stuttering and fluency-inducing conditions with a neural model of speech production. J Fluency Disord. 2010; 35(3):246-79. PMC: 2939043. DOI: 10.1016/j.jfludis.2010.05.002. View

13.

Kim J, Horwitz B . Investigating the neural basis for fMRI-based functional connectivity in a blocked design: application to interregional correlations and psycho-physiological interactions. Magn Reson Imaging. 2008; 26(5):583-93. DOI: 10.1016/j.mri.2007.10.011. View

14.

Foundas A, Bollich A, Corey D, Hurley M, Heilman K . Anomalous anatomy of speech-language areas in adults with persistent developmental stuttering. Neurology. 2001; 57(2):207-15. DOI: 10.1212/wnl.57.2.207. View

15.

Ludlow C . Stuttering: dysfunction in a complex and dynamic system. Brain. 2000; 123 ( Pt 10):1983-4. DOI: 10.1093/brain/123.10.1983. View

16.

Smits-Bandstra S, De Nil L, Rochon E . The transition to increased automaticity during finger sequence learning in adult males who stutter. J Fluency Disord. 2006; 31(1):22-42. DOI: 10.1016/j.jfludis.2005.11.004. View

17.

Behrens T, Johansen-Berg H, Woolrich M, Smith S, Wheeler-Kingshott C, Boulby P . Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 2003; 6(7):750-7. DOI: 10.1038/nn1075. View

18.

Max L, Yudman E . Accuracy and variability of isochronous rhythmic timing across motor systems in stuttering versus nonstuttering individuals. J Speech Lang Hear Res. 2003; 46(1):146-63. DOI: 10.1044/1092-4388(2003/012). View

19.

Guenther F . Cortical interactions underlying the production of speech sounds. J Commun Disord. 2006; 39(5):350-65. DOI: 10.1016/j.jcomdis.2006.06.013. View

20.

Hall D, Haggard M, Akeroyd M, Palmer A, Summerfield A, Elliott M . "Sparse" temporal sampling in auditory fMRI. Hum Brain Mapp. 1999; 7(3):213-23. PMC: 6873323. DOI: 10.1002/(sici)1097-0193(1999)7:3<213::aid-hbm5>3.0.co;2-n. View