Computational modeling of stuttering caused by impairments in a basal ganglia thalamo-cortical circuit involved in syllable selection and initiation

Oren Civier; Daniel Bullock; Ludo Max; Frank H. Guenther

doi:10.1016/j.bandl.2013.05.016

Computational modeling of stuttering caused by impairments in a basal ganglia thalamo-cortical circuit involved in syllable selection and initiation

Oren Civier, Daniel Bullock, Ludo Max, Frank H. Guenther

Research output: Contribution to journal › Article › peer-review

70 Scopus citations

Abstract

Atypical white-matter integrity and elevated dopamine levels have been reported for individuals who stutter. We investigated how such abnormalities may lead to speech dysfluencies due to their effects on a syllable-sequencing circuit that consists of basal ganglia (BG), thalamus, and left ventral premotor cortex (vPMC). "Neurally impaired" versions of the neurocomputational speech production model GODIVA were utilized to test two hypotheses: (1) that white-matter abnormalities disturb the circuit via corticostriatal projections carrying copies of executed motor commands and (2) that dopaminergic abnormalities disturb the circuit via the striatum. Simulation results support both hypotheses: in both scenarios, the neural abnormalities delay readout of the next syllable's motor program, leading to dysfluency. The results also account for brain imaging findings during dysfluent speech. It is concluded that each of the two abnormality types can cause stuttering moments, probably by affecting the same BG-thalamus-vPMC circuit.

Original language	English
Pages (from-to)	263-278
Number of pages	16
Journal	Brain and Language
Volume	126
Issue number	3
DOIs	https://doi.org/10.1016/j.bandl.2013.05.016
State	Published - Sep 2013
Externally published	Yes

Bibliographical note

Funding Information:
This study is part of the PhD dissertation of Oren Civier at Boston University and was supported by NIH/NIDCD Grants R01 DC07683 and R01 DC02852 (P.I. Frank Guenther) and RO1 DC007603 (P.I. Ludo Max). We are grateful to Jason Bohland for developing the GODIVA model code and helping with the simulations, to Jason Tourville for the extensive knowledge and guidance with the prediction of BOLD responses, and to Gerald Maguire and Per Alm whose novel hypotheses and suggestions paved the way for this study. We thank Satrajit Ghosh, Alfonso Nieto-Castanon, and Jonathan Brumberg for the development of the DIVA model code, and Joseph Perkell, Amit Bajaj, and Michal Ben-Shachar for sharing their insights on stuttering and speech production. Lastly, thanks to Helen Barbas, Jonathan Mink, Hagai Bergman, Can Tan, and Alon Nevet for consulting on basal ganglia circuitry, to Vered Kronfeld, Paul Brocklehurst, and the three anonymous reviewers, for their comments on earlier versions of this manuscript, and to Maya Peeva, Shanqing Cai, Hayo Terband, and Elisa Golfinopoulos for their assistance.

Keywords

Basal ganglia
Brain imaging
Dopamine
Neural modeling
Speech fluency
Speech motor control
Stuttering
Thalamus
Ventral premotor cortex
White matter

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10.1016/j.bandl.2013.05.016

Cite this

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title = "Computational modeling of stuttering caused by impairments in a basal ganglia thalamo-cortical circuit involved in syllable selection and initiation",

abstract = "Atypical white-matter integrity and elevated dopamine levels have been reported for individuals who stutter. We investigated how such abnormalities may lead to speech dysfluencies due to their effects on a syllable-sequencing circuit that consists of basal ganglia (BG), thalamus, and left ventral premotor cortex (vPMC). {"}Neurally impaired{"} versions of the neurocomputational speech production model GODIVA were utilized to test two hypotheses: (1) that white-matter abnormalities disturb the circuit via corticostriatal projections carrying copies of executed motor commands and (2) that dopaminergic abnormalities disturb the circuit via the striatum. Simulation results support both hypotheses: in both scenarios, the neural abnormalities delay readout of the next syllable's motor program, leading to dysfluency. The results also account for brain imaging findings during dysfluent speech. It is concluded that each of the two abnormality types can cause stuttering moments, probably by affecting the same BG-thalamus-vPMC circuit.",

keywords = "Basal ganglia, Brain imaging, Dopamine, Neural modeling, Speech fluency, Speech motor control, Stuttering, Thalamus, Ventral premotor cortex, White matter",

author = "Oren Civier and Daniel Bullock and Ludo Max and Guenther, {Frank H.}",

note = "Funding Information: This study is part of the PhD dissertation of Oren Civier at Boston University and was supported by NIH/NIDCD Grants R01 DC07683 and R01 DC02852 (P.I. Frank Guenther) and RO1 DC007603 (P.I. Ludo Max). We are grateful to Jason Bohland for developing the GODIVA model code and helping with the simulations, to Jason Tourville for the extensive knowledge and guidance with the prediction of BOLD responses, and to Gerald Maguire and Per Alm whose novel hypotheses and suggestions paved the way for this study. We thank Satrajit Ghosh, Alfonso Nieto-Castanon, and Jonathan Brumberg for the development of the DIVA model code, and Joseph Perkell, Amit Bajaj, and Michal Ben-Shachar for sharing their insights on stuttering and speech production. Lastly, thanks to Helen Barbas, Jonathan Mink, Hagai Bergman, Can Tan, and Alon Nevet for consulting on basal ganglia circuitry, to Vered Kronfeld, Paul Brocklehurst, and the three anonymous reviewers, for their comments on earlier versions of this manuscript, and to Maya Peeva, Shanqing Cai, Hayo Terband, and Elisa Golfinopoulos for their assistance. ",

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N2 - Atypical white-matter integrity and elevated dopamine levels have been reported for individuals who stutter. We investigated how such abnormalities may lead to speech dysfluencies due to their effects on a syllable-sequencing circuit that consists of basal ganglia (BG), thalamus, and left ventral premotor cortex (vPMC). "Neurally impaired" versions of the neurocomputational speech production model GODIVA were utilized to test two hypotheses: (1) that white-matter abnormalities disturb the circuit via corticostriatal projections carrying copies of executed motor commands and (2) that dopaminergic abnormalities disturb the circuit via the striatum. Simulation results support both hypotheses: in both scenarios, the neural abnormalities delay readout of the next syllable's motor program, leading to dysfluency. The results also account for brain imaging findings during dysfluent speech. It is concluded that each of the two abnormality types can cause stuttering moments, probably by affecting the same BG-thalamus-vPMC circuit.

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ER -

Computational modeling of stuttering caused by impairments in a basal ganglia thalamo-cortical circuit involved in syllable selection and initiation

Abstract

Bibliographical note

Keywords

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