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Published in: Brain Structure and Function 1/2018

Open Access 01-01-2018 | Original Article

Shifted dynamic interactions between subcortical nuclei and inferior frontal gyri during response preparation in persistent developmental stuttering

Authors: F. Luise Metzger, Tibor Auer, Gunther Helms, Walter Paulus, Jens Frahm, Martin Sommer, Nicole E. Neef

Published in: Brain Structure and Function | Issue 1/2018

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Abstract

Persistent developmental stuttering is associated with basal ganglia dysfunction or dopamine dysregulation. Here, we studied whole-brain functional connectivity to test how basal ganglia structures coordinate and reorganize sensorimotor brain networks in stuttering. To this end, adults who stutter and fluent speakers (control participants) performed a response anticipation paradigm in the MRI scanner. The preparation of a manual Go/No-Go response reliably produced activity in the basal ganglia and thalamus and particularly in the substantia nigra. Strikingly, in adults who stutter, substantia nigra activity correlated positively with stuttering severity. Furthermore, functional connectivity analyses yielded altered task-related network formations in adults who stutter compared to fluent speakers. Specifically, in adults who stutter, the globus pallidus and the thalamus showed increased network synchronization with the inferior frontal gyrus. This implies dynamic shifts in the response preparation-related network organization through the basal ganglia in the context of a non-speech motor task in stuttering. Here we discuss current findings in the traditional framework of how D1 and D2 receptor activity shapes focused movement selection, thereby suggesting a disproportional involvement of the direct and the indirect pathway in stuttering.
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Literature
go back to reference Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271PubMedCrossRef Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271PubMedCrossRef
go back to reference Anderson J, Hughes J, Rothi L et al (1999) Developmental stuttering and Parkinson’s disease: the effects of levodopa treatment. J Neurol Neurosurg Psychiatry 66:776–778PubMedPubMedCentralCrossRef Anderson J, Hughes J, Rothi L et al (1999) Developmental stuttering and Parkinson’s disease: the effects of levodopa treatment. J Neurol Neurosurg Psychiatry 66:776–778PubMedPubMedCentralCrossRef
go back to reference Bandettini PA, Wong EC, Jesmanowicz A et al (1994) Spin-echo and gradient-echo EPI of human brain activation using BOLD contrast: a comparative study at 1.5 T. NMR Biomed 7:12–20PubMedCrossRef Bandettini PA, Wong EC, Jesmanowicz A et al (1994) Spin-echo and gradient-echo EPI of human brain activation using BOLD contrast: a comparative study at 1.5 T. NMR Biomed 7:12–20PubMedCrossRef
go back to reference Bianciardi M, Toschi N, Eichner C et al (2016) In vivo functional connectome of human brainstem nuclei of the ascending arousal, autonomic, and motor systems by high spatial resolution 7-Tesla fMRI. Magn Reson Mater Phys Biol Med 29:451–462. doi:10.1007/s10334-016-0546-3 CrossRef Bianciardi M, Toschi N, Eichner C et al (2016) In vivo functional connectome of human brainstem nuclei of the ascending arousal, autonomic, and motor systems by high spatial resolution 7-Tesla fMRI. Magn Reson Mater Phys Biol Med 29:451–462. doi:10.​1007/​s10334-016-0546-3 CrossRef
go back to reference Birbaumer N, Elbert T, Canavan AG, Rockstroh B (1990) Slow potentials of the cerebral cortex and behavior. Physiol Rev 70:1–41PubMedCrossRef Birbaumer N, Elbert T, Canavan AG, Rockstroh B (1990) Slow potentials of the cerebral cortex and behavior. Physiol Rev 70:1–41PubMedCrossRef
go back to reference Bloodstein O, Ratner NB (2008) A handbook on stuttering, 6th edn. Delmar Learning, Clifton Park Bloodstein O, Ratner NB (2008) A handbook on stuttering, 6th edn. Delmar Learning, Clifton Park
go back to reference Bothe AK, Franic DM, Ingham RJ, Davidow JH (2008) Pharmacological approaches to stuttering treatment: reply to Meline and Harn (2008). Am J Speech Lang Pathol 17:98–101CrossRef Bothe AK, Franic DM, Ingham RJ, Davidow JH (2008) Pharmacological approaches to stuttering treatment: reply to Meline and Harn (2008). Am J Speech Lang Pathol 17:98–101CrossRef
go back to reference Burns D, Brady JP, Kuruvilla K (1978) The acute effect of haloperidol and apomorphine on the severity of stuttering. Biol Psychiatry 13:255–264PubMed Burns D, Brady JP, Kuruvilla K (1978) The acute effect of haloperidol and apomorphine on the severity of stuttering. Biol Psychiatry 13:255–264PubMed
go back to reference Chang, Erickson KI, Ambrose NG et al (2008) Brain anatomy differences in childhood stuttering. Neuroimage 39:1333PubMedCrossRef Chang, Erickson KI, Ambrose NG et al (2008) Brain anatomy differences in childhood stuttering. Neuroimage 39:1333PubMedCrossRef
go back to reference Crone NE, Miglioretti DL, Gordon B et al (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain J Neurol 121(Pt 12):2271–2299CrossRef Crone NE, Miglioretti DL, Gordon B et al (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain J Neurol 121(Pt 12):2271–2299CrossRef
go back to reference Dahlstroem A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. Acta Physiol Scand Suppl SUPPL 232:1–55 Dahlstroem A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. Acta Physiol Scand Suppl SUPPL 232:1–55
go back to reference Deniau JM, Mailly P, Maurice N, Charpier S (2007) The pars reticulata of the substantia nigra: a window to basal ganglia output. Prog Brain Res 160:151–172PubMedCrossRef Deniau JM, Mailly P, Maurice N, Charpier S (2007) The pars reticulata of the substantia nigra: a window to basal ganglia output. Prog Brain Res 160:151–172PubMedCrossRef
go back to reference Foundas AL, Bollich AM, Corey DM et al (2001) Anomalous anatomy of speech-language areas in adults with persistent developmental stuttering. Neurology 57:207–215PubMedCrossRef Foundas AL, Bollich AM, Corey DM et al (2001) Anomalous anatomy of speech-language areas in adults with persistent developmental stuttering. Neurology 57:207–215PubMedCrossRef
go back to reference Kent RD (2000) Research on speech motor control and its disorders: a review and prospective. J Commun Disord 33:391–428PubMedCrossRef Kent RD (2000) Research on speech motor control and its disorders: a review and prospective. J Commun Disord 33:391–428PubMedCrossRef
go back to reference Lancaster JL, Woldorff MG, Parsons LM et al (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120–131PubMedCrossRef Lancaster JL, Woldorff MG, Parsons LM et al (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120–131PubMedCrossRef
go back to reference Lancaster JL, Tordesillas-Gutiérrez D, Martinez M et al (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205. doi:10.1002/hbm.20345 PubMedCrossRef Lancaster JL, Tordesillas-Gutiérrez D, Martinez M et al (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205. doi:10.​1002/​hbm.​20345 PubMedCrossRef
go back to reference Ludlow CL, Loucks T (2003) Stuttering: a dynamic motor control disorder. J Fluen Disord 28:273–295 (quiz 295) CrossRef Ludlow CL, Loucks T (2003) Stuttering: a dynamic motor control disorder. J Fluen Disord 28:273–295 (quiz 295) CrossRef
go back to reference Lütcke H, Gevensleben H, Albrecht B, Frahm J (2008) Brain networks involved in early versus late response anticipation and their relation to conflict processing. J Cogn Neurosci 21:2172–2184. doi:10.1162/jocn.2008.21165 CrossRef Lütcke H, Gevensleben H, Albrecht B, Frahm J (2008) Brain networks involved in early versus late response anticipation and their relation to conflict processing. J Cogn Neurosci 21:2172–2184. doi:10.​1162/​jocn.​2008.​21165 CrossRef
go back to reference Maguire G, Franklin D, Vatakis NG et al (2010) Exploratory randomized clinical study of pagoclone in persistent developmental stuttering: the examining pagoclone for persistent developmental stuttering study. J Clin Psychopharmacol 30:48-56. doi:10.1097/JCP.0b013e3181caebbe PubMedCrossRef Maguire G, Franklin D, Vatakis NG et al (2010) Exploratory randomized clinical study of pagoclone in persistent developmental stuttering: the examining pagoclone for persistent developmental stuttering study. J Clin Psychopharmacol 30:48-56. doi:10.​1097/​JCP.​0b013e3181caebbe​ PubMedCrossRef
go back to reference Neef NE (2013) Reduced dynamic range to tune the sensory-motor coupling on the left, at least in males who stutter. Presented at the ASHA Convention 2013-Updated Perspectives on the Neural Bases of Stuttering: Sensory & Motor Mechanisms Underlying Dysfluent Speech, November 14–16, 2013, Chicago Neef NE (2013) Reduced dynamic range to tune the sensory-motor coupling on the left, at least in males who stutter. Presented at the ASHA Convention 2013-Updated Perspectives on the Neural Bases of Stuttering: Sensory & Motor Mechanisms Underlying Dysfluent Speech, November 14–16, 2013, Chicago
go back to reference Poldrack RA, Mumford JA, Nichols TE (2011) Handbook of functional MRI data analysis. Cambridge University Press, CambridgeCrossRef Poldrack RA, Mumford JA, Nichols TE (2011) Handbook of functional MRI data analysis. Cambridge University Press, CambridgeCrossRef
go back to reference Riley G (2008) SSI-4: Stuttering Severity Instrument. PROED Riley G (2008) SSI-4: Stuttering Severity Instrument. PROED
go back to reference Shahed J, Jankovic J (2001) Re-emergence of childhood stuttering in Parkinson’s disease: a hypothesis. Mov Disord 16:114–118PubMedCrossRef Shahed J, Jankovic J (2001) Re-emergence of childhood stuttering in Parkinson’s disease: a hypothesis. Mov Disord 16:114–118PubMedCrossRef
go back to reference Tepper JM, Lee CR (2007) GABAergic control of substantia nigra dopaminergic neurons. Prog Brain Res 160:189–208PubMedCrossRef Tepper JM, Lee CR (2007) GABAergic control of substantia nigra dopaminergic neurons. Prog Brain Res 160:189–208PubMedCrossRef
go back to reference Walker HC, Phillips DE, Boswell DB et al (2009) Relief of acquired stuttering associated with Parkinson’s disease by unilateral left subthalamic brain stimulation. J Speech Lang Hear Res 52:1652–1657PubMedCrossRef Walker HC, Phillips DE, Boswell DB et al (2009) Relief of acquired stuttering associated with Parkinson’s disease by unilateral left subthalamic brain stimulation. J Speech Lang Hear Res 52:1652–1657PubMedCrossRef
go back to reference Walter WG, Cooper R, Aldridge VJ et al (1964) Contingent negative variation: an electric sign of sensori-motor association and expectancy in the human brain. Nature 203:380–384. doi:10.1038/203380a0 PubMedCrossRef Walter WG, Cooper R, Aldridge VJ et al (1964) Contingent negative variation: an electric sign of sensori-motor association and expectancy in the human brain. Nature 203:380–384. doi:10.​1038/​203380a0 PubMedCrossRef
go back to reference Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds) Functional MRI: An Introduction to Methods. OUP Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds) Functional MRI: An Introduction to Methods. OUP
go back to reference Wu JC, Maguire G, Riley G et al (1995) A positron emission tomography [18F]deoxyglucose study of developmental stuttering. Neuroreport 6:501–505PubMedCrossRef Wu JC, Maguire G, Riley G et al (1995) A positron emission tomography [18F]deoxyglucose study of developmental stuttering. Neuroreport 6:501–505PubMedCrossRef
go back to reference Wu JC, Maguire G, Riley G et al (1997) Increased dopamine activity associated with stuttering. Neuroreport 8:767–770PubMedCrossRef Wu JC, Maguire G, Riley G et al (1997) Increased dopamine activity associated with stuttering. Neuroreport 8:767–770PubMedCrossRef
go back to reference Yairi E, Ambrose NG (1999) Early childhood stuttering I: persistency and recovery rates. J Speech Lang Hear Res 42:1097–1112PubMedCrossRef Yairi E, Ambrose NG (1999) Early childhood stuttering I: persistency and recovery rates. J Speech Lang Hear Res 42:1097–1112PubMedCrossRef
Metadata
Title
Shifted dynamic interactions between subcortical nuclei and inferior frontal gyri during response preparation in persistent developmental stuttering
Authors
F. Luise Metzger
Tibor Auer
Gunther Helms
Walter Paulus
Jens Frahm
Martin Sommer
Nicole E. Neef
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1476-1

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