Skip to main content
Erschienen in: Brain Structure and Function 1/2017

12.12.2015 | Short Communication

Sustained enhancements in inhibitory control depend primarily on the reinforcement of fronto-basal anatomical connectivity

verfasst von: Camille Chavan, Michael Mouthon, Marie Simonet, Henri-Marcel Hoogewoud, Bogdan Draganski, Wietske van der Zwaag, Lucas Spierer

Erschienen in: Brain Structure and Function | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

What are the neurophysiological determinants of sustained supra-normal inhibitory control performance? We addressed this question by coupling multimodal neuroimaging and behavioral investigations of experts in fencing who underwent more than 20,000 h of inhibitory control training over 15 years. The superior control of the experts manifested behaviorally as a speeding-up of inhibition processes during a Go/NoGo task and was accompanied by changes in bilateral inferior frontal white matter microstructure. In the expert group, inhibition performance correlated positively with the fractional anisotropy (FA) of white matter tracts projecting to the basal ganglia, and the total training load with the FA in supplementary motor areas. Critically, the experts showed no changes in grey matter volume or in the functional organization of the fronto-basal inhibitory control network. The fencers’ performance and neural activity during a 2-back working memory task did not differ from those of the controls, ensuring that their expertise was specific to inhibitory control. Our results indicate that while phasic changes in the patterns of neural activity and grey matter architecture accompany inhibitory control improvement after short- to medium- term training, long-lasting inhibitory control improvements primarily depend on the reinforcement of fronto-basal structural connectivity.
Literatur
Zurück zum Zitat Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38(1):95–113CrossRefPubMed Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38(1):95–113CrossRefPubMed
Zurück zum Zitat Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. [Research Support, Non-US Gov’t Review]. NMR Biomed 15(7–8):435–455. doi:10.1002/nbm.782 CrossRefPubMed Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. [Research Support, Non-US Gov’t Review]. NMR Biomed 15(7–8):435–455. doi:10.​1002/​nbm.​782 CrossRefPubMed
Zurück zum Zitat Chan JSY, Wong AC-N, Liu Y, Yu J, Yan JH (2011) Fencing expertise and physical fitness enhance action inhibition. Psychol Sport Exerc 1212(5):509–514CrossRef Chan JSY, Wong AC-N, Liu Y, Yu J, Yan JH (2011) Fencing expertise and physical fitness enhance action inhibition. Psychol Sport Exerc 1212(5):509–514CrossRef
Zurück zum Zitat Chavan CF, Mouthon M, Draganski B, van der Zwaag W, Spierer L (2015) Differential patterns of functional and structural plasticity within and between inferior frontal gyri support training-induced improvements in inhibitory control proficiency. Hum Brain Mapp. doi:10.1002/hbm.22789 PubMed Chavan CF, Mouthon M, Draganski B, van der Zwaag W, Spierer L (2015) Differential patterns of functional and structural plasticity within and between inferior frontal gyri support training-induced improvements in inhibitory control proficiency. Hum Brain Mapp. doi:10.​1002/​hbm.​22789 PubMed
Zurück zum Zitat Hartmann L, Sallard E, Spierer L (2015) Enhancing frontal top-down inhibitory control with Go/NoGo training. Brain Struct Funct [Epub ahead of print] PMID: 26459141 Hartmann L, Sallard E, Spierer L (2015) Enhancing frontal top-down inhibitory control with Go/NoGo training. Brain Struct Funct [Epub ahead of print] PMID: 26459141
Zurück zum Zitat Johnstone T, Ores Walsh KS, Greischar LL, Alexander AL, Fox AS, Davidson RJ, Oakes TR (2006) Motion correction and the use of motion covariates in multiple-subject fMRI analysis. [Research Support, N.I.H., Extramural]. Hum Brain Mapp 27(10):779–788. doi:10.1002/hbm.20219 CrossRefPubMed Johnstone T, Ores Walsh KS, Greischar LL, Alexander AL, Fox AS, Davidson RJ, Oakes TR (2006) Motion correction and the use of motion covariates in multiple-subject fMRI analysis. [Research Support, N.I.H., Extramural]. Hum Brain Mapp 27(10):779–788. doi:10.​1002/​hbm.​20219 CrossRefPubMed
Zurück zum Zitat Lee KM, Chang KH, Roh JK (1999) Subregions within the supplementary motor area activated at different stages of movement preparation and execution. Neuroimage 9(1):117–123CrossRefPubMed Lee KM, Chang KH, Roh JK (1999) Subregions within the supplementary motor area activated at different stages of movement preparation and execution. Neuroimage 9(1):117–123CrossRefPubMed
Zurück zum Zitat Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21(1):450–455CrossRefPubMed Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21(1):450–455CrossRefPubMed
Zurück zum Zitat Manuel AL, Bernasconi F, Spierer L (2013) Plastic modifications within inhibitory control networks induced by practicing a stop-signal task: an electrical neuroimaging study [Research Support, Non-US Gov’t]. Cortex 49(4):1141–1147. doi:10.1016/j.cortex.2012.12.009 CrossRefPubMed Manuel AL, Bernasconi F, Spierer L (2013) Plastic modifications within inhibitory control networks induced by practicing a stop-signal task: an electrical neuroimaging study [Research Support, Non-US Gov’t]. Cortex 49(4):1141–1147. doi:10.​1016/​j.​cortex.​2012.​12.​009 CrossRefPubMed
Zurück zum Zitat Mechelli A, Henson RN, Price CJ, Friston KJ (2003) Comparing event-related and epoch analysis in blocked design fMRI. Neuroimage 18(3):806–810CrossRefPubMed Mechelli A, Henson RN, Price CJ, Friston KJ (2003) Comparing event-related and epoch analysis in blocked design fMRI. Neuroimage 18(3):806–810CrossRefPubMed
Zurück zum Zitat Nachev P, Wydell H, O’neill K, Husain M, Kennard C (2007) The role of the pre-supplementary motor area in the control of action. Neuroimage 36(Suppl 2):T155–T163CrossRefPubMedPubMedCentral Nachev P, Wydell H, O’neill K, Husain M, Kennard C (2007) The role of the pre-supplementary motor area in the control of action. Neuroimage 36(Suppl 2):T155–T163CrossRefPubMedPubMedCentral
Zurück zum Zitat Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. [Research Support, Non-US Gov’t]. Hum Brain Mapp 15(1):1–25CrossRefPubMed Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. [Research Support, Non-US Gov’t]. Hum Brain Mapp 15(1):1–25CrossRefPubMed
Zurück zum Zitat Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113CrossRefPubMed Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113CrossRefPubMed
Zurück zum Zitat Roi GS, Bianchedi D (2008) The science of fencing: implications for performance and injury prevention [Review]. Sports Med 38(6):465–481CrossRefPubMed Roi GS, Bianchedi D (2008) The science of fencing: implications for performance and injury prevention [Review]. Sports Med 38(6):465–481CrossRefPubMed
Zurück zum Zitat Simmonds DJ, Pekar JJ, Mostofsky SH (2008) Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46(1):224–232CrossRefPubMed Simmonds DJ, Pekar JJ, Mostofsky SH (2008) Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46(1):224–232CrossRefPubMed
Zurück zum Zitat Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, Miller KL, Behrens TE (2007) Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. [Research Support, Non-US Gov’t]. Nat Protoc 2(3):499–503. doi:10.1038/nprot.2007.45 CrossRefPubMed Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, Miller KL, Behrens TE (2007) Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. [Research Support, Non-US Gov’t]. Nat Protoc 2(3):499–503. doi:10.​1038/​nprot.​2007.​45 CrossRefPubMed
Zurück zum Zitat 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. doi:10.1006/nimg.2001.0978 CrossRefPubMed 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. doi:10.​1006/​nimg.​2001.​0978 CrossRefPubMed
Zurück zum Zitat Waxman SG (1980) Determinants of conduction velocity in myelinated nerve fibers. Muscle Nerve 3:141–150CrossRefPubMed Waxman SG (1980) Determinants of conduction velocity in myelinated nerve fibers. Muscle Nerve 3:141–150CrossRefPubMed
Zurück zum Zitat White CN, Congdon E, Mumford JA, Karlsgodt KH, Sabb FW, Freimer NB, Poldrack RA (2014) Decomposing decision components in the stop-signal task: a model-based approach to individual differences in inhibitory control. [Research Support, N.I.H., Extramural Research Support, Non-US Gov’t]. J Cogn Neurosci 26(8):1601–1614. doi:10.1162/jocn_a_00567 CrossRefPubMedPubMedCentral White CN, Congdon E, Mumford JA, Karlsgodt KH, Sabb FW, Freimer NB, Poldrack RA (2014) Decomposing decision components in the stop-signal task: a model-based approach to individual differences in inhibitory control. [Research Support, N.I.H., Extramural Research Support, Non-US Gov’t]. J Cogn Neurosci 26(8):1601–1614. doi:10.​1162/​jocn_​a_​00567 CrossRefPubMedPubMedCentral
Metadaten
Titel
Sustained enhancements in inhibitory control depend primarily on the reinforcement of fronto-basal anatomical connectivity
verfasst von
Camille Chavan
Michael Mouthon
Marie Simonet
Henri-Marcel Hoogewoud
Bogdan Draganski
Wietske van der Zwaag
Lucas Spierer
Publikationsdatum
12.12.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2017
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-015-1156-y

Weitere Artikel der Ausgabe 1/2017

Brain Structure and Function 1/2017 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Neu im Fachgebiet Neurologie

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.