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01-01-2022 | Magnetic Resonance Imaging | Original Article

Imaging functional neuroplasticity in human white matter tracts

Authors: Tory O. Frizzell, Elisha Phull, Mishaa Khan, Xiaowei Song, Lukas A. Grajauskas, Jodie Gawryluk, Ryan C. N. D’Arcy

Published in: Brain Structure and Function | Issue 1/2022

Abstract

Magnetic resonance imaging (MRI) studies are sensitive to biological mechanisms of neuroplasticity in white matter (WM). In particular, diffusion tensor imaging (DTI) has been used to investigate structural changes. Historically, functional MRI (fMRI) neuroplasticity studies have been restricted to gray matter, as fMRI studies have only recently expanded to WM. The current study evaluated WM neuroplasticity pre–post motor training in healthy adults, focusing on motor learning in the non-dominant hand. Neuroplasticity changes were evaluated in two established WM regions-of-interest: the internal capsule and the corpus callosum. Behavioral improvements following training were greater for the non-dominant hand, which corresponded with MRI-based neuroplasticity changes in the internal capsule for DTI fractional anisotropy, fMRI hemodynamic response functions, and low-frequency oscillations (LFOs). In the corpus callosum, MRI-based neuroplasticity changes were detected in LFOs, DTI, and functional correlation tensors (FCT). Taken together, the LFO results converged as significant amplitude reductions, implicating a common underlying mechanism of optimized transmission through altered myelination. The structural and functional neuroplasticity findings open new avenues for direct WM investigations into mapping connectomes and advancing MRI clinical applications.

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Andersson JLR, Sotiropoulos SN (2015) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125(2016):1063–1078. https://doi.org/10.1016/j.neuroimage.2015.10.019CrossRefPubMed

Biswal B, Zerrin Yetkin F, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar Mri. Magn Reson Med 34(4):537–541. https://doi.org/10.1002/mrm.1910340409CrossRefPubMed

Bonzano L, Tacchino A, Roccatagliata L, Abbruzzese G, Mancardi GL, Bove M (2008) Callosal contributions to simultaneous bimanual finger movements. J Neurosci 28(12):3227–3233. https://doi.org/10.1523/JNEUROSCI.4076-07.2008CrossRefPubMedPubMedCentral

Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929. https://doi.org/10.1126/science.1099745CrossRefPubMed

Caillé S, Sauerwein HC, Schiavetto A, Villemure JG, Lassonde M (2005) Sensory and motor interhemispheric integration after section of different portions of the anterior corpus callosum in nonepileptic patients. Neurosurgery 57(1):50–58. https://doi.org/10.1227/01.NEU.0000163089.31657.08CrossRefPubMed

Chang Y (2014) Reorganization and plastic changes of the human brain associated with skill learning and expertise. Front Hum Neurosci 8:1–7. https://doi.org/10.3389/fnhum.2014.00035CrossRef

Courtemanche M, Sparrey C, Song X, McKay A, D’Arcy RCN (2018) Detecting white matter activity using conventional 3 Tesla fMRI: an evaluation of standard field strength and hemodynamic response function. Neuroimage 169:145–150. https://doi.org/10.1016/j.neuroimage.2017.12.008CrossRefPubMed

D’Arcy RCN, Hamilton A, Jarmasz M, Sullivan S, Stroink G (2006) Exploratory data analysis reveals visuovisual interhemispheric transfer in functional magnetic resonance imaging. Magn Reson Med 55(4):952–958. https://doi.org/10.1002/mrm.20839CrossRefPubMed

D’Arcy RCN, Lindsay DS, Song X, Gawryluk JR, Greene D, Mayo C, Hajra SG et al (2016) Long-term motor recovery after severe traumatic brain injury: beyond established limits. J Head Trauma Rehabil 31(5):E50-58. https://doi.org/10.1097/HTR.0000000000000185CrossRefPubMed

Deng F, Zhao L, Liu C, Min Lu, Zhang S, Huang H, Chen L et al (2018) Plasticity in deep and superficial white matter: a DTI study in world class gymnasts. Brain Struct Funct 223(4):1849–1862. https://doi.org/10.1007/s00429-017-1594-9CrossRefPubMed

Ding Z, Newton AT, Xu R, Anderson AW, Morgan VL, Gore JC (2013) Spatio-temporal correlation tensors reveal functional structure in human brain. PLoS ONE. https://doi.org/10.1371/journal.pone.0082107CrossRefPubMedPubMedCentral

Ding Z, Ran Xu, Bailey SK, Tung Lin Wu, Morgan VL, Cutting LE, Anderson AW, Gore JC (2016) Visualizing functional pathways in the human brain using correlation tensors and magnetic resonance imaging. Magn Reson Imaging 34(1):8–17. https://doi.org/10.1016/j.mri.2015.10.003CrossRefPubMed

Dodd K, Nair VA, Prabhakaran V (2017) Role of the contralesional vs ipsilesional hemisphere in stroke recovery. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2017.00469CrossRefPubMedPubMedCentral

Fabri M (2014) Functional topography of the corpus callosum investigated by DTI and FMRI. World J Radiol 6(12):895. https://doi.org/10.4329/wjr.v6.i12.895CrossRefPubMedPubMedCentral

Fabri M, Polonara G (2013) Functional topography of human corpus callosum: an FMRI mapping study. Neural Plast. https://doi.org/10.1155/2013/251308CrossRefPubMedPubMedCentral

Fabri M, Polonara G, Mascioli G, Salvolini U, Manzoni T (2011) Topographical organization of human corpus callosum: an FMRI mapping study. Brain Res 1370:99–111. https://doi.org/10.1016/j.brainres.2010.11.039CrossRefPubMed

Faragó P, Tóth E, Kocsis K, Kincses B, Veréb D, Király A, Bozsik B et al (2019) Altered resting state functional activity and microstructure of the white matter in migraine with aura. Front Neurol. https://doi.org/10.3389/fneur.2019.01039CrossRefPubMedPubMedCentral

Fickling S, Greene T, Greene D, Frehlick Z, Campbell N, Etheridge T, Smith CJ, Bollinger F, Danilov Y, Rizzotti R, Livingstone AC, Lakhani B, D’Arcy RCN (2020) Brain vital signs detect cognitive improvements during combined physical therapy and neuromodulation in rehabilitation from severe traumatic brain injury: a case report. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2020.00347CrossRefPubMedPubMedCentral

Fields RD (2011) Change in the brain’s white matter: the role of the brain’s white matter in active learning and memory may be underestimated. Science 330(6005):768–769. https://doi.org/10.1126/science.1199139.ChangeCrossRef

Fields RD (2015) A new mechanism of nervous system plasticity: activity-dependent myelination. Nat Rev Neurosci 16(12):756–767. https://doi.org/10.1038/nrn4023CrossRefPubMedPubMedCentral

Foster AY, Bujalka H, Emery B (2019) Axoglial interactions in myelin plasticity: evaluating the relationship between neuronal activity and oligodendrocyte dynamics. Wiley, New York. https://doi.org/10.1002/glia.23629CrossRef

Frizzell T, Grajauskas LA, Liu CC, Hajra SG, Song X, D’Arcy RCN (2020) White matter neuroplasticity: motor learning activates the internal capsule and reduces hemodynamic response variability. Font Hum Neurosci 14:509258CrossRef

Fryer SL, Roach BJ, Wiley K, Loewy RL, Ford JM, Mathalon DH (2016) Reduced amplitude of low-frequency brain oscillations in the psychosis risk syndrome and early illness schizophrenia. Neuropsychopharmacology 41(9):2388–2398. https://doi.org/10.1038/npp.2016.51CrossRefPubMedPubMedCentral

Gawryluk JR, D’Arcy RCN, Mazerolle EL, Brewer KD, Beyea SD (2011a) Functional mapping in the corpus callosum: a 4T FMRI study of white matter. Neuroimage 54(1):10–15. https://doi.org/10.1016/j.neuroimage.2010.07.028CrossRefPubMed

Gawryluk JR, Mazerolle EL, Brewer KD, Beyea SD, D’Arcy RCN (2011b) Investigation of FMRI activation in the internal capsule. BMC Neurosci 12(1):56. https://doi.org/10.1186/1471-2202-12-56CrossRefPubMedPubMedCentral

Gawryluk JR, Mazerolle EL, D’Arcy RCN (2014) Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions. Front Neurosci 8:1–12. https://doi.org/10.3389/fnins.2014.00239CrossRef

Grajauskas LA, Frizzell T, Song X, D’Arcy RCN (2019) White matter fmri activation cannot be treated as a nuisance regressor: overcoming a historical blind spot. Front Neurosci. https://doi.org/10.3389/fnins.2019.01024CrossRefPubMedPubMedCentral

Hamaide J, de Groof G, van der Linden A (2016) Neuroplasticity and MRI: a perfect match. Neuroimage 131:13–28. https://doi.org/10.1016/j.neuroimage.2015.08.005CrossRefPubMed

Ji GJ, Liao W, Chen FF, Zhang L, Wang K (2017) Low-frequency blood oxygen level-dependent fluctuations in the brain white matter: more than just noise. Sci Bull 62(9):656–657. https://doi.org/10.1016/j.scib.2017.03.021CrossRef

Jiang Y, Luo C, Li X, Li Y, Yang H, Li J, Chang X et al (2019) White-matter functional networks changes in patients with schizophrenia. Neuroimage 190:172–181. https://doi.org/10.1016/j.neuroimage.2018.04.018CrossRefPubMed

Jiang Y, Luo C, Li X, Huang H, Zhao G, Li X, Li S, Song X, Yao D, Duan M (2021) Function-structure coupling: white matter FMRI hyper-activation associates with structural integrity reductions in schizophrenia. Hum Brain Mapp 42(12):4022–4034. https://doi.org/10.1002/hbm.25536CrossRefPubMedPubMedCentral

Keller TA, Just MA (2016) Structural and functional neuroplasticity in human learning of spatial routes. Neuroimage 125:256–266. https://doi.org/10.1016/j.neuroimage.2015.10.015CrossRefPubMed

Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M (2009) Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci USA 106(41):17558–17563. https://doi.org/10.1073/pnas.0902455106CrossRefPubMedPubMedCentral

Li M, Newton AT, Anderson AW, Ding Z, Gore JC (2019) Characterization of the hemodynamic response function in white matter tracts for event-related FMRI. Nat Commun 10(1):1140. https://doi.org/10.1038/s41467-019-09076-2CrossRefPubMedPubMedCentral

Li M, Gao Y, Ding Z, Gore JC (2021) Power spectra reveal distinct BOLD resting-state time courses in white matter. PNAS. https://doi.org/10.1101/2021.02.24.432346CrossRefPubMedPubMedCentral

Maldjian JA, Gottschalk A, Detre JA, Alsop D (1999) Basal ganglia and white matter activation using functional MRI at 4 Tesla. In: Proceedings of the 7th annual meeting of the international society of magnetic resonance in medicine, Philadelphia, USA.

Mather M, Nga L (2013) Age differences in thalamic low-frequency fluctuations. NeuroReport 24(7):349–353. https://doi.org/10.1097/WNR.0b013e32835f6784CrossRefPubMedPubMedCentral

Mazerolle EL, D’Arcy RCN, Beyea SD (2008) Detecting functional magnetic resonance imaging activation in white matter: interhemispheric transfer across the corpus callosum. BMC Neurosci. https://doi.org/10.1186/1471-2202-9-84CrossRefPubMedPubMedCentral

Mazerolle EL, Beyea SD, Gawryluk JR, Brewer KD, Bowen CV, D’Arcy RCN (2010) Confirming white matter FMRI activation in the corpus callosum: co-localization with DTI tractography. Neuroimage 50(2):616–621. https://doi.org/10.1016/j.neuroimage.2009.12.102CrossRefPubMed

Mazerolle EL, Kim JRG, Dillen NH, Patterson SA, Feindel KW, Beyea SD, Stevens M et al (2013) Sensitivity to white matter FMRI activation increases with field strength. PLoS ONE 8(3):1–12. https://doi.org/10.1371/journal.pone.0058130CrossRef

Mishra A, Li M, Anderson AW, Newton AT, Ding Z, Gore JC (2020) Concomitant modulation of BOLD responses in white matter pathways and cortex. Neuroimage 216:116791. https://doi.org/10.1016/j.neuroimage.2020.116791CrossRefPubMed

Mosier KM, Liu WC, Maldjian JA, Shah R, Modi B (1999) Lateralization of cortical function in swallowing: a functional MR imaging study. Am J Neuroradiol 20(8):1520–1526PubMedPubMedCentral

Niu C, Zhang M, Min Z, Rana N, Zhang Q, Liu X, Li M, Lin P (2014) Motor network plasticity and low-frequency oscillations abnormalities in patients with brain gliomas: a functional MRI study. PLoS ONE 9(5):e96850. https://doi.org/10.1371/journal.pone.0096850CrossRefPubMedPubMedCentral

Pernice V, Staude B, Cardanobile S, Rotter S (2011) How structure determines correlations in neuronal networks. PLoS Comput Biol 7(5):1002059. https://doi.org/10.1371/journal.pcbi.1002059CrossRef

Reid LB, Sale MV, Cunnington R, Mattingley JB, Rose SE (2017) Brain changes following four weeks of unimanual motor training: evidence from FMRI-guided diffusion MRI tractography. Hum Brain Mapp 38(9):4302–4312. https://doi.org/10.1002/hbm.23514CrossRefPubMedPubMedCentral

Sale MV, Reid LB, Cocchi L, Pagnozzi AM, Rose SE, Mattingley JB (2017) Brain changes following four weeks of unimanual motor training: evidence from behavior, neural stimulation, cortical thickness, and functional MRI. Hum Brain Mapp 38(9):4773–4787. https://doi.org/10.1002/hbm.23710CrossRefPubMedPubMedCentral

Sampaio-Baptista C, Johansen-Berg H (2017) White matter plasticity in the adult brain. Neuron 96(6):1239–1251. https://doi.org/10.1016/j.neuron.2017.11.026CrossRefPubMedPubMedCentral

Sarma MK, Pal A, Keller MA, Welikson T, Ventura J, Michalik DE, Nielsen-Saines K et al (2021) White matter of perinatally HIV infected older youths shows low frequency fluctuations that may reflect glial cycling. Sci Rep 11(1):3086. https://doi.org/10.1038/s41598-021-82587-5CrossRefPubMedPubMedCentral

Scholz J, Klein MC, Behrens TEJ, Johansen-Berg H (2009) Training induces changes in white-matter architecture. Nat Neurosci 12(11):1370CrossRefPubMedPubMedCentral

Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155. https://doi.org/10.1002/hbm.10062CrossRefPubMedPubMedCentral

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL technical report TR04SS2. www.fmrib.ox.ac.uk/analysis.

Steele CJ, Bailey JA, Zatorre RJ, Penhune VB (2013) Early musical training and white-matter plasticity in the corpus callosum: evidence for a sensitive period. J Neurosci 33(3):1282–1290CrossRefPubMedPubMedCentral

Tettamanti M, Paulesu E, Scifo P, Maravita A, Fazio F, Perani D, Marzi CA (2002) Interhemispheric transmission of visuomotor information in humans: FMRI evidence. J Neurophysiol. https://doi.org/10.1152/jn.00417.2001CrossRefPubMed

Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, Cassol E, Chollet F (2004) A longitudinal FMRI study. In recovering and then in clinically stable sub-cortical stroke patients. Neuroimage 23(3):827–839. https://doi.org/10.1016/j.neuroimage.2004.07.058CrossRefPubMed

Vien C, Boré A, Lungu O, Benali H, Carrier J, Fogel S, Doyon J (2016) Age-related white-matter correlates of motor sequence learning and consolidation. Neurobiol Aging 48:13–22. https://doi.org/10.1016/j.neurobiolaging.2016.08.006CrossRefPubMed

Wang P, Meng C, Yuan R, Wang J, Yang H, Zhang T, Zaborszky L et al (2020a) The organization of the human corpus callosum estimated by intrinsic functional connectivity with white-matter functional networks. Cereb Cortex 30(5):3313–3324. https://doi.org/10.1093/cercor/bhz311CrossRefPubMed

Wang T, Mitchell Wilkes D, Li M, Xi Wu, Gore JC, Ding Z (2020b) Hemodynamic response function in brain white matter in a resting state. Cereb Cortex Commun 1(1):1–13. https://doi.org/10.1093/texcom/tgaa056CrossRef

Weber B, Treyer V, Oberholzer N, Jaermann T, Boesiger P, Brugger P, Regard M, Buck A, Savazzi S, Marzi CA (2005) Attention and interhemispheric transfer: a behavioral and f MRI study. J Cogn Neurosci 17:113–123CrossRefPubMed

Woolrich MW, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14(2001):1370–1386. https://doi.org/10.1006/nimg.2001.0931CrossRefPubMed

Wu TL, Wang F, Anderson AW, Chen LM, Ding Z, Gore JC (2016) Effects of anesthesia on resting state BOLD signals in white matter of non-human primates. Magn Reson Imaging 34(9):1235–1241. https://doi.org/10.1016/j.mri.2016.07.001CrossRefPubMedPubMedCentral

Xu G, Yin Xu, Gaohong Wu, Antuono PG, Hammeke TA, Li SJ (2006) Task-modulation of functional synchrony between spontaneous low-frequency oscillations in the human brain detected by FMRI. Magn Reson Med 56(1):41–50. https://doi.org/10.1002/mrm.20932CrossRefPubMed

Zhan J, Gao L, Zhou F, Bai L, Kuang H, He L, Zeng X, Gong H (2016) Amplitude of low-frequency fluctuations in multiple-frequency bands in acute mild traumatic brain injury. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2016.00027CrossRefPubMedPubMedCentral

Zhang L, Zhang H, Chen X, Wang Q, Yap PT, Shen D (2017) Learning-based structurally-guided construction of resting-state functional correlation tensors. Magn Reson Imaging 43:110–121. https://doi.org/10.1016/j.mri.2017.07.008CrossRefPubMedPubMedCentral

Zhou Y, Yap P-T, Zhang H, Zhang L, Feng Q, Shen D (2017) Improving functional MRI registration using whole-brain functional correlation tensors. Med Image Comput Comput Assist Interv 2:416–423. https://doi.org/10.1007/978-3-319-66182-7CrossRef

Zhou Y, Zhang H, Zhang L, Xiaohuan Cao Ru, Yang QF, Yap P-T, Shen D (2018) Functional MRI registration with tissue-specific patch-based functional correlation tensors. Hum Brain Mapp 39(6):2303–2316. https://doi.org/10.1002/hbm.24021CrossRefPubMedPubMedCentral

Zuo XN, di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, Xavier Castellanos F, Biswal BB, Milham MP (2010) The oscillating brain: complex and reliable. Neuroimage 49(2):1432–1445. https://doi.org/10.1016/j.neuroimage.2009.09.037CrossRefPubMed

Title: Imaging functional neuroplasticity in human white matter tracts
Authors: Tory O. Frizzell
Elisha Phull
Mishaa Khan
Xiaowei Song
Lukas A. Grajauskas
Jodie Gawryluk
Ryan C. N. D’Arcy
Publication date: 01-01-2022
Publisher: Springer Berlin Heidelberg
Keywords: Magnetic Resonance Imaging
Magnetic Resonance Imaging
Published in: Brain Structure and Function / Issue 1/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-021-02407-4

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Imaging functional neuroplasticity in human white matter tracts

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