Top

Published in:

Open Access 01-05-2018 | Original Article

Knowing left from right: asymmetric functional connectivity during resting state

Authors: Mathijs Raemaekers, Wouter Schellekens, Natalia Petridou, Nick F. Ramsey

Published in: Brain Structure and Function | Issue 4/2018

Abstract

The functional organization of left and right hemispheres is different, and hemispheric asymmetries are thought to underlie variations in brain function across individuals. In this study, we assess how differences between hemispheres are reflected in Asymmetric Functional Connectivity (AFC), which provides a full description of how the brain’s connectivity structure during resting state differs from that of the same brain mirrored over the longitudinal fissure. In addition, we assess how AFC varies across subjects. Data were provided by the Human Connectome Project, including 423 resting state and combined language task fMRI data sets, and the pattern of AFC was established for all subjects. While we could quantify the symmetry of brain connectivity at 95%, significant asymmetries were observed, consisting foremost of: (1) higher correlations between language areas in the left hemisphere than between their right hemisphere homologues. (2) Higher correlations between language homologue areas in the right hemisphere and left default mode network, than between language areas in the left hemisphere and the default mode network in the right hemisphere. The extent to which subjects exhibited this pattern correlated with language lateralization and handedness. Further exploration in intersubject variation in AFC revealed several additional patterns, one involving entire hemispheres, and another correlations with limbic areas. These results show that language is an important, but not only determinant of AFC. The additional patterns of AFC require further research to be linked to specific asymmetric neuronal states or events.

Available only for authorised users

Barch DM, Burgess GC, Harms MP et al (2013) Function in the human connectome: task-fMRI and individual differences in behavior. Neuroimage 80:169–189. https://doi.org/10.1016/j.neuroimage.2013.05.033 CrossRefPubMedPubMedCentral

Binder JR, Gross WL, Allendorfer JB et al (2011) Mapping anterior temporal lobe language areas with fMRI: a multicenter normative study. Neuroimage 54:1465–1475. https://doi.org/10.1016/j.neuroimage.2010.09.048 CrossRefPubMed

Biswal BB, Van Kylen J, Hyde JS (1997) Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR Biomed 10:165–170CrossRefPubMed

Broca P (1861) Remarques sur le siége de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bull la Société Anat 36:330–356

Burbaud P, Degreze P, Lafon P et al (1995) Lateralization of prefrontal activation during internal mental calculation: a functional magnetic resonance imaging study. J Neurophysiol 74:2194–2200CrossRefPubMed

Ciçek M, Deouell LY, Knight RT (2009) Brain activity during landmark and line bisection tasks. Front Hum Neurosci 3:7. https://doi.org/10.3389/neuro.09.007.2009 CrossRefPubMedPubMedCentral

Damoiseaux JS, Rombouts SARB, Barkhof F et al (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853. https://doi.org/10.1073/pnas.0601417103 CrossRefPubMedPubMedCentral

Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021 CrossRefPubMed

Fischl B (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22. https://doi.org/10.1093/cercor/bhg087 CrossRefPubMed

Flor-Henry P, Lind JC, Koles ZJ (2004) A source-imaging (low-resolution electromagnetic tomography) study of the EEGs from unmedicated males with depression. Psychiatry Res 130:191–207. https://doi.org/10.1016/j.pscychresns.2003.08.006 CrossRefPubMed

Fox MD, Corbetta M, Snyder AZ et al (2006) Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc Natl Acad Sci 103:10046–10051. https://doi.org/10.1073/pnas.0604187103 CrossRefPubMedPubMedCentral

Friston KJ (2011) Functional and effective connectivity: a review. Brain Connect 1:13–36. https://doi.org/10.1089/brain.2011.0008 CrossRefPubMed

Frith C (2005) The neural basis of hallucinations and delusions. C R Biol 328:169–175. https://doi.org/10.1016/j.crvi.2004.10.012 CrossRefPubMed

Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? Brain 123:1293–1326. https://doi.org/10.1093/brain/123.7.1293 CrossRefPubMed

Glasser MF, Sotiropoulos SN, Wilson JA et al (2013) The minimal preprocessing pipelines for the human connectome project. Neuroimage 80:105–124. https://doi.org/10.1016/j.neuroimage.2013.04.127 CrossRefPubMedPubMedCentral

Hasler R, Preti MG, Meskaldji DE et al (2017) Inter-hemispherical asymmetry in default-mode functional connectivity and BAIAP2 gene are associated with anger expression in ADHD adults. Psychiatry Res Neuroimaging 269:54–61. https://doi.org/10.1016/j.pscychresns.2017.09.004 CrossRefPubMed

Henriques JB, Davidson RJ (1991) Left frontal hypoactivation in depression. J Abnorm Psychol 100:535–545CrossRefPubMed

Hervé PY, Zago L, Petit L et al (2013) Revisiting human hemispheric specialization with neuroimaging. Trends Cogn Sci 17:80CrossRef

Jarbo K, Verstynen T, Schneider W (2012) In vivo quantification of global connectivity in the human corpus callosum. Neuroimage 59:1988–1996. https://doi.org/10.1016/j.neuroimage.2011.09.056 CrossRefPubMed

Joliot M, Tzourio-Mazoyer N, Mazoyer B (2016) Intra-hemispheric intrinsic connectivity asymmetry and its relationships with handedness and language Lateralization. Neuropsychologia 93:437–447. https://doi.org/10.1016/j.neuropsychologia.2016.03.013 CrossRefPubMed

Knecht S (2000) Handedness and hemispheric language dominance in healthy humans. Brain 123:2512–2518. https://doi.org/10.1093/brain/123.12.2512 CrossRefPubMed

Krueger F, Spampinato MV, Pardini M et al (2008) Integral calculus problem solving: an fMRI investigation. Neuroreport 19:1095–1099. https://doi.org/10.1097/WNR.0b013e328303fd85 CrossRefPubMedPubMedCentral

Liu H, Stufflebeam SM, Sepulcre J et al (2009) Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors. Proc Natl Acad Sci USA 106:20499–20503. https://doi.org/10.1073/pnas.0908073106 CrossRefPubMedPubMedCentral

Mathiak KA, Zvyagintsev M, Ackermann H, Mathiak K (2012) Lateralization of amygdala activation in fMRI may depend on phase-encoding polarity. MAGMA 25:177–182. https://doi.org/10.1007/s10334-011-0285-4 CrossRefPubMed

Mazoyer B, Zago L, Jobard G et al (2014) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS One 9:e101165. https://doi.org/10.1371/journal.pone.0101165 CrossRefPubMedPubMedCentral

McAvoy M, Mitra A, Coalson RS et al (2015) Unmasking language lateralization in human brain intrinsic activity. Cereb Cortex bhv007-. https://doi.org/10.1093/cercor/bhv007

Moore DW, Bhadelia RA, Billings RL et al (2009) Hemispheric connectivity and the visual-spatial divergent-thinking component of creativity. Brain Cogn 70:267–272. https://doi.org/10.1016/j.bandc.2009.02.011 CrossRefPubMed

Nielsen JA, Zielinski BA, Ferguson MA et al (2013) An evaluation of the left-brain vs. right-brain hypothesis with resting state functional connectivity magnetic resonance imaging. PLoS One 8:e71275. https://doi.org/10.1371/journal.pone.0071275 CrossRefPubMedPubMedCentral

Petridou N, Gaudes CC, Dryden IL et al (2013) Periods of rest in fMRI contain individual spontaneous events which are related to slowly fluctuating spontaneous activity. Hum Brain Mapp 34:1319–1329. https://doi.org/10.1002/hbm.21513 CrossRefPubMed

Pool E-M, Rehme AK, Eickhoff SB et al (2015) Functional resting-state connectivity of the human motor network: differences between right- and left-handers. Neuroimage 109:298–306. https://doi.org/10.1016/j.neuroimage.2015.01.034 CrossRefPubMedPubMedCentral

Raemaekers M, Schellekens W, van Wezel RJA et al (2014) Patterns of resting state connectivity in human primary visual cortical areas: a 7T fMRI study. Neuroimage 84:911–921. https://doi.org/10.1016/j.neuroimage.2013.09.060 CrossRefPubMed

Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449–476. https://doi.org/10.1146/annurev.neuro.29.051605.112819 CrossRefPubMed

Saenger VM, Barrios FA, Martínez-Gudiño ML, Alcauter S (2012) Hemispheric asymmetries of functional connectivity and grey matter volume in the default mode network. Neuropsychologia 50:1308–1315. https://doi.org/10.1016/j.neuropsychologia.2012.02.014 CrossRefPubMed

Santarnecchi E, Tatti E, Rossi S et al (2015) Intelligence-related differences in the asymmetry of spontaneous cerebral activity. Hum Brain Mapp 36:3586–3602. https://doi.org/10.1002/hbm.22864 CrossRefPubMed

Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428CrossRefPubMed

Singh KD, Fawcett IP (2008) Transient and linearly graded deactivation of the human default-mode network by a visual detection task. Neuroimage 41:100–112. https://doi.org/10.1016/j.neuroimage.2008.01.051 CrossRefPubMed

Skudlarski P, Jagannathan K, Calhoun VD et al (2008) Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations. Neuroimage 43:554–561. https://doi.org/10.1016/j.neuroimage.2008.07.063 CrossRefPubMedPubMedCentral

Smith SM, Fox PT, Miller KL et al (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045. https://doi.org/10.1073/pnas.0905267106 CrossRefPubMedPubMedCentral

Sporns O (2011) The human connectome: a complex network. Ann NY Acad Sci 1224:109–125. https://doi.org/10.1111/j.1749-6632.2010.05888.x CrossRefPubMed

Stephane M, Barton S, Boutros N (2001) Auditory verbal hallucinations and dysfunction of the neural substrates of speech. Schizophr Res 50:61–78. https://doi.org/10.1016/S0920-9964(00)00150-X CrossRefPubMed

Tzourio-Mazoyer N, Joliot M, Marie D, Mazoyer B (2015) Variation in homotopic areas’ activity and inter-hemispheric intrinsic connectivity with type of language lateralization: an FMRI study of covert sentence generation in 297 healthy volunteers. Brain Struct Funct. https://doi.org/10.1007/s00429-015-1068-x

Van Essen DC, Glasser MF, Dierker DL et al (2012a) Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. Cereb Cortex 22:2241–2262. https://doi.org/10.1093/cercor/bhr291 CrossRefPubMed

Van Essen DC, Ugurbil K, Auerbach E et al (2012b) The human connectome project: a data acquisition perspective. Neuroimage 62:2222–2231. https://doi.org/10.1016/j.neuroimage.2012.02.018 CrossRefPubMedPubMedCentral

Wang D, Buckner RL, Liu H (2014) Functional specialization in the human brain estimated by intrinsic hemispheric interaction. J Neurosci 34:12341–12352. https://doi.org/10.1523/JNEUROSCI.0787-14.2014 CrossRefPubMedPubMedCentral

Wilkinson D, Ko P, Wiriadjaja A et al (2009) Unilateral damage to the right cerebral hemisphere disrupts the apprehension of whole faces and their component parts. Neuropsychologia 47:1701–1711. https://doi.org/10.1016/j.neuropsychologia.2009.02.008 CrossRefPubMed

Xiao Y, Brauer J, Lauckner M et al (2016) Development of the intrinsic language network in preschool children from ages 3 to 5 years. PLoS One 11:e0165802. https://doi.org/10.1371/journal.pone.0165802 CrossRefPubMedPubMedCentral

Yovel G, Tambini A, Brandman T (2008) The asymmetry of the fusiform face area is a stable individual characteristic that underlies the left-visual-field superiority for faces. Neuropsychologia 46:3061–3068. https://doi.org/10.1016/j.neuropsychologia.2008.06.017 CrossRefPubMed

Title: Knowing left from right: asymmetric functional connectivity during resting state
Authors: Mathijs Raemaekers
Wouter Schellekens
Natalia Petridou
Nick F. Ramsey
Publication date: 01-05-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1604-y

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Knowing left from right: asymmetric functional connectivity during resting state

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

The number of neurons in specific amygdala regions is associated with boldness in mink: a study in animal personality

Development of inhibitory synaptic inputs on layer 2/3 pyramidal neurons in the rat medial prefrontal cortex

Translaminar circuits formed by the pyramidal cells in the superficial layers of cat visual cortex

Different neural substrates for precision stepping and fast online step adjustments in youth

Neuronal density and proportion of interneurons in the associative, sensorimotor and limbic human striatum

GABAergic and non-GABAergic projections to the superior colliculus from the auditory brainstem