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01-03-2020 | Original Article

Functional connectivity at rest captures individual differences in visual search

Authors: Elisenda Bueichekú, Anna Miró-Padilla, César Ávila

Published in: Brain Structure and Function | Issue 2/2020

Abstract

Brain functional connectivity is supposed to capture personal and lifetime learning experiences and contribute to generating individual differences in cognitive abilities. We tested this possibility using the visual search task as a measure of visual information processing and the functioning of the visual attention control system. Forty-two undergraduate students completed a functional MRI study with a resting-state session and a visual search task scan. The visual attention and control systems were studied by investigating the functional connectivity of the primary visual area, the posterior parietal cortex, the dorsolateral prefrontal cortex, and the dorsal anterior cingulate cortex because these areas have been closely related to the visual search task. A pairwise resting-state functional connectivity analysis was conducted between these regions, followed by a correlation analysis with the behavioral measures from the visual search task. Results showed that higher connectivity values between the posterior parietal cortex and the dorsal anterior cingulate cortex were positively correlated with faster response speed. The posterior parietal cortex has been related to the formation of priority maps and the integration of sensory and executive information. Inhibitory control, performance monitoring during top–down cognitive tasks, and target detection have been associated with the dorsal anterior cingulate cortex. In light of these results, we suggest that a priori enhanced connectivity between these regions defines individual differences in visual information processing and the ability to adapt to cognitive demands.

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Albert NB, Robertson EM, Miall RC (2009) The resting human brain and motor learning. Curr Biol 19(12):1023–1027. https://doi.org/10.1016/j.cub.2009.04.028 CrossRefPubMedPubMedCentral

Baldassarre A, Lewis CM, Committeri G, Snyder AZ, Romani GL, Corbetta M (2012) Individual variability in functional connectivity predicts performance of a perceptual task. Proc Natl Acad Sci USA 109(9):3516–3521. https://doi.org/10.1073/pnas.1113148109 CrossRefPubMedPubMedCentral

Bisley JW (2010) The neural basis of visual attention. J Physiol 589(1):49–57. https://doi.org/10.1113/jphysiol.2010.192666 CrossRefPubMedPubMedCentral

Bisley JW, Goldberg ME (2010) Attention, intention, and priority in the parietal lobe. Annu Rev Neurosci 33(1):1–21. https://doi.org/10.1146/annurev-neuro-060909-152823 CrossRefPubMedPubMedCentral

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.1910340409 CrossRefPubMed

Bressler SL, Menon V (2010) Large-scale brain networks in cognition: emerging ethods and principles. Trends Cogn Sci 14(6):277–290. https://doi.org/10.1016/j.tics.2010.04.004 CrossRefPubMed

Buckner RL, Vincent JL (2007) Unrest at rest: default activity and spontaneous network correlations. Neuroimage 37(4):1091–1096. https://doi.org/10.1016/j.neuroimage.2007.01.010 CrossRefPubMed

Buckner RL, Krienen FM, Yeo BTT (2013) Opportunities and limitations of intrinsic functional connectivity MRI. Nat Neurosci 16(7):832–837. https://doi.org/10.1038/nn.3423 CrossRefPubMed

Bueichekú E, Ventura-Campos N, Palomar-García M-Á, Miró-Padilla A, Parcet M-A, Ávila C (2015) Functional connectivity between superior parietal lobule and primary visual cortex “at rest” predicts visual search efficiency. Brain Connect 5(8):517–526. https://doi.org/10.1089/brain.2015.0352 CrossRefPubMed

Bueichekú E, Miró-Padilla A, Palomar-García MÁ, Ventura-Campos N, Parcet MA, Barrós-Loscertales A, Ávila C (2016) Reduced posterior parietal cortex activation after training on a visual search task. Neuroimage 135:204–213. https://doi.org/10.1016/j.neuroimage.2016.04.059 CrossRefPubMed

Bueichekú E, Ávila C, Miró-Padilla A, Sepulcre J (2018) Visual search task immediate training effects on task-related functional connectivity. Brain Imaging Behav. https://doi.org/10.1007/s11682-018-9993-y CrossRef

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

Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13PubMedPubMedCentral

Chou Y, Chen N, Madden DJ (2013) Functional brain connectivity and cognition: effects of adult age and task demands. Neurobiol Aging 34(8):1925–1934. https://doi.org/10.1016/j.neurobiolaging.2013.02.012 CrossRefPubMedPubMedCentral

Cieslik EC, Mueller VI, Eickhoff CR, Langner R, Eickhoff SB (2015) Three key regions for supervisory attentional control: evidence from neuroimaging meta-analyses. Neurosci Biobehav Rev 48:22–34. https://doi.org/10.1016/j.neubiorev.2014.11.003 CrossRefPubMed

Deco G, Corbetta M (2010) The dynamical balance of the brain at rest. Neuroscientist 17(1):107–123. https://doi.org/10.1177/1073858409354384 CrossRefPubMedPubMedCentral

Deco G, Rolls ET (2005) Attention, short-term memory, and action selection: a unifying theory. Prog Neurobiol 76(4):236–256. https://doi.org/10.1016/j.pneurobio.2005.08.004 CrossRefPubMed

Dosenbach NUF, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HC, Burgund ED, Grimes AL, Schlaggar BL, Petersen SE (2006) A core system for the implementation of task sets. Neuron 50(5):799–812. https://doi.org/10.1016/j.neuron.2006.04.031 CrossRefPubMedPubMedCentral

Dosenbach NUF, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RAT, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104(26):11073–11078. https://doi.org/10.1073/pnas.0704320104 CrossRefPubMedPubMedCentral

Dosenbach NUF, Fair DA, Cohen AL, Schlaggar BL, Petersen SE (2008) A dual-networks architecture of top-down control. Trends Cogn Sci 12(3):99–105. https://doi.org/10.1016/j.tics.2008.01.001 CrossRefPubMedPubMedCentral

Eckstein MP (2011) Visual search: a retrospective. J Vis 11(5):14–14. https://doi.org/10.1167/11.5.14 CrossRefPubMed

Egner T, Monti JMP, Trittschuh EH, Wieneke CA, Hirsch J, Mesulam M-M (2008) Neural integration of top–down spatial and feature-based information in visual search. J Neurosci 28(24):6141–6151. https://doi.org/10.1523/jneurosci.1262-08.2008 CrossRefPubMedPubMedCentral

Eickhoff SB, Heim S, Zilles K, Amunts K (2006) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 32(2):570–582CrossRefPubMed

Eickhoff SB, Paus T, Caspers S, Grosbras MH, Evans A, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36(3):511–521CrossRefPubMed

Eimer M (2014) The neural basis of attentional control in visual search. Trends Cogn Sci 18(10):526–535. https://doi.org/10.1016/j.tics.2014.05.005 CrossRefPubMed

Fair DA, Cohen AL, Power JD, Dosenbach NUF, Church JA, Miezin FM, Petersen SE (2009) Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol 5(5):e1000381. https://doi.org/10.1371/journal.pcbi.1000381 CrossRefPubMedPubMedCentral

Fecteau JH, Munoz DP (2006) Warning signals influence motor processing. J Neurophysiol 97(2):1600–1609. https://doi.org/10.1152/jn.00978.2005 CrossRefPubMed

Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711. https://doi.org/10.1038/nrn2201 CrossRefPubMed

Greicius MD, Supekar K, Menon V, Dougherty RF (2008) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19(1):72–78. https://doi.org/10.1093/cercor/bhn059 CrossRefPubMedPubMedCentral

Guerra-Carrillo B, Mackey AP, Bunge SA (2014) Resting-state fMRI: a window into human brain plasticity. Neuroscientist 20(5):522–533. https://doi.org/10.1177/1073858414524442 CrossRefPubMed

Gusnard DA, Raichle ME (2001) Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci 2(10):685–694. https://doi.org/10.1038/35094500 CrossRefPubMed

Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT (2006) Brain connectivity related to working memory performance. J Neurosci 26(51):13338–13343. https://doi.org/10.1523/jneurosci.3408-06.2006 CrossRefPubMedPubMedCentral

Harmelech T, Malach R (2013) Neurocognitive biases and the patterns of spontaneous correlations in the human cortex. Trends Cogn Sci 17:606–615. https://doi.org/10.1016/j.tics.2013.09.014 CrossRefPubMed

Heilbronner SR, Hayden BY (2016) Dorsal anterior cingulate cortex: a bottom–up view. Annu Rev Neurosci 39(1):149–170. https://doi.org/10.1146/annurev-neuro-070815-013952 CrossRefPubMedPubMedCentral

Ipata AE, Gee AL, Bisley JW, Goldberg ME (2008) Neurons in the lateral intraparietal area create a priority map by the combination of disparate signals. Exp Brain Res 192(3):479–488. https://doi.org/10.1007/s00221-008-1557-8 CrossRefPubMedPubMedCentral

Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for therobust and accurate linear registration and motion correction of brain images. Neuroimage 17(2):825–841. https://doi.org/10.1006/nimg.2002.1132 CrossRefPubMed

Kanai R, Rees G (2011) The structural basis of inter-individual differences in human behaviour and cognition. Nat Rev Neurosci 12(4):231–242. https://doi.org/10.1038/nrn3000 CrossRefPubMed

Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23(1):315–341. https://doi.org/10.1146/annurev.neuro.23.1.315 CrossRefPubMed

Kelly AM, Garavan H (2005) Human functional neuroimaging of brain changes associated with practice. Cereb Cortex. 5(8):1089–1102. https://doi.org/10.1093/cercor/bhi005 CrossRef

Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2008) Competition between functional brain networks mediates behavioral variability. Neuroimage 39(1):527–537. https://doi.org/10.1016/j.neuroimage.2007.08.008 CrossRefPubMed

Kübler A, Dixon V, Garavan H (2006) Automaticity and reestablishment of executive control—an fMRI study. J Cogn Neurosci 18(8):1331–1342. https://doi.org/10.1162/jocn.2006.18.8.1331 CrossRefPubMed

Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239CrossRefPubMed

Miall RC, Robertson EM (2006) Functional imaging: is the resting brain resting? Curr Biol 16(23):R998–R1000. https://doi.org/10.1016/j.cub.2006.10.041 CrossRefPubMedPubMedCentral

Murphy K, Fox MD (2017) Towards a consensus regarding global signal regression for resting state functional connectivity MRI. Neuroimage 154:169–173. https://doi.org/10.1016/j.neuroimage.2016.11.052 CrossRefPubMed

Nakayama K, Martini P (2011) Situating visual search. Vis Res 51(13):1526–1537. https://doi.org/10.1016/j.visres.2010.09.003 CrossRefPubMed

Nardo D, Santangelo V, Macaluso E (2011) Stimulus-driven orienting of visuo-spatial attention in complex dynamic environments. Neuron 69(5):1015–1028. https://doi.org/10.1016/j.neuron.2011.02.020 CrossRefPubMed

Nardo D, Santangelo V, Macaluso E (2014) Spatial orienting in complex audiovisual environments. Hum Brain Mapp 35(4):1597–1614. https://doi.org/10.1002/hbm.22276 CrossRefPubMed

Nee DE, Wager TD, Jonides J (2007) Interference resolution: insights from a meta-analysis of neuroimaging tasks. Cogn Affect Behav Neurosci 7:1–17CrossRefPubMed

Niendam TA, Laird AR, Ray KL, Dean YM, Glahn DC, Carter CS (2012) Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 12(2):241–268. https://doi.org/10.3758/s13415-011-0083-5 CrossRefPubMedPubMedCentral

Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113. https://doi.org/10.1016/0028-3932(71)90067-4 CrossRefPubMed

Petersen SE, Posner MI (2012) The attention system of the human brain: 20 years after. Annu Rev Neurosci 35(1):73–89. https://doi.org/10.1146/annurev-neuro-062111-150525 CrossRefPubMedPubMedCentral

Posner MI (2012) Imaging attention networks. Neuroimage 61(2):450–456. https://doi.org/10.1016/j.neuroimage.2011.12.040 CrossRefPubMed

Posner MI, Petersen SE (1990) The attention system of the human brain. Annu Rev Neurosci 13(1):25–42. https://doi.org/10.1146/annurev.ne.13.030190.000325 CrossRefPubMed

Power JD, Plitt M, Laumann TO, Martin A (2017) Sources and implications of whole-brain fMRI signals in humans. Neuroimage 146:609–625. https://doi.org/10.1016/j.neuroimage.2016.09.038 CrossRefPubMed

Prado J, Carp J, Weissman DH (2011) Variations of response time in a selective attention task are linked to variations of functional connectivity in the attentional network. Neuroimage 54(1):541–549. https://doi.org/10.1016/j.neuroimage.2010.08.022 CrossRefPubMed

Raichle ME (2011) The restless brain. Brain Connect 1(1):3–12. https://doi.org/10.1089/brain.2011.0019 CrossRefPubMedPubMedCentral

Raichle ME, Snyder AZ (2007) A default mode of brain function: a brief history of an evolving idea. Neuroimage 37(4):1083–1090. https://doi.org/10.1016/j.neuroimage.2007.02.041 CrossRefPubMed

Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98(2):676–682. https://doi.org/10.1073/pnas.98.2.676 CrossRefPubMedPubMedCentral

Ridderinkhof KR (2004) The role of the medial frontal cortex in cognitive control. Science 306(5695):443–447. https://doi.org/10.1126/science.1100301 CrossRefPubMed

Sala-Llonch R, Peña-Gómez C, Arenaza-Urquijo EM, Vidal-Piñeiro D, Bargalló N, Junqué C, Bartrés-Faz D (2012) Brain connectivity during resting state and subsequent working memory task predicts behavioural performance. Cortex 48(9):1187–1196. https://doi.org/10.1016/j.cortex.2011.07.006 CrossRefPubMed

Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2(8):539–550. https://doi.org/10.1038/35086012 CrossRefPubMedPubMedCentral

Satterthwaite TD, Elliott MA, Gerraty RT, Ruparel K, Loughead J, Calkins ME, Eickhoff SB, Hakonarson H, Gur RC, Gur RE, Wolf DH (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240–256. https://doi.org/10.1016/j.neuroimage.2012.08.052 CrossRefPubMed

Schneider W, Eschmann A, Zuccolotto A (2002) E-Prime reference guide. Psychology Software Tools Inc, Pittsburgh

Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356. https://doi.org/10.1523/jneurosci.5587-06.2007 CrossRefPubMedPubMedCentral

Serences JT, Yantis S (2006) Selective visual attention and perceptual coherence. Trends Cogn Sci 10(1):38–45. https://doi.org/10.1016/j.tics.2005.11.008 CrossRefPubMed

Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12(3):154–167. https://doi.org/10.1038/nrn2994 CrossRefPubMedPubMedCentral

Shehzad Z, Kelly AMC, Reiss PT, Gee DG, Gotimer K, Uddin LQ, Milham MP (2009) The resting brain: unconstrained yet reliable. Cereb Cortex 19(10):2209–2229. https://doi.org/10.1093/cercor/bhn256 CrossRefPubMedPubMedCentral

Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2011) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22(1):158–165. https://doi.org/10.1093/cercor/bhr099 CrossRefPubMedPubMedCentral

Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci USA 106(31):13040–13045. https://doi.org/10.1073/pnas.0905267106 CrossRefPubMedPubMedCentral

Vogel EK, Awh E (2008) How to exploit diversity for scientific gain. Curr Dir Psychol Sci 17(2):171–176. https://doi.org/10.1111/j.1467-8721.2008.00569.x CrossRef

Womelsdorf T, Everling S (2015) Long-range attention networks: circuit motifs underlying endogenously controlled stimulus selection. Trends Cogn Sci 38(11):682–700. https://doi.org/10.1016/j.tins.2015.08.009 CrossRef

Zelinsky GJ, Bisley JW (2015) The what, where, and why of priority maps and their interactions with visual working memory. Ann N Y Acad Sci 1339(1):154–164. https://doi.org/10.1111/nyas.12606 CrossRefPubMedPubMedCentral

Title: Functional connectivity at rest captures individual differences in visual search
Authors: Elisenda Bueichekú
Anna Miró-Padilla
César Ávila
Publication date: 01-03-2020
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 2/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-019-02008-2

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