Abstract
Attention is considered as one of the pre-requisites of conscious perception. Phasic alerting and exogenous orienting improve conscious perception of near-threshold information through segregated brain networks. Using a multimodal neuroimaging approach, combining data from functional MRI (fMRI) and diffusion-weighted imaging (DWI), we investigated the influence of white matter properties of the ventral branch of superior longitudinal fasciculus (SLF III) in functional interactions between attentional systems and conscious perception. Results revealed that (1) reduced integrity of the left hemisphere SLF III was predictive of the neural interactions observed between exogenous orienting and conscious perception, and (2) increased integrity of the left hemisphere SLF III was predictive of the neural interactions observed between phasic alerting and conscious perception. Our results combining fMRI and DWI data demonstrate that structural properties of the white matter organization determine attentional modulations over conscious perception.
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Notes
Note that although cues were spatially informative, they consisted of peripheral and salient stimuli, which are known to exogenously capture attention to that location, i.e. peripheral informative cues produce both an initial exogenous attentional capture, and an endogenous maintenance of attention at the indicated location (Chica et al. 2013a). Therefore, although we refer to Chica et al. (2013b) study as the “Exogenous Orienting” study, we acknowledge there is an endogenous maintenance component in the orienting of attention.
In Bayesian statistics a Bayesian factor = 1 indicates no evidence in favor of either the null or the alternative hypothesis. Bayesian factors >3 indicate moderate evidence in favor of the alternative hypothesis, while Bayesian factors <−3 indicate moderate evidence in favor of the null hypothesis. Bayesian factor values between −3 and 3 indicate anecdotal evidence.
References
Aru J, Axmacher N, Do Lam AT, Fell J, Elger CE, Singer W, Melloni L (2012a) Local category-specific gamma band responses in the visual cortex do not reflect conscious perception. J Neurosci 32(43):14909–14914. doi:10.1523/JNEUROSCI.2051-12.2012
Aru J, Bachmann T, Singer W, Melloni L (2012b) Distilling the neural correlates of consciousness. Neurosci Biobehav Rev 36(2):737–746. doi:10.1016/j.neubiorev.2011.12.003
Bartolomeo P (2007) Visual neglect. Curr Opin Neurol 20(4):381–386
Bartolomeo P, Thiebaut de Schotten M (2016) Let thy left brain know what thy right brain doeth: inter-hemispheric compensation of functional deficits after brain damage. Neuropsychologia 93:407–412. doi:10.1016/j.neuropsychologia.2016.06.016
Bartolomeo P, Siéroff E, Decaix C, Chokron S (2001) Modulating the attentional bias in unilateral neglect: the effects of the strategic set. Exp Brain Res 137(3–4):432–444
Bartolomeo P, Thiebaut de Schotten M, Doricchi F (2007) Left unilateral neglect as a disconnection syndrome. Cereb Cortex 17(11):2479–2490
Bartolomeo P, Thiebaut de Schotten M, Chica AB (2013) Brain networks of visuospatial attention and their disruption in visual neglect. Front Hum Neurosci 6:110. doi:10.3389/fnhum.2012.00110
Bartolomeo P, Seidel Malkinson T, de Vito S (2017) Botallo’s error, or the quandaries of the universality assumption. Cortex 86:176–185. doi:10.1016/j.cortex.2016.09.026
Botta F, Lupiáñez J, Chica AB (2014) When endogenous spatial attention improves conscious perception: effects of alerting and bottom-up activation. Conscious Cognit 23:63–73. doi:10.1016/j.concog.2013.12.003
Bourgeois A, Chica AB, Migliaccio R, Thiebaut de Schotten M, Bartolomeo P (2012) Cortical control of inhibition of return: evidence from patients with inferior parietal damage and visual neglect. Neuropsychologia 50(5):800–809. doi:10.1016/j.neuropsychologia.2012.01.014
Bourgeois A, Chica AB, Valero-Cabre A, Bartolomeo P (2013a) Cortical control of inhibition of return: causal evidence for task-dependent modulations by dorsal and ventral parietal regions. Cortex 49(8):2229–2238. doi:10.1016/j.cortex.2012.10.017
Bourgeois A, Chica AB, Valero-Cabre A, Bartolomeo P (2013b) Cortical control of inhibition of return: exploring the causal contributions of the left parietal cortex. Cortex 49(10):2927–2934. doi:10.1016/j.cortex.2013.08.004
Bourgeois A, Chica AB, Migliaccio R, Bayle DJ, Duret C, Pradat-Diehl P, Bartolomeo P (2015) Inappropriate rightward saccades after right hemisphere damage: oculomotor analysis and anatomical correlates. Neuropsychologia 73:1–11. doi:10.1016/j.neuropsychologia.2015.04.013
Calabro RS, Cacciola A, Bramanti P, Milardi D (2015) Neural correlates of consciousness: what we know and what we have to learn! Neurol Sci 36(4):505–513. doi:10.1007/s10072-015-2072-x
Carretie L, Rios M, Perianez JA, Kessel D, Alvarez-Linera J (2012) The role of low and high spatial frequencies in exogenous attention to biologically salient stimuli. PLoS ONE 7(5):e37082. doi:10.1371/journal.pone.0037082
Chica AB, Bartolomeo P, Valero-Cabré A (2011a) Dorsal and ventral parietal contributions to spatial orienting in the human brain. J Neurosci 31(22):8143–8149. doi:10.1523/JNEUROSCI.5463-10.2010
Chica AB, Lasaponara S, Chanes L, Valero-Cabré A, Doricchi F, Lupiáñez J, Bartolomeo P (2011b) Spatial attention and conscious perception: the role of endogenous and exogenous orienting. Atten Percept Psychophys 73(4):1065–1081. doi:10.3758/s13414-010-0082-6
Chica AB, Thiebaut de Schotten M, Toba M, Malhotra P, Lupianez J, Bartolomeo P (2011c) Attention networks and their interactions after right-hemisphere damage. Cortex 48(6):654–663. doi:10.1016/j.cortex.2011.01.009
Chica AB, Bartolomeo P, Lupiáñez J (2013a) Two cognitive and neural systems for endogenous and exogenous spatial attention. Behav Brain Res 237:107–123. doi:10.1016/j.bbr.2012.09.027
Chica AB, Paz-Alonso PM, Valero-Cabre A, Bartolomeo P (2013b) Neural bases of the interactions between spatial attention and conscious perception. Cereb Cortex 23(6):1269–1279. doi:10.1093/cercor/bhs087
Chica AB, Valero-Cabré A, Paz-Alonso PM, Bartolomeo P (2014) Causal contributions of the left frontal eye field to conscious perception. Cereb Cortex 24(3):745–753. doi:10.1093/cercor/bhs357
Chica AB, Bayle DJ, Botta F, Bartolomeo P, Paz-Alonso PM (2016) Interactions between phasic alerting and consciousness in the fronto-striatal network. Sci Rep 6:31868. doi:10.1038/srep31868
Ciaraffa F, Castelli G, Parati EA, Bartolomeo P, Bizzi A (2013) Visual neglect as a disconnection syndrome? A confirmatory case report. Neurocase 19(4):351–359. doi:10.1080/13554794.2012.667130
Clemens B, Zvyagintsev M, Sack AT, Heinecke A, Willmes K, Sturm W (2011) Revealing the functional neuroanatomy of intrinsic alertness using fMRI: methodological peculiarities. PLoS ONE 6(9):e25453. doi:10.1371/journal.pone.0025453
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58(3):306–324
Coull JT, Frith CD, Buchel C, Nobre AC (2000) Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts. Neuropsychologia 38(6):808–819
Coull JT, Nobre AC, Frith CD (2001) The noradrenergic alpha2 agonist clonidine modulates behavioural and neuroanatomical correlates of human attentional orienting and alerting. Cereb Cortex 11(1):73–84
Dale AM (1999) Optimal experimental design for event-related fMRI. Hum Brain Mapp 8(2–3):109–114
Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70(2):200–227. doi:10.1016/j.neuron.2011.03.018
Dehaene S, Changeux JP, Naccache L, Sackur J, Sergent C (2006) Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cognit Sci 10(5):204–211
Dell’Acqua F, Scifo P, Rizzo G, Catani M, Simmons A, Scotti G, Fazio F (2010) A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution. Neuroimage 49(2):1446–1458. doi:10.1016/j.neuroimage.2009.09.033
Dell’Acqua F, Simmons A, Williams SC, Catani M (2013) Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Hum Brain Mapp 34(10):2464–2483. doi:10.1002/hbm.22080
Doricchi F, Thiebaut de Schotten M, Tomaiuolo F, Bartolomeo P (2008) White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness. Cortex 44(8):983–995
Downar J, Crawley AP, Mikulis DJ, Davis KD (2002) A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. J Neurophysiol 87(1):615–620
Forkel SJ, Thiebaut de Schotten M, Dell’Acqua F, Kalra L, Murphy DG, Williams SC, Catani M (2014) Anatomical predictors of aphasia recovery: a tractography study of bilateral perisylvian language networks. Brain 137(Pt 7):2027–2039. doi:10.1093/brain/awu113
Ge H, Yin X, Xu J, Tang Y, Han Y, Xu W, Liu S (2013) Fiber pathways of attention subnetworks revealed with tract-based spatial statistics (TBSS) and probabilistic tractography. PLoS ONE 8(11):e78831. doi:10.1371/journal.pone.0078831
Kim H (2014) Involvement of the dorsal and ventral attention networks in oddball stimulus processing: a meta-analysis. Hum Brain Mapp 35(5):2265–2284. doi:10.1002/hbm.22326
Kincade JM, Abrams RA, Astafiev SV, Shulman GL, Corbetta M (2005) An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. J Neurosci 25(18):4593–4604
Klarborg B, Skak Madsen K, Vestergaard M, Skimminge A, Jernigan TL, Baare WF (2013) Sustained attention is associated with right superior longitudinal fasciculus and superior parietal white matter microstructure in children. Hum Brain Mapp 34(12):3216–3232. doi:10.1002/hbm.22139
Koch C, Tsuchiya N (2007) Attention and consciousness: two distinct brain processes. Trends Cognit Sci 11(1):16–22
Koch C, Massimini M, Boly M, Tononi G (2016) Neural correlates of consciousness: progress and problems. Nat Rev Neurosci 17(5):307–321. doi:10.1038/nrn.2016.22
Kusnir F, Chica AB, Mitsumasu MA, Bartolomeo P (2011) Phasic auditory alerting improves visual conscious perception. Conscious Cogn 20(4):1201–1210. doi:10.1016/j.concog.2011.01.012
Lamme VA (2006) Towards a true neural stance on consciousness. Trends Cognit Sci 10(11):494–501
Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61(6):1336–1349
Lunven M, Thiebaut De Schotten M, Bourlon C, Duret C, Migliaccio R, Rode G, Bartolomeo P (2015) White matter lesional predictors of chronic visual neglect: a longitudinal study. Brain 138(Pt 3):746–760. doi:10.1093/brain/awu389
Mack A, Rock I (1998) Inattentional blindness. The MIT Press, Cambridge
Manly T, Dobler VB, Dodds CM, George MA (2005) Rightward shift in spatial awareness with declining alertness. Neuropsychologia 43(12):1721–1728
Marois R, Ivanoff J (2005) Capacity limits of information processing in the brain. Trends Cognit Sci 9(6):296–305. doi:10.1016/j.tics.2005.04.010
Müller HJ, Rabbitt PM (1989) Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J Exp Psychol Hum Percept Perform 15(2):315–330
Niogi S, Mukherjee P, Ghajar J, McCandliss BD (2010) Individual differences in distinct components of attention are linked to anatomical variations in distinct white matter tracts. Front Neuroanat 4:2. doi:10.3389/neuro.05.002.2010
Petersen SE, Posner MI (2013) The attention system of the human brain: 20 years after. Annu Rev Neurosci 35:73–89. doi:10.1146/annurev-neuro-062111-150525
Pins D, Ffytche D (2003) The neural correlates of conscious vision. Cereb Cortex 13(5):461–474
Posner MI (1994) Attention: the mechanisms of consciousness. Proc Natl Acad Sci USA 91(16):7398–7403
Posner MI (2012) Attentional networks and consciousness. Front Psychol 3:64. doi:10.3389/fpsyg.2012.00064
Rees G, Kreiman G, Koch C (2002) Neural correlates of consciousness in humans. Nat Rev Neurosci 3:261–270
Robertson IH, Tegnér R, Tham K, Lo A, Nimmo-Smith I (1995) Sustained attention training for unilateral neglect: theoretical and rehabilitation implications. J Clin Exp Neuropsychol 17(3):416–430
Robertson IH, Mattingley JB, Rorden C, Driver J (1998) Phasic alerting of neglect patients overcomes their spatial deficit in visual awareness. Nature 395(6698):169–172
Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, Thiebaut de Schotten M (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221(3):1751–1766. doi:10.1007/s00429-015-1001-3
Seth AK (2009) Explanatory correlates of consciousness: theoretical and computational challenges. Cognit Comput 1:50–63
Shinoura N, Suzuki Y, Yamada R, Tabei Y, Saito K, Yagi K (2009) Damage to the right superior longitudinal fasciculus in the inferior parietal lobe plays a role in spatial neglect. Neuropsychologia 47(12):2600–2603. doi:10.1016/j.neuropsychologia.2009.05.010
Shulman GL, Astafiev SV, McAvoy MP, d’Avossa G, Corbetta M (2007) Right TPJ deactivation during visual search: functional significance and support for a filter hypothesis. Cereb Cortex 17(11):2625–2633. doi:10.1093/cercor/bhl170
Shulman GL, Astafiev SV, Franke D, Pope DL, Snyder AZ, McAvoy MP, Corbetta M (2009) Interaction of stimulus-driven reorienting and expectation in ventral and dorsal frontoparietal and basal ganglia-cortical networks. J Neurosci 29(14):4392–4407. doi:10.1523/JNEUROSCI.5609-08.2009
Sperling G (1960) The information available in brief visual presentations. Psychol Monogr 74(11):1–29
Sturm W, Willmes K (2001) On the functional neuroanatomy of intrinsic and phasic alertness. Neuroimage 14(1 Pt 2):S76–S84. doi:10.1006/nimg.2001.0839
Sturm W, de Simone A, Krause BJ, Specht K, Hesselmann V, Radermacher I, Willmes K (1999) Functional anatomy of intrinsic alertness: evidence for a fronto-parietal-thalamic-brainstem network in the right hemisphere. Neuropsychologia 37(7):797–805
Sturm W, Longoni F, Fimm B, Dietrich T, Weis S, Kemna S, Willmes K (2004) Network for auditory intrinsic alertness: a PET study. Neuropsychologia 42(5):563–568
Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Lévy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 5744:2226–2228
Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246. doi:10.1038/nn.2905
Thiebaut de Schotten M, Tomaiuolo F, Aiello M, Merola S, Silvetti M, Lecce F, Doricchi F (2014) Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete virtual “in vivo” tractography dissection. Cereb Cortex 24(3):691–706. doi:10.1093/cercor/bhs351
Thiel CM, Fink GR (2007) Visual and auditory alertness: modality-specific and supramodal neural mechanisms and their modulation by nicotine. J Neurophysiol 97(4):2758–2768. doi:10.1152/jn.00017.2007
Thimm M, Fink GR, Kust J, Karbe H, Sturm W (2006) Impact of alertness training on spatial neglect: a behavioural and fMRI study. Neuropsychologia 44(7):1230–1246
Tsuchiya N, Wilke M, Frassle S, Lamme VA (2015) No-report paradigms: extracting the true neural correlates of consciousness. Trends Cognit Sci 19(12):757–770. doi:10.1016/j.tics.2015.10.002
Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16(1):55–61. doi:10.1038/nrn3857
Urbanski M, Thiebaut de Schotten M, Rodrigo S, Catani M, Oppenheim C, Touze E, Bartolomeo P (2008) Brain networks of spatial awareness: evidence from diffusion tensor imaging tractography. J Neurol Neurosurg Psychiatry 79(5):598–601
Urbanski M, Thiebaut de Schotten M, Rodrigo S, Oppenheim C, Touze E, Meder JF, Bartolomeo P (2011) DTI-MR tractography of white matter damage in stroke patients with neglect. Exp Brain Res 208(4):491–505. doi:10.1007/s00221-010-2496-8
Wingen M, Kuypers KP, van de Ven V, Formisano E, Ramaekers JG (2008) Sustained attention and serotonin: a pharmaco-fMRI study. Hum Psychopharmacol 23(3):221–230. doi:10.1002/hup.923
Wyart V, Tallon-Baudry C (2008) Neural dissociation between visual awareness and spatial attention. J Neurosci 28(10):2667–2679. doi:10.1523/JNEUROSCI.4748-07.2008
Wyart V, Dehaene S, Tallon-Baudry C (2011) Early dissociation between neural signatures of endogenous spatial attention and perceptual awareness during visual masking. Front Hum Neurosci 6:16. doi:10.3389/fnhum.2012.00016
Yanaka HT, Saito DN, Uchiyama Y, Sadato N (2010) Neural substrates of phasic alertness: a functional magnetic resonance imaging study. Neurosci Res 68(1):51–58. doi:10.1016/j.neures.2010.05.005
Zeki S (2005) The Ferrier Lecture 1995 behind the seen: the functional specialization of the brain in space and time. Philos Trans R Soc Lond B Biol Sci 360(1458):1145–1183. doi:10.1098/rstb.2005.1666
Acknowledgements
ABC was supported by a Ramón y Cajal fellowship (RYC-2011-09320) and research project PSI2014-58681-P from the Spanish Ministry of Economy and Competitiveness (MINECO). PMP-A was supported by a Ramón y Cajal fellowship (RYC-2014-15440), and grants PSI2015-65696 and SEV-2015-049 from the MINECO. MTdS received funding from the ‘Agence Nationale de la Recherche’ (Grant number ANR-13-JSV4-0001-01) and “Investissements d’avenir” ANR-10-IAIHU-06. PB received funding from the ‘Agence Nationale de la Recherche’ (Grant number R16139DD).
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Chica, A.B., Thiebaut de Schotten, M., Bartolomeo, P. et al. White matter microstructure of attentional networks predicts attention and consciousness functional interactions. Brain Struct Funct 223, 653–668 (2018). https://doi.org/10.1007/s00429-017-1511-2
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DOI: https://doi.org/10.1007/s00429-017-1511-2