Abstract
Language comprehension during reading requires fine-grained management of saccadic eye movements. A critical question, therefore, is how the brain controls eye movements in reading. Neural correlates of simple eye movements have been found in multiple cortical regions, but little is known about how this network operates in reading. To investigate this question in the present study, participants were presented with normal text, pseudo-word text, and consonant string text in a magnetic resonance imaging (MRI) scanner with eyetracking. Participants read naturally in the normal text condition and moved their eyes “as if they were reading” in the other conditions. Multi-voxel pattern analysis was used to analyze the fMRI signal in the oculomotor network. We found that activation patterns in a subset of network regions differentiated between stimulus types. These results suggest that the oculomotor network reflects more than simple saccade generation and are consistent with the hypothesis that specific network areas interface with cognitive systems.
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Notes
Univariate analysis was also completed on the ROIs and showed significant differences in overall activation between normal reading, pseudo-text reading, and consonant string reading in rlFEF, and SEF.
References
Choi W, Henderson JM (2015) Neural correlates of active vision: an fMRI comparison of natural reading and scene viewing. Neuropsychologia 75:109–118
Choi W, Desai RH, Henderson JM (2014) The neural substrates of natural reading: a comparison of normal and nonword text using eyetracking and fMRI. Front Hum Neurosci 8:1024
Clifton CE, Ferreira F, Henderson JM, Inhoff AW, Liversedge S, Reichle ED, Schotter ER (2016) Eye movements in reading and information processing: keith Rayner’s 20 year legacy. J Mem Lang 86:1–19
Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173
Cox RW, Jesmanowicz A (1999) Real-time 3D image registration of functional MRI. Magn Reson Imaging 42:1014–1018
Desai RH, Choi W, Lai V, Henderson JM (2016) Towards semantics in the wild: activation to manipulable nouns in naturalistic reading. J Neurosci 36(14):4050–4055
Engbert R, Nuthmann A, Richter EM, Kliegl R (2005) SWIFT: a dynamical model of saccade generation during reading. Psychol Rev 112(4):777
Ettinger U, Ffytche DH, Kumari V, Kathmann N, Reuter B, Zelaya F, Williams SCR (2008) Decomposing the neural correlates of antisaccade eye movements using event-related fMRI. Cereb Cortex 18:1148–1159
Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36:885–899
Grosbras MH, Leonards U, Lobel E, Poline JB, LeBihan D, Berthoz A (2001) Human cortical networks for new and familiar sequences of saccades. Cereb Cortex 11:936–945
Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. J Exp Psychol Hum Percept Perform 28:1039–1054
Hanke M, Halchenko YO, Sederberg PB, Hanson SJ, Haxby JV, Pollmann S (2009) PyMVPA: a Python toolbox for multivariate pattern analysis of fMRI data. Neuroinformatics 7:37–53
Henderson JM, Choi W (2015) Neural correlates of fixation duration during real-world scene viewing: evidence from fixation-related (FIRE) fMRI. J Cognit Neurosci 27(6):1137–1145
Henderson JM, Luke SG (2012) Oculomotor inhibition of return in normal and mindless reading. Psychon Bull Rev 19:1101–1107
Henderson JM, Luke SG, Schmidt J, Richards JE (2013) Co-registration of eye movements and event-related potentials in connected-text paragraph reading. Front Syst Neurosci 7:28
Henderson JM, Choi W, Luke SG (2014) Morphology of primary visual cortex predicts individual differences in fixation duration during text reading. J Cognit Neurosci 27:1137–1145
Henderson JM, Choi W, Luke SG, Desai RH (2015) Neural correlates of fixation duration in natural reading: evidence from fixation-related fMRI. NeuroImage 119:390–397
Henderson JM, Choi W, Lowder MW, Ferreira F (2016) Language structure in the brain: a fixation-related fMRI study of syntactic surprisal in reading. NeuroImage 132:293–300
Hillen R, Gunther T, Kohlen C, Eckers C, van Ermingen-Marbach M, Sass K, Scharke W, Vollmar J, Radach R, Heim S (2013) Identifying brain systems for gaze orienting during reading: fMRI investigation of the Landolt paradigm. Front Hum Neurosci 7:284
Huey EB (1908/1968) The psychology and pedagogy of reading. McMillan, New York. (Reprinted: Cambridge, MA: MIT Press, 1968)
Husain M, Parton A, Hodgson TL, Mort D, Rees G (2002) Self-control during response conflict by human supplementary eye field. Nat Neurosci 6(2):117–118
Hutton SB (2008) Cognitive control of saccadic eye movements. Brain Cogn 68:327–340
Jamadar SD, Fielding J, Egan GF (2013) Quantitative meta-analysis of fMRI and PET studies reveals consistent activation in fronto-striatal-parietal regions and cerebellum during antisaccades and prosaccades. Front Psychol 4:749
Javal LE (1878) Essai sur la physiologie de la lecture. Ann Ocullistique 80:61–73
Luke SG, Henderson JM (2013) Oculomotor and cognitive control of eye movements in reading: evidence from mindless reading. Attent Percept Psychophys 75:1230–1242
Luke SG, Henderson JM (2016) The influence of content meaningfulness on eye movements across tasks: evidence from scene viewing and reading. Front Psychol 7:257
McDowell JE, Kissler JM, Berg P, Dyckman KA, Gao Y, Rockstroh B, Clementz BA (2005) Electroencephalography/magnetoencephalography study of cortical activities preceding prosaccades and antisaccades. NeuroReport 16(7):663–668
McDowell JE, Dyckman KA, Austin BP, Clementz BA (2008) Neurophysiology and neuroanatomy of reflexive and volitional saccades: evidence from studies of humans. Brain Cogn 68:255–270
Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218–228
Nuthmann A, Engbert R, Kliegle R (2007) The IOVP effect in mindless reading: experiment and modeling. Vision Res 47:990–1002
O’Regan JK (1992) Optimal viewing position in words and the strategy-tactics theory of eye movements in reading. Eye movements and visual cognition. Springer, New York, pp 333–354
Pierrot-Deseilligny C, Israel I, Berthoz A, Rivaud S, Gaymard B (1993) Role of the different frontal lobe areas in the control of the horizontal component of memory-guided saccades in man. Exp Brain Res 95:166–171
Pierrot-Deseilligny C, Milea D, Muri RM (2004) Eye movement control by the cerebral cortex. Curr Opin Neurol 17:17–25
Rayner K (1978) Eye movements in reading and information processing. Psychol Bull 85(3):618–660
Rayner K (1998) Eye movements in reading and information processing: 20 years of research. Psychol Bull 124:372–422
Rayner K (2009a) Eye movements in reading: models and data. J Eye Movement Res 2:1–10
Rayner K (2009b) The thirty fifth sir frederick bartlett lecture: eye movements and attention in reading, scene perception, and visual search. Q J Exp Psychol 62:1457–1506
Rayner K, Fischer M (1996) Mindless reading revisited: eye movements during reading and scanning are different. Percept Psychophys 58:734–747
Reichle ED, Sheridan H (2015) EZ reader: an overview of the model and two recent applications. In: Oxford Handbook of Reading, pp 277–292
Reichle ED, Pollatsek A, Fisher DL, Rayner K (1998) Toward a model of eye movement control in reading. Psychol Rev 105(1):125
Reichle ED, Rayner K, Pollatsek A (2003) The EZ Reader model of eye-movement control in reading: comparisons to other models. Behav Brain Sci 26(4):445–476
Reilly R, O’Regan JK (1998) Eye-movement control in reading: a simulation of some word-targeting strategies. Vis Res 38:303–317
Saad ZS, Glen DR, Chen G, Beauchamp MS, Desai R, Cox RW (2009) A new method for improving functional-to-structural MRI alignment using local Pearson correlation. Neuroimage 44:839–848
Schiller P, Tehovnik E (2001) Look and see: how the brain moves the eyes around. Prog Brain Res 134(9):127–142
Stuphorn V, Shall JD (2006) Executive control of countermanding saccades by the supplementary eye field. Nat Neurosci 9(7):925–931
Vitu F, O’Regan JK, Inhoff AW, Topolski R (1995) Mindless reading: eye-movement characteristic are similar in scanning letter strings and reading texts. Percept Psychophys 57:352–364
Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD (2011) Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8:665–670
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Research reported in this publication was supported by the National Institute on Aging of the National Institutes of Health under award number R56AG053346. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
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Goold, J.E., Choi, W. & Henderson, J.M. Cortical control of eye movements in natural reading: Evidence from MVPA. Exp Brain Res 237, 3099–3107 (2019). https://doi.org/10.1007/s00221-019-05655-3
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DOI: https://doi.org/10.1007/s00221-019-05655-3