Intra-hemispheric integration underlies perception of tilt illusion

&NA; The integration of inputs across the entire visual field into a single conscious experience is fundamental to human visual perception. This integrated nature of visual experience is illustrated by contextual illusions such as the tilt illusion, in which the perceived orientation of a central grating appears tilted away from its physical orientation, due to the modulation by a surrounding grating with a different orientation. Here we investigated the relative contribution of local, intra‐hemispheric and global, inter‐hemispheric integration mechanisms to perception of the tilt illusion. We used Dynamic Causal Modelling of fMRI signals to estimate effective connectivity in human early visual cortices (V1, V2, V3) during bilateral presentation of a tilt illusion stimulus. Our analysis revealed that neural responses associated with the tilt illusion were modulated by intra‐ rather than inter‐hemispheric connectivity. Crucially, across participants, intra‐hemispheric connectivity in V1 correlated with the magnitude of the tilt illusion, while no such correlation was observed for V1 inter‐hemispheric connectivity, or V2, V3 connectivity. Moreover, when the illusion stimulus was presented unilaterally rather than bilaterally, the illusion magnitude did not change. Together our findings suggest that perception of the tilt illusion reflects an intra‐hemispheric integration mechanism. This is in contrast to the existing literature, which suggests inter‐hemispheric modulation of neural activity as early as V1. This discrepancy with our findings may reflect the diversity and complexity of integration mechanisms involved in visual processing and visual perception. HighlightsInvolvement of orientation‐dependent, intra‐hemispheric integration in tilt illusion.Correlation between V1 intra‐hemispheric connectivity and tilt illusion magnitude.No correlation between inter‐hemispheric connectivity and tilt illusion magnitude.No change in tilt illusion magnitude between bilateral and unilateral presentation.Intra‐hemispheric connectivity modulates neural responses to bilateral tilt illusion.

[1]  C. Clifford,et al.  A functional angle on some after-effects in cortical vision , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  D. Schwarzkopf,et al.  Neural Population Tuning Links Visual Cortical Anatomy to Human Visual Perception , 2015, Neuron.

[3]  Reto Meuli,et al.  Imaging of a synchronous neuronal assembly in the human visual brain , 2006, NeuroImage.

[4]  G. Tononi,et al.  Plasticity in the Structure of Visual Space , 2017, eNeuro.

[5]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[6]  P. Dayan,et al.  Perceptual organization in the tilt illusion. , 2009, Journal of vision.

[7]  I. V. D. van der Ham,et al.  How does the corpus callosum mediate interhemispheric transfer? A review. , 2011, Behavioural brain research.

[8]  William D. Penny,et al.  Bayesian model selection and averaging , 2007 .

[9]  D. Margulies,et al.  Regional Variation in Interhemispheric Coordination of Intrinsic Hemodynamic Fluctuations , 2008, The Journal of Neuroscience.

[10]  Marcello Massimini,et al.  Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients , 2012, Brain : a journal of neurology.

[11]  William D. Penny,et al.  Comparing Dynamic Causal Models using AIC, BIC and Free Energy , 2012, NeuroImage.

[12]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[13]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[14]  Kerstin E. Schmidt,et al.  The Visual Callosal Connection: A Connection Like Any Other? , 2013, Neural plasticity.

[15]  Colin W G Clifford,et al.  The tilt illusion: Phenomenology and functional implications , 2014, Vision Research.

[16]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[17]  P. Dayan,et al.  Space and time in visual context , 2007, Nature Reviews Neuroscience.

[18]  Geraint Rees,et al.  Neural correlates of consciousness in humans , 2002, Nature Reviews Neuroscience.

[19]  Interhemispheric Integration , 2017 .

[20]  G. Edelman,et al.  Complexity and coherency: integrating information in the brain , 1998, Trends in Cognitive Sciences.

[21]  Y. Dan,et al.  Clonally Related Visual Cortical Neurons Show Similar Stimulus Feature Selectivity , 2012, Nature.

[22]  Ione Fine,et al.  Serveur Académique Lausannois SERVAL serval.unil.ch , 2022 .

[23]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[24]  D. Schwarzkopf,et al.  Contextual Illusions Reveal the Limit of Unconscious Visual Processing , 2011, Psychological science.

[25]  B. Wandell,et al.  Functional organization of human occipital-callosal fiber tracts. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in ferrets. , 1999, Journal of neurophysiology.

[27]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in humans. , 1999, Journal of neurophysiology.

[28]  P. Wenderoth,et al.  The different mechanisms of the direct and indirect tilt illusions , 1988, Vision Research.

[29]  Geraint Rees,et al.  Human Occipital and Parietal GABA Selectively Influence Visual Perception of Orientation and Size , 2017, The Journal of Neuroscience.

[30]  Hiroshi Ban,et al.  Toward a Common Circle: Interhemispheric Contextual Modulation in Human Early Visual Areas , 2006, The Journal of Neuroscience.

[31]  D. Chklovskii,et al.  Maps in the brain: what can we learn from them? , 2004, Annual review of neuroscience.

[32]  Reto Meuli,et al.  Interhemispheric integration at different spatial scales: the evidence from EEG coherence and FMRI. , 2006, Journal of neurophysiology.

[33]  C. Koch,et al.  Integrated information theory: from consciousness to its physical substrate , 2016, Nature Reviews Neuroscience.

[34]  Geraint Rees,et al.  Variability in visual cortex size reflects tradeoff between local orientation sensitivity and global orientation modulation , 2013, Nature Communications.

[35]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[36]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[37]  H. Yao,et al.  Unconscious processing of invisible visual stimuli , 2016, Scientific Reports.

[38]  G Tononi,et al.  Measures of degeneracy and redundancy in biological networks. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Caleo,et al.  The Corpus Callosum and the Visual Cortex: Plasticity Is a Game for Two , 2012, Neural plasticity.

[40]  Anna W Roe,et al.  The organization of orientation-selective, luminance-change and binocular- preference domains in the second (V2) and third (V3) visual areas of New World owl monkeys as revealed by intrinsic signal optical imaging. , 2009, Cerebral cortex.

[41]  D. Hubel,et al.  Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor , 1974, The Journal of comparative neurology.

[42]  Geraint Rees,et al.  Interocular induction of illusory size perception , 2011, BMC Neuroscience.

[43]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[44]  D. Samuel Schwarzkopf,et al.  Effective Connectivity within Human Primary Visual Cortex Predicts Interindividual Diversity in Illusory Perception , 2013, The Journal of Neuroscience.

[45]  L. Knaap,et al.  How does the corpus callosum mediate interhemispheric transfer? A review , 2011, Behavioural Brain Research.

[46]  S. Clarke,et al.  Occipital cortex in man: Organization of callosal connections, related myelo‐ and cytoarchitecture, and putative boundaries of functional visual areas , 1990, The Journal of comparative neurology.

[47]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[48]  Victor A. F. Lamme,et al.  Feedforward, horizontal, and feedback processing in the visual cortex , 1998, Current Opinion in Neurobiology.

[49]  Jean Bennett,et al.  Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex , 2002, Neuron.

[50]  M. Peters,et al.  The Parallel Brain: The Cognitive Neuroscience of the Corpus Callosum , 2004 .