Occipital Cortex of Blind Individuals Is Functionally Coupled with Executive Control Areas of Frontal Cortex

In congenital blindness, the occipital cortex responds to a range of nonvisual inputs, including tactile, auditory, and linguistic stimuli. Are these changes in functional responses to stimuli accompanied by altered interactions with nonvisual functional networks? To answer this question, we introduce a data-driven method that searches across cortex for functional connectivity differences across groups. Replicating prior work, we find increased fronto-occipital functional connectivity in congenitally blind relative to blindfolded sighted participants. We demonstrate that this heightened connectivity extends over most of occipital cortex but is specific to a subset of regions in the inferior, dorsal, and medial frontal lobe. To assess the functional profile of these frontal areas, we used an n-back working memory task and a sentence comprehension task. We find that, among prefrontal areas with overconnectivity to occipital cortex, one left inferior frontal region responds to language over music. By contrast, the majority of these regions responded to working memory load but not language. These results suggest that in blindness occipital cortex interacts more with working memory systems and raise new questions about the function and mechanism of occipital plasticity.

[1]  Lawrence L. Wald,et al.  Effect of spatial smoothing on physiological noise in high-resolution fMRI , 2006, NeuroImage.

[2]  Chunshui Yu,et al.  Abnormal diffusion of cerebral white matter in early blindness , 2009, Human brain mapping.

[3]  Abraham Z Snyder,et al.  Dissociated mean and functional connectivity BOLD signals in visual cortex during eyes closed and fixation. , 2012, Journal of neurophysiology.

[4]  T. Hensch Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

[5]  Norihiro Sadato,et al.  Tactile discrimination activates the visual cortex of the recently blind naive to Braille: a functional magnetic resonance imaging study in humans , 2004, Neuroscience Letters.

[6]  E. Zohary,et al.  Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects , 2004, Nature Neuroscience.

[7]  D. Maurer,et al.  Multiple sensitive periods in human visual development: evidence from visually deprived children. , 2005, Developmental psychobiology.

[8]  Lawrence L. Wald,et al.  Comparison of physiological noise at 1.5 T, 3 T and 7 T and optimization of fMRI acquisition parameters , 2005, NeuroImage.

[9]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[10]  A. Snyder,et al.  Diffusion tensor imaging reveals white matter reorganization in early blind humans. , 2006, Cerebral cortex.

[11]  E. Zohary,et al.  V1 activation in congenitally blind humans is associated with episodic retrieval. , 2005, Cerebral cortex.

[12]  Yufeng Zang,et al.  Eyes-Open/Eyes-Closed Dataset Sharing for Reproducibility Evaluation of Resting State fMRI Data Analysis Methods , 2013, Neuroinformatics.

[13]  M. Raichle,et al.  Adaptive changes in early and late blind: a fMRI study of Braille reading. , 2002, Journal of neurophysiology.

[14]  A. Cowey,et al.  Imaging studies in congenital anophthalmia reveal preservation of brain architecture in 'visual' cortex. , 2009, Brain : a journal of neurology.

[15]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[16]  D. Maurer,et al.  Impairment in Holistic Face Processing Following Early Visual Deprivation , 2004, Psychological science.

[17]  Christopher P. Said,et al.  Top-down attention switches coupling between low-level and high-level areas of human visual cortex , 2012, Proceedings of the National Academy of Sciences.

[18]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[19]  Rebecca Saxe,et al.  Theory of mind performance in children correlates with functional specialization of a brain region for thinking about thoughts. , 2012, Child development.

[20]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .

[21]  Kurt E. Weaver,et al.  Attention and Sensory Interactions within the Occipital Cortex in the Early Blind: An fMRI Study , 2007, Journal of Cognitive Neuroscience.

[22]  Yong Liu,et al.  Altered Anatomical Network in Early Blindness Revealed by Diffusion Tensor Tractography , 2009, PloS one.

[23]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[24]  Aaron S. Andalman,et al.  Vision Following Extended Congenital Blindness , 2006, Psychological science.

[25]  P. Alku,et al.  The role of blind humans’ visual cortex in auditory change detection , 2005, Neuroscience Letters.

[26]  Nicola Filippini,et al.  Language networks in anophthalmia: maintained hierarchy of processing in 'visual' cortex. , 2012, Brain : a journal of neurology.

[27]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[28]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[29]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[30]  B. Ripley,et al.  A new statistical approach to detecting significant activation in functional MRI , 2000, NeuroImage.

[31]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[32]  Nancy Kanwisher,et al.  Functional specificity for high-level linguistic processing in the human brain , 2011, Proceedings of the National Academy of Sciences.

[33]  Hae-Jeong Park,et al.  Reorganization of neural circuits in the blind on diffusion direction analysis , 2007, Neuroreport.

[34]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[35]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[36]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

[37]  Dost Öngür,et al.  Anticorrelations in resting state networks without global signal regression , 2012, NeuroImage.

[38]  Franco Lepore,et al.  Differential occipital responses in early- and late-blind individuals during a sound-source discrimination task , 2008, NeuroImage.

[39]  Alex R. Wade,et al.  Long-term deprivation affects visual perception and cortex , 2003, Nature Neuroscience.

[40]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[41]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[42]  M. Ptito,et al.  Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. , 2005, Brain : a journal of neurology.

[43]  Rebecca Saxe,et al.  Sensitive Period for a Multimodal Response in Human Visual Motion Area MT/MST , 2010, Current Biology.

[44]  R. K. Simpson Nature Neuroscience , 2022 .

[45]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[46]  Catherine J. Mondloch,et al.  Missing sights: consequences for visual cognitive development , 2005, Trends in Cognitive Sciences.

[47]  F. Rösler,et al.  Speech processing activates visual cortex in congenitally blind humans , 2002, The European journal of neuroscience.

[48]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[49]  M. Catani,et al.  The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography , 2014, Cortex.

[50]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[51]  M. Raichle,et al.  Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. , 2002, Journal of neurophysiology.

[52]  Tanya Orlov,et al.  Superior Serial Memory in the Blind: A Case of Cognitive Compensatory Adjustment , 2007, Current Biology.

[53]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[54]  R. Zatorre,et al.  A Functional Neuroimaging Study of Sound Localization: Visual Cortex Activity Predicts Performance in Early-Blind Individuals , 2005, PLoS biology.

[55]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[56]  Chunshui Yu,et al.  Whole brain functional connectivity in the early blind. , 2007, Brain : a journal of neurology.

[57]  Uri Hasson,et al.  Congenital blindness is associated with large-scale reorganization of anatomical networks , 2016, NeuroImage.

[58]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[59]  G. Vandewalle,et al.  Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans , 2011, Proceedings of the National Academy of Sciences.

[60]  Stephen M. Smith,et al.  Permutation inference for the general linear model , 2014, NeuroImage.

[61]  M. Stryker,et al.  Development and Plasticity of the Primary Visual Cortex , 2012, Neuron.

[62]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.