Task-Modulated Coactivation of Vergence Neural Substrates

While functional magnetic resonance imaging (fMRI) has identified which regions of interests (ROIs) are functionally active during a vergence movement (inward or outward eye rotation), task-modulated coactivation between ROIs is less understood. This study tested the following hypotheses: (1) significant task-modulated coactivation would be observed between the frontal eye fields (FEFs), the posterior parietal cortex (PPC), and the cerebellar vermis (CV); (2) significantly more functional activity and task-modulated coactivation would be observed in binocularly normal controls (BNCs) compared with convergence insufficiency (CI) subjects; and (3) after vergence training, the functional activity and task-modulated coactivation would increase in CIs compared with their baseline measurements. A block design of sustained fixation versus vergence eye movements stimulated activity in the FEFs, PPC, and CV. fMRI data from four CI subjects before and after vergence training were compared with seven BNCs. Functional activity was assessed using the blood oxygenation level dependent (BOLD) percent signal change. Task-modulated coactivation was assessed using an ROI-based task-modulated coactivation analysis that revealed significant correlation between the FEF, PPC, and CV ROIs. Prior to vergence training, the CIs had a reduced BOLD percent signal change compared with BNCs for the CV (p<0.05), FEFs, and PPC (p<0.01). The BOLD percent signal change increased within the CV, FEF, and PPC ROIs (p<0.001) as did the task-modulated coactivation between the FEFs and CV as well as the PPC and CV (p<0.05) when comparing the CI pre- and post-training datasets. Results from the Convergence Insufficiency Symptom Survey were correlated to the percent BOLD signal change from the FEFs and CV (p<0.05).

[1]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[2]  Jody C. Culham,et al.  fMRI reveals a preference for near viewing in the human parieto-occipital cortex , 2007, NeuroImage.

[3]  G. Wylie,et al.  Increased functional connectivity within memory networks following memory rehabilitation in multiple sclerosis , 2012, Brain Imaging and Behavior.

[4]  A. Sprenger,et al.  Vergence deficits in patients with cerebellar lesions. , 2009, Brain : a journal of neurology.

[5]  B. Velichkovsky,et al.  Eye tracking and usability research: An introduction to the special issue , 2008 .

[6]  Zoï Kapoula,et al.  Saccades during symmetrical vergence , 2008, Graefe's Archive for Clinical and Experimental Ophthalmology.

[7]  Bharat B. Biswal,et al.  Functional anatomy of predictive vergence and saccade eye movements in humans: A functional MRI investigation , 2010, Vision Research.

[8]  R H Wurtz,et al.  Disparity sensitivity of frontal eye field neurons. , 2000, Journal of neurophysiology.

[9]  Simon B. Eickhoff,et al.  An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data , 2013, NeuroImage.

[10]  S. Ogawa,et al.  Biophysical and Physiological Origins of Blood Oxygenation Level-Dependent fMRI Signals , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[11]  Aldo Genovesio,et al.  Integration of retinal disparity and fixation-distance related signals toward an egocentric coding of distance in the posterior parietal cortex of primates. , 2004, Journal of neurophysiology.

[12]  M. T. Bergen,et al.  Short-term predictive changes in the dynamics of disparity vergence eye movements. , 2005, Journal of vision.

[13]  G Lynn Mitchell,et al.  Treatment of Convergence Insufficiency in Childhood: A Current Perspective , 2009, Optometry and vision science : official publication of the American Academy of Optometry.

[14]  L. Laatsch,et al.  Changes in fMRI activation following rehabilitation of reading and visual processing deficits in subjects with traumatic brain injury , 2006, Brain injury.

[15]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[16]  Bharat B. Biswal,et al.  Differentiation between Vergence and Saccadic Functional Activity within the Human Frontal Eye Fields and Midbrain Revealed through fMRI , 2011, PloS one.

[17]  G. J. van der Wildt,et al.  Effects of vision restoration training on early visual cortex in patients with cerebral blindness investigated with functional magnetic resonance imaging. , 2011, Journal of neurophysiology.

[18]  Ravi S. Menon,et al.  Functional connectivity of the frontal eye fields in humans and macaque monkeys investigated with resting-state fMRI. , 2012, Journal of neurophysiology.

[19]  J. Hirsch,et al.  Distinct cortical areas associated with native and second languages , 1997, Nature.

[20]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[21]  Egill Rostrup,et al.  Motion or activity: their role in intra- and inter-subject variation in fMRI , 2005, NeuroImage.

[22]  Paul A Taylor,et al.  Segregation of frontoparietal and cerebellar components within saccade and vergence networks using hierarchical independent component analysis of fMRI , 2011, Visual Neuroscience.

[23]  G. Lynn Mitchell,et al.  The Convergence Insufficiency Treatment Trial: Design, Methods, and Baseline Data , 2008, Ophthalmic epidemiology.

[24]  Z. Kapoula,et al.  Effects of transcranial magnetic stimulation of the posterior parietal cortex on saccades and vergence , 2001, Neuroreport.

[25]  Toru Nakamura,et al.  Resting Network Plasticity Following Brain Injury , 2009, PloS one.

[26]  B. Velichkovsky,et al.  Eye typing in application: A comparison of two interfacing systems with ALS patients , 2008 .

[27]  J. Grisham.  Visual therapy results for convergence insufficiency: a literature review. , 1988, American journal of optometry and physiological optics.

[28]  Mary E. Meyerand,et al.  Age-Related Differences in Test-Retest Reliability in Resting-State Brain Functional Connectivity , 2012, PloS one.

[29]  K. Kiehl,et al.  Reproducibility of the hemodynamic response to auditory oddball stimuli: A six‐week test–retest study , 2003, Human brain mapping.

[30]  John C Gore,et al.  Neural systems for compensation and persistence: young adult outcome of childhood reading disability , 2003, Biological Psychiatry.

[31]  Gregory G. Brown,et al.  Reproducibility of functional MR imaging: preliminary results of prospective multi-institutional study performed by Biomedical Informatics Research Network. , 2005, Radiology.

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

[33]  L. Pickwell,et al.  THE SIGNIFICANCE OF INADEQUATE CONVERGENCE , 1981, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[34]  Kikuro Fukushima,et al.  Coding of smooth eye movements in three-dimensional space by frontal cortex , 2002, Nature.

[35]  K. Fukushima,et al.  Vergence eye movement signals in the cerebellar dorsal vermis. , 2008, Progress in brain research.

[36]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[37]  Paul D. Gamlin,et al.  An area for vergence eye movement in primate frontal cortex , 2000, Nature.

[38]  Daniel S. Margulies,et al.  Long-term effects of motor training on resting-state networks and underlying brain structure , 2011, NeuroImage.

[39]  N. Geschwind.  The Organization of Language and the Brain: Language disorders after brain damage help in elucidating the neural basis of verbal behavior , 1970 .

[40]  Yanning H. Han,et al.  Properties of anticipatory vergence responses. , 2002, Investigative ophthalmology & visual science.

[41]  Emiliano Brunamonti,et al.  Reaching in Depth: Hand Position Dominates over Binocular Eye Position in the Rostral Superior Parietal Lobule , 2009, The Journal of Neuroscience.

[42]  Z. Kapoula,et al.  Transcranial magnetic stimulation of the posterior parietal cortex delays the latency of both isolated and combined vergence–saccade movements in humans , 2004, Neuroscience Letters.

[43]  H. Sakata,et al.  Parietal neurons represent surface orientation from the gradient of binocular disparity. , 2000, Journal of neurophysiology.

[44]  F. Chollet,et al.  Within-Session and Between-Session Reproducibility of Cerebral Sensorimotor Activation: A Test–Retest Effect Evidenced with Functional Magnetic Resonance Imaging , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[45]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[46]  B. Biswal,et al.  The resting brain: unconstrained yet reliable. , 2009, Cerebral cortex.

[47]  O. Dietrich,et al.  Test–retest reproducibility of the default‐mode network in healthy individuals , 2009, Human brain mapping.

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

[49]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[50]  Keith R Thulborn,et al.  Reproducibility of activation maps for longitudinal studies of visual function by functional magnetic resonance imaging. , 2012, Investigative ophthalmology & visual science.

[51]  Mitchell Scheiman,et al.  Validity and reliability of the revised convergence insufficiency symptom survey in adults , 2004, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[52]  M E Meyerand,et al.  Reliability of functional MR imaging with word-generation tasks for mapping Broca's area. , 2001, AJNR. American journal of neuroradiology.

[53]  M. Filippi,et al.  Changes of brain resting state functional connectivity predict the persistence of cognitive rehabilitation effects in patients with multiple sclerosis , 2014, Multiple sclerosis.

[54]  Kikuro Fukushima,et al.  Visual and vergence eye movement-related responses of pursuit neurons in the caudal frontal eye fields to motion-in-depth stimuli , 2005, Experimental Brain Research.

[55]  H. Sakata,et al.  Neural representation of three-dimensional features of manipulation objects with stereopsis , 1999, Experimental Brain Research.

[56]  Arno Villringer,et al.  Resting developments: a review of fMRI post-processing methodologies for spontaneous brain activity , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.

[57]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[58]  W. Graf,et al.  Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. , 2010, Cerebral cortex.

[59]  O. Tzeng,et al.  The dorsal attentional system in oculomotor learning of predictive information , 2013, Front. Hum. Neurosci..

[60]  N Jon Shah,et al.  Assessment of reliability in functional imaging studies , 2003, Journal of magnetic resonance imaging : JMRI.

[61]  F. Bremmer,et al.  Test–retest reliability of fMRI activation generated by different saccade tasks , 2014, Journal of magnetic resonance imaging : JMRI.

[62]  Á. Pascual-Leone,et al.  Longitudinal Changes of Resting-State Functional Connectivity During Motor Recovery After Stroke , 2011, Stroke.

[63]  Olivier A. Coubard,et al.  Role of the Posterior Parietal Cortex in the Initiation of Saccades and Vergence: Right/Left Functional Asymmetry , 2005, Annals of the New York Academy of Sciences.

[64]  K R Thulborn,et al.  Investigating the neurobiological basis of cognitive rehabilitation therapy with fMRI , 2004, Brain injury.

[65]  Silvio P. Sabatini,et al.  Eye Position Encoding in Three-Dimensional Space: Integration of Version and Vergence Signals in the Medial Posterior Parietal Cortex , 2012, The Journal of Neuroscience.

[66]  Yanning H. Han,et al.  Anticipatory Saccadic‐Vergence Responses in Humans , 2002, Annals of the New York Academy of Sciences.

[67]  Ali-Mohammad Golestani,et al.  Longitudinal Evaluation of Resting-State fMRI After Acute Stroke With Hemiparesis , 2013, Neurorehabilitation and neural repair.

[68]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[69]  L E Mays,et al.  Neurons in monkey parietal area LIP are tuned for eye-movement parameters in three-dimensional space. , 1995, Journal of neurophysiology.

[70]  Paul D. Gamlin,et al.  The role of cerebro-ponto-cerebellar pathways in the control of vergence eye movements , 1996, Eye.

[71]  P. Downing,et al.  Within‐subject reproducibility of category‐specific visual activation with functional MRI , 2005, Human brain mapping.

[72]  K. Fukushima,et al.  Involvement of the cerebellar dorsal vermis in vergence eye movements in monkeys. , 2008, Cerebral cortex.

[73]  N. Chiaravalloti,et al.  Vision Therapy in Adults with Convergence Insufficiency: Clinical and Functional Magnetic Resonance Imaging Measures , 2010, Optometry and vision science : official publication of the American Academy of Optometry.

[74]  V. Glauche,et al.  Test–retest reliability of event-related functional MRI in a probabilistic reversal learning task , 2009, Psychiatry Research: Neuroimaging.

[75]  C. Dickey,et al.  Long-Term Reproducibility Analysis of Fmri using Hand Motor Task , 2005, The International journal of neuroscience.

[76]  R. Cox,et al.  Test-retest precision of functional MR in sensory and motor task activation. , 1996, AJNR. American journal of neuroradiology.

[77]  Qing Yang,et al.  TMS over the left posterior parietal cortex prolongs latency of contralateral saccades and convergence. , 2004, Investigative ophthalmology & visual science.

[78]  Paul D. Gamlin.  Neural Mechanisms for the Control of Vergence Eye Movements , 2002, Annals of the New York Academy of Sciences.