An Investigation Into the Neural Basis of Convergence Eye Movements

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An Investigation Into the Neural Basis of Convergence Eye Movements An Investigation into the Neural Basis of Convergence Eye Movements Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Emmanuel Owusu Graduate Program in Vision Science The Ohio State University 2018 Dissertation Committee Marjean T. Kulp, Advisor Nicklaus F. Fogt, Co-Advisor Andrew J. Toole Bradley Dougherty Michael J. Earley Xiangrui Li 1 Copyrighted by Emmanuel Owusu 2018 2 Abstract Introduction: Different components of convergence are tonic convergence, disparity convergence, accommodative convergence and proximal. However, it is not clear whether these different components ultimately draw on similar innervational control. Better understanding of the neurology of convergence eye movements could lead to improvement in interventions for deficits in convergence eye movements. Therefore, the purpose of this dissertation is to investigate the neural basis for convergence eye movements in binocularly normal young adults. Methods: Two approaches were used. First, clinical measurements were used to determine the correlations among accommodative, disparity and proximal convergence eye movements, as well as between proximal convergence and vergence facility. These correlations were used as an index of the extent of overlaps in their neurological control. Second, functional magnetic resonance imaging (fMRI) was performed on a group of adults with normal binocular function as they converged their eyes in response to stimuli for accommodative, disparity, proximal and voluntary convergence eye movements. Results: In the clinical study, stimulus gradient accommodative convergence was negatively correlated with far-near proximal convergence (Spearman’s correlation = -0.6111, p < 0.0001). However, the correlation may be at least in part attributable to the inclusion of gradient AC/A as a component of the calculation of far-near proximal convergence. Disparity convergence ii did not correlate with measures of proximal convergence. Gradient accommodative convergence was not correlated with the amount of disparity convergence in operation (Spearman’s correlation = -0.1512, p=0.3649). Finally, proximal convergence was not correlated with vergence facility (Spearman’s correlation = +0.1107, p=0.5082 and - 0.0149, p=0.9291 for far-near proximal and +2.50D proximal, respectively). In the fMRI study, cluster-based group analysis showed that disparity vergence activated regions in the cuneus, lingual gyrus, precuneus, and middle occipital gyrus of the occipital cortex. Accommodative convergence stimulated regions in the occipital (cuneus and middle occipital gyrus), parietal (precuneus, superior parietal and postcentral) and frontal lobes (precentral and postcentral gyri). Proximal convergence activated regions in the occipital (cuneus and middle occipital gyrus) and parietal lobes (precuneus, inferior parietal lobule and superior parietal lobule). Voluntary convergence activated brain areas in the occipital (cuneus, lingual gyrus and middle occipital gyrus), temporal (middle temporal gyrus), and frontal lobes (precentral and middle central gyri) as well as culmen and declive in the cerebellum. Each of the convergence stimuli activated the cuneus and middle occipital gyrus in the occipital lobe. In addition, both accommodative and proximal convergence eye movements activated the precuneus in the parietal lobe. Similarly, the accommodative and voluntary convergence eye movements both activated the precentral gyrus in the frontal lobe, and the disparity and voluntary convergence eye movements activated the lingual gyrus in the occipital lobe. Conclusion: The imaging study suggests that the convergence components share common neural control pathways even though iii each also retains unique neural activations. The clinical study suggests that the open-loop vergence components are independent. iv Dedication This document is dedicated to Mrs. Patricia Asuama Owusu, the mum and dad to the Owusu family while I was away on this pursuit. More is thy due than I can say… or pay. v Acknowledgments I am immensely grateful to my dissertation mentors Dr. Marjean Kulp and Dr. Nicklaus Fogt for their tireless and patient guidance during my graduate training. I also appreciate Dr. Andrew Toole who wrote the program for displaying the stimuli in the functional imaging study, and Dr. Nasser Kashou who helped in the design of the functional imaging study. In addition, I am grateful to Drs. Bradley Dougherty and Andrew Toole for serving on my Academic Progress Committee, and Drs. Michael Earley and Xiangrui Li for serving on my dissertation committee. Further, I appreciate Dr. Xiangrui Li’s great supervision of the functional imaging analysis. Also, I am grateful to the Ohio Lions Eye Research Foundation for generously providing funds for the functional imaging study. The Center for Behavioral Brain Imaging of the Department of Psychology, the Ohio State University provided pilot scan hours and assistance with logistics to implement the functional imaging study, and the American Academy of Optometry provided a Student’s Travel Fellowship to attend and present portions of the clinical study at Academy 2016 in Anaheim, CA. In addition, I gratefully acknowledge the Graduate Research Associateship from the College of Optometry, The Ohio State University which enabled me undertake my graduate training. Finally, I am very grateful to all the participants who volunteered to be in both studies. vi Vita 2014 to 2018 ……………………………….. Graduate Research Associate, The Ohio State University 2015 ………………………………………… Master of Optometry, University of KwaZulu-Natal, South Africa 2012 ………………………………………... Master of Science, University of London 2009 to 2014 ……………………………….. Technical Instructor, Kwame Nkrumah University of Science & Technology, Ghana 2001 to 2007 ………………………………… OD Optometry Kwame Nkrumah University of Science & Technology, Ghana 1997 to 1999 …………………………………. Sunyani Secondary School, Ghana Publications 1. Koomson, N. Y., Amedo, A. O., Owusu, E., Ampeh, P. B., Kobia-Acquah, E., & Bonsu, K. (2015). Under-correction of myopia reduces lag of accommodation in school children in Kumasi, Ghana. International Journal of Health Sciences, 5: 137-150 2. Koomson, N. Y., Amedo, A. O., Owusu, E., Ampeh, P. B., Kobia-Acquah, E., & Bonsu, K. (2014). Under-correction Induces Peripheral Myopic Defocus in School vii Children in Kumasi, Ghana. International Journal of Innovation and Applied Studies, 9(4), 1598 3. Kumah, D. B., Owusu, E., & Kyeremaa, F. A. (2013). Prevalence of hyperopia among school children in the Kumasi metropolis, Ghana. Journal of the Ghana Science Association, 14(1), 63-68 Fields of Study Major Field: Vision Science viii Table of Contents Abstract ............................................................................................................................... ii Dedication ........................................................................................................................... v Acknowledgments.............................................................................................................. vi Vita .................................................................................................................................... vii List of Tables .................................................................................................................... xii List of Figures .................................................................................................................. xiii Chapter 1: Introduction ....................................................................................................... 1 Background ..................................................................................................................... 1 The Maddox Components of Horizontal Vergence Response ........................................ 2 Open-Loop and Closed-Loop Vergence Errors and Vergence Control .......................... 5 Classifying Vergence Components Based on Control of Response Error ...................... 8 Feed-Forward and Feed-Back Control Systems in the Neural Control of Vergence ... 10 Conceptual Models on Control of Vergence Eye Movements ..................................... 13 Sequence for Vergence Eye Movement Response ....................................................... 17 Organization of Neural Control for Vergence Eye Movements ................................... 21 Methods for Investigating Vergence Eye Movements.................................................. 23 Assessing Vergence Eye Movements ........................................................................... 27 Chapter 2: Correlations among Vergence Eye Movements .............................................. 37 Background ................................................................................................................... 37 Contribution of Vergence Components to Total Vergence Response .......................... 38 Correlations among the Vergence Components ........................................................... 40 Rationale for the Study ................................................................................................. 42 Objectives ..................................................................................................................... 43 Hypotheses .................................................................................................................... 43 Chapter
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