Altered White Matter Structure In Adults Following Early Monocular Enucleation Nikita Ann Wong A ...

108 Pages·2017·2.81 MB·English

Altered White Matter Structure In Adults Following Early Monocular
Enucleation

Nikita Ann Wong

A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN
PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF
MASTERS

Graduate Program in Psychology
York University
Toronto, Ontario

July 2017

© Nikita Ann Wong, 2017
ABSTRACT
Visual deprivation from early monocular enucleation (the surgical removal of one eye) results in
a number of long-term behavioural and morphological adaptations in the visual, auditory, and
multisensory systems. This thesis aims to investigate how the loss of one eye early in life affects
structural connectivity within the brain. A combination of diffusion tensor imaging and
tractography was used to examine structural differences in 18 tracts throughout the brain of adult
participants who had undergone early monocular enucleation compared to binocularly intact
controls. We report significant structural changes to white matter in early monocular enucleation
participants that extend beyond the primary visual pathway to include interhemispheric, auditory
and multisensory tracts, as well as several long association fibres. Overall these results suggest
that early monocular enucleation has long-term effects on white matter structure throughout the
brain.

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ACKNOWLEDGMENTS
My sincere thanks go first to my supervisor Dr. Jennifer Steeves whose support and
guidance throughout my graduate education have been paramount to my development as a
researcher. I am grateful for the opportunity to have worked alongside you and to have been a
member of your lab. This thesis would not have been possible without you.
I would also like to acknowledge the support of my committee members and all of my
participants for the dedication of their time, as well as the Natural Sciences and Engineering
Council of Canada and the Canada Foundation for Innovation for funding this research.
I must express my many thanks to my labmates in the Perceptual Neuroscience Lab,
Stefania Moro and Sara Rafique. Your constant willingness to provide help and answer my
unending stream of questions, along with your advice on all matters has made all the difference
over the past two years. I attribute much of my remaining sanity to the laughs we have shared.
Special thanks also go to all of my friends, especially Sarah Wall, who have been endless
in their encouragement and who endured countless conversations about graduate school with
minimal complaint.
Above all, I have to thank my family – Mom, Dad, and Tianna – for their unwavering
love and support over the course of my university career. Without you I would have never made
it this far!
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TABLE OF CONTENTS
ABSTRACT ................................................................................................................................... 1
ACKNOWLEDGMENTS ........................................................................................................... iii
TABLE OF CONTENTS ............................................................................................................ iv
LIST OF FIGURES .................................................................................................................... vii
ABBREVIATIONS .................................................................................................................... viii
CHAPTER I: GENERAL INTRODUCTION ........................................................................... 1
Monocular enucleation and behavioural adaptations ......................................................................... 1
Visual adaptations. ............................................................................................................................... 2
Audiovisual adaptations. ...................................................................................................................... 6
Structural changes following early monocular enucleation ............................................................... 8
Early sensory deprivation and white matter structure ..................................................................... 11
Diffusion tensor imaging ...................................................................................................................... 13
Tractography. ..................................................................................................................................... 14
DTI of the visual and auditory systems. ............................................................................................. 15
DTI and novel tracts. .......................................................................................................................... 17
DTI in clinical populations. ................................................................................................................ 17
Summary ............................................................................................................................................... 19
Research aims ....................................................................................................................................... 20
Hypotheses. ........................................................................................................................................ 21
Visual system. ................................................................................................................................................ 22
Auditory system. ............................................................................................................................................ 23
Audiovisual system. ....................................................................................................................................... 23
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Other major white matter tracts. ..................................................................................................................... 24
CHAPTER II: METHODS ........................................................................................................ 25
Participants ........................................................................................................................................... 25
Early monocular enucleation (ME) participants. ............................................................................... 25
Binocular control (BC) participants. .................................................................................................. 25
Data acquisition .................................................................................................................................... 25
Data processing ..................................................................................................................................... 26
Pre-processing. ................................................................................................................................... 26
Mask creation. .................................................................................................................................... 27
Probabilistic tractography. ................................................................................................................. 27
Statistical analysis ................................................................................................................................. 28
CHAPTER III: RESULTS ......................................................................................................... 30
Optic radiations (LGN-V1) .................................................................................................................. 30
V1-LGN ................................................................................................................................................. 31
V1-V1 ..................................................................................................................................................... 34
Auditory radiations (MGB-A1) ........................................................................................................... 35
A1-MGB ................................................................................................................................................ 37
A1-V1 ..................................................................................................................................................... 39
V1-A1 ..................................................................................................................................................... 41
Other major white matter tracts ......................................................................................................... 43
CHAPTER IV: DISCUSSION ................................................................................................... 46
Review of diffusion indices ................................................................................................................... 46
Visual system tracts of interest ............................................................................................................ 50
Optic radiations. ................................................................................................................................. 50
V1-LGN. ............................................................................................................................................ 52
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V1-V1. ................................................................................................................................................ 53
Nonvisual tracts of interest .................................................................................................................. 56
Other major white matter tracts ......................................................................................................... 60
Conclusions ............................................................................................................................................ 66
Limitations ............................................................................................................................................ 70
Future directions ................................................................................................................................... 74
REFERENCES ............................................................................................................................ 77

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LIST OF FIGURES
Figure 1. Mean values for diffusion indices in the optic radiations for all participants................29
Figure 2. Mean values for diffusion indices in the V1-LGN tracts for all participants.................30
Figure 3. Mean values for diffusion indices in the V1-V1 tracts for all participants....................31
Figure 4. Mean values for diffusion indices in the auditory radiations for all participants...........32
Figure 5. Mean values for diffusion indices in the A1-MGB tracts for all participants................33
Figure 6. Mean values for diffusion indices in the A1-V1 tracts for all participants....................34
Figure 7. Mean values for diffusion indices in the V1-A1 tracts for all participants....................35
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ABBREVIATIONS

3D Three-dimensional
A1 Primary auditory cortex
AD Axial diffusivity
ATR Anterior thalamic radiation
BC Binocular control
BEDPOSTX Bayesian estimation of diffusion parameters
obtained using sampling techniques for
modelling crossing fibres
BET Brain extraction tool
CSF Cerebral spinal fluid
dLGN Dorsal lateral geniculate nucleus
DSI Diffusion spectrum imaging
DTI Diffusion tensor imaging
FA Fractional anisotropy
FDR False-discovery rate
FDT FSL’s diffusion toolbox
FLIRT FSL’s linear registration tool
fMRI Functional magnetic resonance imaging
FNIRT FSL’s non-linear registration tool
FSL FMRIB3’s software library
HARDI High angular resolution diffusion imaging
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IFOF Inferior fronto-occipital fasciculus
ILF Inferior longitudinal fasciculus
JHU John Hopkins University
LGN Lateral geniculate nucleus
MD Mean diffusivity
ME Monocular enucleation
MGB Medial geniculate body
MNI Montreal Neurological Institute
MPRAGE Magnetisation-prepared rapid gradient-echo
MRI Magnetic resonance imaging
MRS Magnetic resonance spectroscopy
OKN Optokinetic nystagmus
PROBTRACKX Probabilistic tracking with crossing fibres
RD Radial diffusivity
SLF Superior longitudinal fasciculus
SLFt Superior longitudinal fasciculus (temporal)
TBSS Tract-based spatial statistics
TTC Time-to-collision
V1 Primary visual cortex
V2 Secondary visual cortex
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CHAPTER I: GENERAL INTRODUCTION
At birth, the visual system is far from mature, and normal development continues well
into adolescence. During this period, typical postnatal maturation of the visual system is
vulnerable to changes in sensory input, particularly in the first few years of life (e.g., Garey & de
Courten, 1983; Huttenlocher & de Courten, 1987). In instances where there is a complete loss of
input from a sensory modality (e.g., blindness) neural reorganisation often follows so that other
sensory systems recruit brain regions previously engaged by the lost sense (e.g., Merabet &
Pascual-Leone, 2010). If vision loss was not complete, but instead reduced only by half, as in the
case of the surgical removal of one eye, similar morphological changes might be expected, in
order to take full advantage of the remaining sensory inputs. This thesis will consider the
morphological adaptations that occur following partial visual deprivation from the loss of one
eye early in life.
Monocular enucleation and behavioural adaptations
A unique form of partial visual deprivation is monocular enucleation. Monocular
enucleation is the surgical removal of one eye, resulting in the complete deafferentation of 50%
of the visual input to the brain. Often the result of retinoblastoma, a childhood cancer of the
retina, the removal of an eye is distinct from other forms of monocular visual deprivation, such
as cataract (cloudy lens), strabismus (misalignment of the eyes), ptosis (eyelid droop), or
anisometropia (unequal focusing power of each eye). Unlike these other types of partial vision
loss, in which degraded visual input continues to reach the brain, monocular enucleation
completely removes all forms of visual input from one eye, making it a unique model for
examining the consequences of the loss of binocularity (Steeves, González & Steinbach, 2008).
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