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Selective Relationships Between Sensory System White Matter Connectivity and Sensory and Cognitive Function in Aged Macaques

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Selective Relationships Between Sensory System White Matter Connectivity and Sensory and Cognitive Function in Aged Macaques Selective Relationships Between Sensory System White Matter Connectivity And Sensory And Cognitive Function In Aged Macaques Item Type text; Electronic Thesis Authors De La Peña, Nicole Marie Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 30/09/2021 22:53:00 Item License http://rightsstatements.org/vocab/InC/1.0/ Link to Item http://hdl.handle.net/10150/632647 SELECTIVE RELATIONSHIPS BETWEEN SENSORY SYSTEM WHITE MATTER CONNECTIVITY AND SENSORY AND COGNITIVE FUNCTION IN AGED MACAQUES By NICOLE MARIE DE LA PEÑA __________________ A Thesis Submitted to the Honors College In Partial Fulfillment of the Bachelor’s Degree With Honors In Neuroscience and Cognitive Science UNIVERSITY OF ARIZONA M A Y 2 0 1 9 Approved by: Dr. Carol Barnes, PhD Department of Psychology, Neurology and Neuroscience 2 Selective Relationships Between Sensory System White Matter Connectivity and Sensory and Cognitive Function in Aged Macaques Authors Nicole M. De La Peña1,2, Daniel T. Gray1,2, Lavanya Umapathy3, Sara N. Burke4, James R. Engle1,2, Theodore P. Trouard2,5, Carol A. Barnes1,2,6 Author Affiliations 1Division of Neural System, Memory & Aging, University of Arizona, Tucson, AZ 2Evelyn F. McKnight Brain Institute, University of Arizona, Tucson, AZ 3Electrical and Computer Engineering, University of Arizona, Tucson, AZ 4Evelyn F. McKnight Brain Institute, University of Florida, Gainesville, FL 5Department of Biomedical Engineering, University of Arizona, Tucson, AZ 6Departments of Psychology, Neurology and Neuroscience, University of Arizona, Tucson, AZ 3 Abstract Normative aging results in deficits in both auditory and visual function, along with degradation of select cognitive functions. Studies have shown that sensory function is a predictor of late-life cognitive abilities, though the neurobiological base of this relationship is unclear. Previously our group found that the connectivity of medial temporal lobe-associated white matter was related to better auditory processing abilities and temporal lobe-dependent cognitive functions. This study concluded that shared impacts of aging on temporal lobe structures could account for the selectivity in these relationships. However, little is known about the association between sensory system white matter connectivity and sensory and cognitive function with age. In this study, adult and aged bonnet macaque monkeys were behaviorally characterized and evaluated for auditory and visual function. Measures of auditory and visual system white matter connectivity were extracted using diffusion MRI and probabilistic tractography. We found that higher connectivity of callosal auditory fibers was associated with better auditory function, and higher connectivity of the posterior forceps and optic radiation were associated with better visual function. Higher connectivity of auditory system white matter was associated with better performance on certain temporal-lobe dependent cognitive tasks. Our results support the idea that a shared impact of aging on temporal lobe structures could partially drive relationships between auditory processing and temporal lobe-dependent cognition. 4 Introduction Relationship between Sensory and Cognitive Function The normative aging process results in decreased functioning in multiple cognitive domains, as well as in sensory systems, especially in the modalities of hearing and vision. In fact, approximately one third of people over the age of 65 are affected by disabling hearing loss and around one fifth of adults over the age of 60 have some degree of visual impairment (Bourne et al., 2017; Brown and Barrett, 2011). Likewise, cognitive abilities, such as executive function, perceptual speed, and memory, tend to decline with age (Madden et al., 2012). Over the past 20 years, there has been an increase in evidence suggesting that there is an association between age-related cognitive decline and sensory deterioration (e.g. Baltes and Lindenberger, 1997; Li and Lindenberger, 2002; Lindenberger and Baltes, 1994). These studies have suggested that sensory function is a strong predictor of late-life individual variability in intelligence, with visual and auditory acuity accounting for around 93% of age-related individual differences in cognitive abilities (Li and Lindenberger, 2002; Lindenberger and Baltes, 1994). When assessments of auditory, visual, and tactile temporal processing were measured, it was found that age, overall sensory processing, and overall cognitive function were significantly correlated (Humes et al., 2013). Critically, when sensory processing was held constant in the model, the correlation between age and cognitive functioning was eliminated (Humes et al., 2013). The correlation between sensory and cognitive impairment, however, was usually present after adjusting for age (Roberts and Allen, 2016). This suggests that age-related changes in cognition may be mediated by age-related changes in sensory processing (Humes et al., 2013). Along with the correlation between sensory function and cognitive abilities, the risk of incident dementia and possibly even Alzheimer’s disease increases with the severity of age-related hearing loss, or presbycusis (Jayakody et al., 2018a; Lin et al., 2011). Additionally, presbycusis is positively correlated with late-life depression, anxiety, social isolation, and stress, which can exacerbate the aging process by increasing certain risk factors for age-associated diseases (Jayakody et al., 2018a, 2018b). Therefore, it is important to consider the prospect of sensory aids in not only correcting for sensory deficits, but also in increasing cognitive function, reducing the risk of dementia and Alzheimer’s disease, and improving the 5 quality of life for older individuals. For instance, it has been shown that older individuals who received cochlear implants have a decrease in stress and depression levels, while also improving in short term memory, spatial working memory, and executive function (Castiglione et al., 2016; Jayakody et al., 2017; Sonnet et al., 2017). Age-Related Changes in White Matter Connectivity Another hallmark of the normal aging process is a decline in the microstructural integrity of white matter throughout the central nervous system, as well as an overall reduction in the volume of white matter in the cerebral cortex (Peters et al., 1996). In contrast, age-related declines in the numbers of neurons in the neocortex and hippocampus is not observed in rhesus monkeys (Makris et al., 2007; Peters et al., 1996; West et al., 1993). In humans, there similarly does not appear to be a loss of neurons with age, although some studies have shown changes in neuronal numbers (e.g. Simic et al., 1997). Decreased white matter integrity throughout the brain is thought to result in a disconnection of widely distributed neural networks and an inability to integrate information, which is important for executive function, perceptual speed, and memory (Makris et al., 2007; Madden et al., 2012). One method of obtaining quantitative estimates of white matter connectivity is to use diffusion magnetic resonance imaging (dMRI) techniques, such as diffusion tensor imaging (DTI). DTI measures the directionality of the displacement of water molecules across brain tissue (Madden et al., 2009). One of the most frequently used summary measures of DTI is fractional anisotropy (FA), a scalar value where higher values reflect higher directional dependence of diffusion (Madden et al., 2009). It is not entirely clear what FA measures biologically, but many consider this value to be a proxy for white matter integrity (Madden et al., 2009). Age-related changes in fractional anisotropy are thought to be more prominent in areas of the brain that become myelinated later in life being more susceptible to deterioration as compared to early myelinating regions (Bartzokis et al., 2004; Davis et al., 2009; Pfefferbaum et al., 2005). It has been shown that age is associated with a decrease in FA in the genu, rostral body, and isthmus of the corpus callosum, as well as the frontal forceps and hippocampal commissure (Bartzokis et al., 2004; Ota et al., 6 2006; Pfefferbaum et al., 2005; Zahr et al., 2009). The literature on age-related white matter decline and its impact on age-related cognitive deficits is inconsistent in its conclusions. In several studies, a decline in FA values in the anterior tracts, such as the genu of the corpus callosum, was associated with poorer performance on executive function tasks, problem-solving tasks, and processing speed (Davis et al., 2009; Kennedy and Raz, 2009; Makris et al., 2007; Zahr et al., 2009). FA values in more posterior tracts, such as the splenium, correlated with performance on visual memory tasks and task switching (Davis et al., 2009; Kennedy and Raz, 2009). These studies indicate that the integrity of different white matter tracts may mediate distinct aspects of cognitive decline. Other studies challenge this hypothesis, however. Salami et al., 2012, for example, found that white matter integrity in the body of the corpus callosum mediated age-related reductions in processing speed but not visuospatial ability or fluency, suggesting that compromised white matter is not a major contributor to decreased cognitive
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