Auditory and Visual System White Matter Is Differentially Impacted by Normative Aging in Macaques

• Published in: The Journal of neuroscience Vol. 40; no. 46; pp. 8913 - 8923
• Main Authors: Gray, Daniel T, De La Peña, Nicole M, Umapathy, Lavanya, Burke, Sara N, Engle, James R, Trouard, Theodore P, Barnes, Carol A
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 11.11.2020
• Subjects: Acoustic Stimulation; Age; Aging; Aging - physiology; Animals; Anisotropy; Assessments; Auditory Cortex - growth & development; Auditory Cortex - physiology; Auditory system; Brain; Cerebral hemispheres; Cochlea; Diffusion; Diffusion Magnetic Resonance Imaging; Diffusion Tensor Imaging; Domains; Electroencephalography; Evoked Potentials, Auditory, Brain Stem - physiology; Evoked Potentials, Visual - physiology; Female; Hearing; Information processing; Life span; Macaca radiata; Magnetic resonance imaging; Male; Monkeys; Neural networks; Neural Pathways - physiology; Neuroimaging; Organs; Photic Stimulation; Questions; Sense organs; Sensory evaluation; Sensory integration; Sensory perception; Sensory systems; Structure-function relationships; Substantia alba; Thalamus; Thalamus - physiology; Visual Cortex - growth & development; Visual Cortex - physiology; Visual pathways; Visual perception; Visual system; White Matter - growth & development; White Matter - physiology; thalamic radiation; diffusion MRI; sensory deficits; auditory brainstem response; splenium; visual evoked potential
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.1163-20.2020

Deficits in auditory and visual processing are commonly encountered by older individuals. In addition to the relatively well described age-associated pathologies that reduce sensory processing at the level of the cochlea and eye, multiple changes occur along the ascending auditory and visual pathways that further reduce sensory function in each domain. One fundamental question that remains to be directly addressed is whether the structure and function of the central auditory and visual systems follow similar trajectories across the lifespan or sustain the impacts of brain aging independently. The present study used diffusion magnetic resonance imaging and electrophysiological assessments of auditory and visual system function in adult and aged macaques to better understand how age-related changes in white matter connectivity at multiple levels of each sensory system might impact auditory and visual function. In particular, the fractional anisotropy (FA) of auditory and visual system thalamocortical and interhemispheric corticocortical connections was estimated using probabilistic tractography analyses. Sensory processing and sensory system FA were both reduced in older animals compared with younger adults. Corticocortical FA was significantly reduced only in white matter of the auditory system of aged monkeys, while thalamocortical FA was lower only in visual system white matter of the same animals. Importantly, these structural alterations were significantly associated with sensory function within each domain. Together, these results indicate that age-associated deficits in auditory and visual processing emerge in part from microstructural alterations to specific sensory white matter tracts, and not from general differences in white matter condition across the aging brain. Age-associated deficits in sensory processing arise from structural and functional alterations to both peripheral sensory organs and central brain regions. It remains unclear whether different sensory systems undergo similar or distinct trajectories in function across the lifespan. To provide novel insights into this question, this study combines electrophysiological assessments of auditory and visual function with diffusion MRI in aged macaques. The results suggest that age-related sensory processing deficits in part result from factors that impact the condition of specific white matter tracts, and not from general decreases in connectivity between sensory brain regions. Such anatomic specificity argues for a framework aimed at understanding vulnerabilities with relatively local influence and brain region specificity.