Age-related delay in visual and auditory evoked responses is mediated by white- and grey-matter differences

Slowing is a common feature of ageing, yet a direct relationship between neural slowing and brain atrophy is yet to be established in healthy humans. We combine magnetoencephalographic (MEG) measures of neural processing speed with magnetic resonance imaging (MRI) measures of white and grey matter in a large population-derived cohort to investigate the relationship between age-related structural differences and visual evoked field (VEF) and auditory evoked field (AEF) delay across two different tasks. Here we use a novel technique to show that VEFs exhibit a constant delay, whereas AEFs exhibit delay that accumulates over time. White-matter (WM) microstructure in the optic radiation partially mediates visual delay, suggesting increased transmission time, whereas grey matter (GM) in auditory cortex partially mediates auditory delay, suggesting less efficient local processing. Our results demonstrate that age has dissociable effects on neural processing speed, and that these effects relate to different types of brain atrophy.

[1]  Matthias Bethge,et al.  Reconstructing Stimuli from the Spike Times of Leaky Integrate and Fire Neurons , 2010, Front. Neurosci..

[2]  M. Onofrj,et al.  Age-related changes of evoked potentials , 1997, Neurophysiologie Clinique/Clinical Neurophysiology.

[3]  J. Helpern,et al.  Three‐dimensional characterization of non‐gaussian water diffusion in humans using diffusion kurtosis imaging , 2006, NMR in biomedicine.

[4]  John Duncan,et al.  Distinct aspects of frontal lobe structure mediate age-related differences in fluid intelligence and multitasking , 2014, Nature Communications.

[5]  Adriana Di Martino,et al.  Age‐related non‐Gaussian diffusion patterns in the prefrontal brain , 2008, Journal of magnetic resonance imaging : JMRI.

[6]  Age-related changes in brain neuromagnetic responses to face perception in humans , 2001, Neuroscience Letters.

[7]  Jennifer J. Lister,et al.  The aging auditory system: anatomic and physiologic changes and implications for rehabilitation , 2003, International journal of audiology.

[8]  G. Harding,et al.  Visual evoked magnetic fields to flash and pattern in 100 normal subjects , 1991, Vision Research.

[9]  N. A. Shaw,et al.  Age-dependent changes in the latency of the pattern visual evoked potential. , 1980, Electroencephalography and clinical neurophysiology.

[10]  Karl J. Friston,et al.  Modelling event-related responses in the brain , 2005, NeuroImage.

[11]  B. Ross,et al.  Effects of age and age-related hearing loss on the brain. , 2007, Journal of communication disorders.

[12]  N. Kraus,et al.  Aging Affects Neural Precision of Speech Encoding , 2012, The Journal of Neuroscience.

[13]  B. Renault,et al.  Age-related changes in brain responses to personally known faces: an event-related potential (ERP) study in humans , 2003, Neuroscience Letters.

[14]  P. Alku,et al.  Electromagnetic recordings reveal latency differences in speech and tone processing in humans. , 1999, Brain research. Cognitive brain research.

[15]  J. Rauschecker,et al.  Hierarchical Organization of the Human Auditory Cortex Revealed by Functional Magnetic Resonance Imaging , 2001, Journal of Cognitive Neuroscience.

[16]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[17]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[18]  G. Pearlson,et al.  Elucidating the contributions of processing speed, executive ability, and frontal lobe volume to normal age-related differences in fluid intelligence , 2000, Journal of the International Neuropsychological Society.

[19]  S A Hillyard,et al.  Effects of aging on event-related brain potentials and reaction times in an auditory oddball task. , 2007, Psychophysiology.

[20]  B. Renault,et al.  An ERP Study of Famous Face Incongruity Detection in Middle Age , 2001, Brain and Cognition.

[21]  Cam-CAN Group,et al.  The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) data repository: Structural and functional MRI, MEG, and cognitive data from a cross-sectional adult lifespan sample , 2017, NeuroImage.

[22]  D. Mackinnon,et al.  Tests of the Three-Path Mediated Effect , 2008 .

[23]  G. Recanzone,et al.  Spatial and temporal processing of single auditory cortical neurons and populations of neurons in the macaque monkey , 2011, Hearing Research.

[24]  N. Raz,et al.  Age, Sex and Regional Brain Volumes Predict Perceptual-Motor Skill Acquisition , 2005, Cortex.

[25]  L. Hughes,et al.  Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system , 2008, Journal of Experimental Biology.

[26]  A. Moskowitz,et al.  Age-related changes in the latency of the visual evoked potential: Influences of check size ☆ , 1981 .

[27]  Claude Alain,et al.  Neural encoding of sound duration persists in older adults , 2009, NeuroImage.

[28]  Erika P. Raven,et al.  Age-related slowing in cognitive processing speed is associated with myelin integrity in a very healthy elderly sample , 2011, Journal of clinical and experimental neuropsychology.

[29]  C C Wood,et al.  Developmental and aging changes in somatosensory, auditory and visual evoked potentials. , 1984, Electroencephalography and clinical neurophysiology.

[30]  U. Lindenberger,et al.  Cross-sectional age variance extraction: what's change got to do with it? , 2011, Psychology and aging.

[31]  Guillaume A. Rousselet,et al.  Healthy Aging Delays Scalp EEG Sensitivity to Noise in a Face Discrimination Task , 2010, Front. Psychology.

[32]  J. Helpern,et al.  Diffusional kurtosis imaging: The quantification of non‐gaussian water diffusion by means of magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[33]  Hari M. Bharadwaj,et al.  Report Why Middle-aged Listeners Have Trouble Hearing in Everyday Settings , 2022 .

[34]  Michael W. L. Chee,et al.  Cognitive function and brain structure correlations in healthy elderly East Asians , 2009, NeuroImage.

[35]  M. Eckert.  Slowing Down: Age-Related Neurobiological Predictors of Processing Speed , 2011, Front. Neurosci..

[36]  William D. Marslen-Wilson,et al.  The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) study protocol: a cross-sectional, lifespan, multidisciplinary examination of healthy cognitive ageing , 2014, BMC Neurology.

[37]  T. Salthouse.  The processing-speed theory of adult age differences in cognition. , 1996, Psychological review.

[38]  Gabriel Curio,et al.  PERTURBATIVE ANALYTICAL SOLUTIONS OF THE ELECTRIC FORWARD PROBLEM FOR REALISTIC VOLUME CONDUCTORS , 1999 .

[39]  Stefan R Schweinberger,et al.  Age-related slowing in face and name recognition: evidence from event-related brain potentials. , 2002, Psychology and aging.

[40]  P. D. Spear,et al.  Neural bases of visual deficits during aging , 1993, Vision Research.

[41]  Jesse S. Husk,et al.  Age-related delay in information accrual for faces: Evidence from a parametric, single-trial EEG approach , 2009, BMC Neuroscience.

[42]  S. Tobimatsu.  Aging and pattern visual evoked potentials. , 1995, Optometry and vision science : official publication of the American Academy of Optometry.

[43]  Vince D. Calhoun,et al.  Age-Related Changes in Processing Speed: Unique Contributions of Cerebellar and Prefrontal Cortex , 2010, Front. Hum. Neurosci..

[44]  S. Hillyard,et al.  Endogenous brain potentials associated with selective auditory attention. , 1980, Electroencephalography and clinical neurophysiology.

[45]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[46]  Ji Young Lee.  Aging and Speech Understanding , 2015, Journal of audiology & otology.

[47]  C Pantev,et al.  Magnetic and electric brain activity evoked by the processing of tone and vowel stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  J. Ford,et al.  Age-related changes in auditory event-related potentials. , 1980, Electroencephalography and clinical neurophysiology.

[49]  M. Xi,et al.  Changes in the axonal conduction velocity of pyramidal tract neurons in the aged cat , 1999, Neuroscience.

[50]  Hugo Alexandre Ferreira,et al.  Exploring the 3D geometry of the diffusion kurtosis tensor—Impact on the development of robust tractography procedures and novel biomarkers , 2015, NeuroImage.

[51]  Yuanye Ma,et al.  Degradation of signal timing in cortical areas V1 and V2 of senescent monkeys. , 2005, Cerebral cortex.

[52]  Paul M. Thompson,et al.  Myelin breakdown mediates age-related slowing in cognitive processing speed in healthy elderly men , 2013, Brain and Cognition.

[53]  T. Carrell,et al.  Central Auditory System Plasticity Associated with Speech Discrimination Training , 1995, Journal of Cognitive Neuroscience.

[54]  A. Peters.  The effects of normal aging on myelin and nerve fibers: A review , 2002, Journal of neurocytology.

[55]  Mary A. Peterson,et al.  Reduction in white matter connectivity, revealed by diffusion tensor imaging, may account for age-related changes in face perception , 2008 .

[56]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[57]  F. D. Silva,et al.  EEG and MEG: Relevance to Neuroscience , 2013, Neuron.

[58]  J. Covington,et al.  Olfactory event-related potentials and aging: normative data. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[59]  Guillaume A. Rousselet,et al.  Early ERPs to faces: aging, luminance, and individual differences , 2013, Front. Psychol..