Spatial and temporal sensitivity degradation of primary visual cortical cells in senescent rhesus monkeys

Human visual function declines with age. Much of this decline is mediated by changes in the central visual pathways. In this study we compared the spatial and temporal sensitivities of striate cortical cells in young and old paralysed macaque monkeys. Extracellular single‐unit recordings were employed. Our results show that cortical neurons in old monkeys exhibit lower optimal spatial and temporal frequencies, lower spatial resolution and lower high temporal frequency cut‐offs than do cells in young adult monkeys. These changes in old monkeys are accompanied by increased visually evoked responses, increased spontaneous activities and decreased signal‐to‐noise ratios. The increased excitability of cells in old animals is consistent with an age‐related degeneration of intracortical inhibition. The degradation of spatial and temporal function in old striate cortex should contribute to the decline in visual function that accompanies normal aging.

[1]  Donald J. Woodward,et al.  Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin microiontophoresis , 1990, Brain Research.

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

[3]  P. Bennett,et al.  Effects of aging on calculation efficiency and equivalent noise. , 1999, Journal of the Optical Society of America. A, Optics, image science, and vision.

[4]  Mark J. West,et al.  Regionally specific loss of neurons in the aging human hippocampus , 1993, Neurobiology of Aging.

[5]  Patrick R Hof,et al.  Morphological alterations in neurons forming corticocortical projections in the neocortex of aged Patas monkeys , 2002, Neuroscience Letters.

[6]  Xiangrui Li,et al.  Effects of bicuculline on direction-sensitive relay cells in the dorsal lateral geniculate nucleus (LGNd) of cats , 2000, Brain Research.

[7]  A. Sillito The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. , 1975, The Journal of physiology.

[8]  M. Brigell,et al.  The effects of age on steady-state pattern electroretinograms and visual evoked potentials , 2004, Documenta Ophthalmologica.

[9]  A. Wagner,et al.  Changes in anesthetic sensitivity and glutamate receptors in the aging canine brain. , 2000, The journals of gerontology. Series A, Biological sciences and medical sciences.

[10]  D. Head,et al.  Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. , 1997, Cerebral cortex.

[11]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[12]  Y. de Koninck,et al.  Loss of Presynaptic and Postsynaptic Structures Is Accompanied by Compensatory Increase in Action Potential-Dependent Synaptic Input to Layer V Neocortical Pyramidal Neurons in Aged Rats , 2000, The Journal of Neuroscience.

[13]  V Bringuier,et al.  Noradrenergic modulation of functional selectivity in the cat visual cortex: an in vivo extracellular and intracellular study , 2002, Neuroscience.

[14]  R. Sekuler,et al.  Assessing spatial vision of older people. , 1982, American journal of optometry and physiological optics.

[15]  David C. Burr,et al.  The effects of ageing on the pattern electroretinogram and visual evoked potential in humans , 1991, Vision Research.

[16]  Lihua He,et al.  Functional degradation of visual cortical cells in old cats , 2006, Neurobiology of Aging.

[17]  H. Haug,et al.  The significance of morphometric procedures in the investigation of age changes in cytoarchitectonic structures of human brain. , 1984, Journal fur Hirnforschung.

[18]  N. A. Lazareva,et al.  Orientation tuning and receptive field structure in cat striate neurons during local blockade of intracortical inhibition , 1998, Neuroscience.

[19]  Alan Peters,et al.  A further evaluation of the effect of age on striate cortex of the rhesus monkey , 1997, Neurobiology of Aging.

[20]  Christopher Patrick Taylor,et al.  Aging Reduces Center-Surround Antagonism in Visual Motion Processing , 2005, Neuron.

[21]  W. Hoffman,et al.  Plasma and myocardial catecholamine levels in young and aged rats during halothane anesthesia , 1985, Neurobiology of Aging.

[22]  Y. Zhou,et al.  Adaptation of visually evoked responses of relay cells in the dorsal lateral geniculate nucleus of the cat following prolonged exposure to drifting gratings , 1996, Visual Neuroscience.

[23]  R. Sekuler,et al.  Improving visual perception in older observers. , 1986, Journal of gerontology.

[24]  R. DeTeresa,et al.  Neocortical cell counts in normal human adult aging , 1987, Annals of neurology.

[25]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[26]  D Regan,et al.  Spatial frequency discrimination in normal vision and in patients with multiple sclerosis. , 1982, Brain : a journal of neurology.

[27]  B. Waterhouse,et al.  Noradrenergic modulation of cat area 17 neuronal responses to moving visual stimuli , 1994, Brain Research.

[28]  J. Mendelson,et al.  Age-related changes in the visual cortex , 2002, Vision Research.

[29]  D. Woodward,et al.  Modification of the visual response properties of cerebellar neurons by norepinephrine , 1990, Brain Research.

[30]  E. Masliah,et al.  Quantitative synaptic alterations in the human neocortex during normal aging , 1993, Neurology.

[31]  R. Sekuler,et al.  Human aging and spatial vision. , 1980, Science.

[32]  R. Sekuler,et al.  Vision, aging, and driving: the problems of older drivers. , 1992, Journal of gerontology.

[33]  P. D. Spear,et al.  Effects of aging on the primate visual system: spatial and temporal processing by lateral geniculate neurons in young adult and old rhesus monkeys. , 1994, Journal of neurophysiology.

[34]  I. Akiguchi,et al.  Age-related changes of pyramidal cell basal dendrites in layers III and V of human motor cortex: A quantitative Golgi study , 2004, Acta Neuropathologica.

[35]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[36]  D. Maurer,et al.  Influence of monocular deprivation during infancy on the later development of spatial and temporal vision , 2000, Vision Research.

[37]  Alan Peters,et al.  The effect of aging on the neuronal population within area 17 of adult rat cerebral cortex , 1983, Neurobiology of Aging.

[38]  K. Haywood,et al.  Altered pattern evoked retinal and cortical potentials associated with human senescence. , 1986, Current eye research.

[39]  A. Leventhal,et al.  Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys , 2000, Nature Neuroscience.

[40]  D. Kline,et al.  Age, the eye, and the visual channels: contrast sensitivity and response speed. , 1983, Journal of gerontology.

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

[42]  D L Rosene,et al.  Feature article: are neurons lost from the primate cerebral cortex during normal aging? , 1998, Cerebral cortex.

[43]  N. Daw,et al.  Effect of electrical stimulation of locus coeruleus on the activity of neurons in the cat visual cortex. , 1989, Journal of neurophysiology.

[44]  A. Leventhal,et al.  GABA and Its Agonists Improved Visual Cortical Function in Senescent Monkeys , 2003, Science.

[45]  P. Poppers,et al.  Electroencephalographic Burst Suppression in Elderly and Young Patients Anesthetized with Isoflurane , 1989, Anesthesia and Analgesia.

[46]  H. Uylings,et al.  Neuronal Changes in Normal Human Aging and Alzheimer's Disease , 2002, Brain and Cognition.