Functional degradation of visual cortical cells in aged rats

Functional degradation of mammalian visual cortex is associated with aging. It has been hypothesized that much of the decline might be mediated by a degradation of cortical inhibitory system during senescence. In the present work, we compared the properties of adaptation, onset latency and signal-to-noise ratio in primary visual cortex of young and old rats using extracellular single-unit techniques. The short-term synaptic plasticity of young and old rats was also studied using field potential recording techniques. We found significant increased adaptation, prolonged onset latency, lower signal-to-noise ratio and decreased short-term synaptic plasticity in aged rats. The results are in accordance with previously reported functional declines in old monkeys and old cats, indicating a universal mechanism of degradation in cortical function that accompanies old age in different mammalian species.

[1]  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.

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

[3]  F. Reinoso-suárez,et al.  Stability of the neuronal population of the dorsal lateral geniculate nucleus (LGNd) of aged rats , 1985, Brain Research.

[4]  F. Amenta,et al.  Neurotransmitters, neuroreceptors and aging , 1991, Mechanisms of Ageing and Development.

[5]  J. Marquié,et al.  Age differences in sensitivity, response bias, and reaction time on a visual discrimination task. , 1992, Experimental aging research.

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

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

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

[9]  M. Diamond,et al.  A golgi study of dendritic morphology in the occipital cortex of socially reared aged rats , 1981, Experimental Neurology.

[10]  S. Kojima,et al.  Object discrimination learning in aged Japanese monkeys. , 2001, Behavioral neuroscience.

[11]  J. Buchwald,et al.  Aging changes in the cat P300 mimic the human. , 1985, Electroencephalography and clinical neurophysiology.

[12]  D. Flood Region-specific stability of dendritic extent in normal human aging and regression in Alzheimer's disease. II. Subiculum , 1991, Brain Research.

[13]  D. Burr,et al.  Visual Ageing: Unspecific Decline of the Responses to Luminance and Colour , 1996, Vision Research.

[14]  Rita Y. Emmerson,et al.  Life Span Changes in Electrophysiological Measures of Inhibition , 1996, Brain and Cognition.

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

[16]  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.

[17]  Alan Peters,et al.  Effects of aging on myelinated nerve fibers in monkey primary visual cortex , 2000, The Journal of comparative neurology.

[18]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[19]  William Schiff,et al.  Aging persons' estimates of vehicular motion. , 1992 .

[20]  N. A. Buchwald,et al.  Quantitative morphology of medium-sized caudate spiny neurons in aged cats , 1986, Neurobiology of Aging.

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

[22]  M. Lidow,et al.  Adrenergic and serotonergic receptors in aged monkey neocortex , 1995, Neurobiology of Aging.

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

[24]  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.

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

[26]  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.

[27]  J. Cerella,et al.  Radial localization in the aged. , 1987, Psychology and aging.

[28]  V. Gribkoff,et al.  Reduced bicuculline response and GABAA agonist binding in aged rat hippocampus , 1994, Neurobiology of Aging.

[29]  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.

[30]  F. Jia,et al.  Short-term depression of synaptic transmission from rat lateral geniculate nucleus to primary visual cortex in vivo , 2004, Brain Research.

[31]  M. Voytko Impairments in acquisition and reversals of two-choice discriminations by aged rhesus monkeys , 1999, Neurobiology of Aging.

[32]  T. Stuve,et al.  Motion perception and aging. , 1992, Psychology and aging.

[33]  Mitsuo Nagamachi,et al.  Age-related decline in color perception and difficulties with daily activities–measurement, questionnaire, optical and computer-graphics simulation studies , 2001 .

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

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

[36]  R A Weale,et al.  Senile changes in visual acuity. , 1975, Transactions of the ophthalmological societies of the United Kingdom.

[37]  C. Owsley,et al.  Contrast sensitivity, acuity, and the perception of 'real-world' targets. , 1987, The British journal of ophthalmology.

[38]  W C Dement,et al.  Sleep-wakefulness patterns in the aged cat. , 1984, Electroencephalography and clinical neurophysiology.

[39]  W. Dement,et al.  Electroencephalogram during sleep in the cat: age effects on slow-wave activity. , 1984, Sleep.

[40]  C. Tanaka,et al.  Regulation of GABA release via NMDA and 5-HT1A receptors in guinea pig dentate gyrus , 1996, Brain Research.

[41]  J. Werner,et al.  Senescent changes in scotopic contrast sensitivity , 1999, Vision Research.

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

[43]  M. Mishkin,et al.  Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction , 1991, Neurobiology of Aging.

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

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

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

[47]  R. Sekuler,et al.  Aging and low-contrast vision: face perception. , 1981, Investigative ophthalmology & visual science.

[48]  B. Pakkenberg,et al.  Neocortical neuron number in humans: Effect of sex and age , 1997, The Journal of comparative neurology.

[49]  R. Killiany,et al.  Effects of age on the thickness of myelin sheaths in monkey primary visual cortex , 2001, The Journal of comparative neurology.

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

[51]  P. D. Spear,et al.  Effects of aging on the densities, numbers, and sizes of retinal ganglion cells in rhesus monkey , 1996, Neurobiology of Aging.

[52]  J. Bartlett,et al.  Familiarity and recognition of faces in old age , 1991, Memory & cognition.

[53]  Fujiko Ando,et al.  Age-related change in contrast sensitivity among Japanese adults. , 2003, Japanese journal of ophthalmology.

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

[55]  A. Bron,et al.  Effect of age on contrast sensitivity function: uniocular and binocular findings. , 1985, The British journal of ophthalmology.

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

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

[58]  W. Levick,et al.  Analysis of orientation bias in cat retina , 1982, The Journal of physiology.

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

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

[61]  Kenneth R. Brizzee,et al.  Neuron numbers and dendritic extent in normal aging and alzheimer's disease , 1987, Neurobiology of Aging.

[62]  P. D. Spear,et al.  Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons , 1993, The Journal of comparative neurology.

[63]  Jocelyn Faubert,et al.  Aging and bilateral symmetry detection. , 2002, The journals of gerontology. Series B, Psychological sciences and social sciences.

[64]  A. Gutiérrez,et al.  GABAA receptor subunit expression changes in the rat cerebellum and cerebral cortex during aging. , 1997, Brain research. Molecular brain research.

[65]  Frances S. Chance,et al.  Synaptic Depression and the Temporal Response Characteristics of V1 Cells , 1998, The Journal of Neuroscience.

[66]  S. Feldon,et al.  Age-related deterioration of motion perception and detection , 1998, Graefe's Archive for Clinical and Experimental Ophthalmology.

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

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

[69]  I. Abrass,et al.  Alpha- and beta-adrenergic receptor function in the brain during senescence , 1988, Neurobiology of Aging.

[70]  Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). , 1990, Behavioral neuroscience.

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

[72]  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.

[73]  G. Trick,et al.  Visual sensitivity to motion , 1991, Neurology.

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

[75]  D. Flood,et al.  Region-specific stability of dendritic extent in normal human aging and regression in Alzheimer's disease. I. CA1 of hippocampus , 1991, Brain Research.

[76]  J. Culham,et al.  Aging Effects on Vernier Hyperacuity: a Function of Oscillation Rate but not Target Contrast , 2001, Optometry and vision science : official publication of the American Academy of Optometry.

[77]  W. Meier-Ruge,et al.  Quantitative morphology of synaptic plasticity in the aging brain. , 1988, Scanning microscopy.

[78]  Burkhart Fischer,et al.  Age effects in dynamic vision based on orientation identification , 2002, Experimental Brain Research.

[79]  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.

[80]  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.

[81]  C. Cepeda,et al.  Aging reduces neostriatal responsiveness toN-methyl-d-aspartate and dopamine: anIn vitro electrophysiological study , 1996, Neuroscience.

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

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

[84]  J. Morrison,et al.  Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. , 2003, Cerebral cortex.

[85]  B. Munoz,et al.  Association of Visual Field Loss and Mobility Performance in Older Adults: Salisbury Eye Evaluation Study , 2004, Optometry and vision science : official publication of the American Academy of Optometry.

[86]  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.

[87]  David Whitaker,et al.  Neural contribution to spatiotemporal contrast sensitivity decline in healthy ageing eyes , 1990, Vision Research.

[88]  S J Anderson,et al.  Effects of glaucoma and aging on photopic and scotopic motion perception. , 2000, Investigative ophthalmology & visual science.