Elsevier

Brain Research

Volume 1274, 5 June 2009, Pages 21-27
Brain Research

Research Report
Aging affects response variability of V1 and MT neurons in rhesus monkeys

https://doi.org/10.1016/j.brainres.2009.04.015Get rights and content

Abstract

Visual function declines with age. Much of the decline may result from functional degradation in central visual areas. To investigate the physiological mechanisms underlying visual function declines during normal aging, we compared the response variability of cells in primary visual cortex (V1) and middle temporal visual area (MT) in young adult and very old macaque monkeys using single-neuron in vivo electrophysiology. We found that mean response and response variability in both V1 and MT of old monkeys are significantly higher than in young monkeys. And response-to-noise ratio in old monkeys is significantly lower than in young ones. The results are consistent with an age-related degradation of inhibitory intracortical circuits. The neural changes described here could contribute to declines in visual function during senescence.

Introduction

Human visual abilities decline with age. Psychological experiments have shown that aged humans exhibit decreased acuity, contrast sensitivity, binocular summation and symmetry perception (Faubert, 2002, Sekuler and Sekuler, 2000, Spear, 1993). Senescent humans are also less efficient at tasks requiring orientation discrimination and/or motion percept (Bennett, 2007, Betts, 2007, Norman, 2003, Snowden and Kavanagh, 2006). Ocular decline in the elderly alone cannot account for all of the changes that occur with normal aging (Ball and Sekuler, 1986, Bennett, 1999, Herbert, 2002, Sekuler, 2000). Therefore, impaired visual performance in aged human must be, at least in part, due to degeneration and/or dysfunction in central visual areas.

In order to relate single cortical cell properties to discrimination behavior one needs to know two factors: the difference in the response to each different stimulus (signal) and the variability of the single cell responses (noise). If aging affects either of the factors, it could affect the performance of sensory neurons in a way that might contribute to or account for the deficiency we observed in elderly humans.

The effects of aging on the first factor, the signal, have been examined in several studies that have measured how aging affects the mean rate of firing elicited by a variety of stimuli. It has been shown that aging increases responsiveness to optimal and non-optimal stimuli disproportionally and reduces stimulus selectivities of single neurons in visual cortical areas (Hua, 2006, Leventhal, 2003, Liang et al., 2008, Schmolesky, 2000, Yang et al, 2008b, Yu, 2006).

However, the effects of aging on the second aspect of neuronal responses, the noise, have so far not been examined. The responses of cortical sensory neurons are extremely variable, with the number of spikes elicited by identical stimuli varying significantly from trial to trial (Nover, 2005, Snowden, 1992, Tolhurst, 1981Tolhurst, 1983, Vogels, 1989). This variability is most often interpreted as ‘noise’ and could be detrimental to the sensory system (Carandini, 2004, Machens, 2003, Sadeghi, 2007, Shadlen and Newsome, 1995, Stein, 2005). Theoretical studies have suggested that a high level of noise would limit the performance of neural encoding (Roddey, 2000, Sadeghi, 2007). Therefore, it is possible that aging affects the response variability of cortical neurons and in turn disturbs visual information processing.

To address this, we used extracellular single-neuron recording techniques to examine the response variability of V1 and MT cells in old rhesus monkeys. The results provide evidence for a significant degradation of function in areas V1 and MT of old monkeys.

Section snippets

Results

Variability of visually evoked responses was measured in a total of 79 V1 cells (23 units from young monkey 1, 27 from young monkey 2, and 29 from young monkey 3) and 93 MT cells (26 units from young monkey 1, 35 from young monkey 2, and 32 from young monkey 3) from three young monkeys and 71 V1 cells (22 units from old monkey 1, 18 from old monkey 2, 17 from old monkey 3 and 14 from old monkey 4) and 102 MT cells (19 units from old monkey 1, 28 from old monkey 2, 29 from old monkey 3 and 26

Discussion

In the present study, we examined how aging affects the trial-by-trial variability of visually evoked responses across macaque V1 and MT and found that, for both V1 and MT populations, spike count variability in old monkeys is significantly higher than in young monkeys. Further, response-to-noise ratio in old animals is significantly lower than in young ones.

In our previous studies, we have measured spontaneous activity as noise and found increased spontaneous activity in old animals (Hua, 2006

Animal preparation and electrophysiology

All experimental followed protocols were consistent with the Society for Neuroscience and National Institute of Health guidelines for the humane use and care of animals. The experiments described here were approved by the University of Utah Institutional Animal Care and Use Committee.

Subjects for this study were two groups of rhesus monkeys (Macaca mulatta). Young adult monkeys (n = 3, male) were 5–9 years old and weighed 3.6–6.2 kg. Old monkeys (n = 4, male) were 23–31 years old and weighed

Acknowledgments

This work was supported by grants from the Natural Science Foundation of China (30520120072, Y.Z.), NIH/NIA R01 AG 17922 (A.G.L.), and National Basic Research Program of China (2005CB522800).

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