Abstract

Aging is a progressive functional decline characterized by a gradual deterioration in physiological function and behavior. The most important age-related change in cognitive function is decline in cognitive performance (i.e., the processing or transformation of information to make decisions that includes speed of processing, working memory, and learning). The purpose of this study is to outline the changes in age-related cognitive performance (i.e., short-term recognition memory and long-term learning and memory) in long-lived Octodon degus. The strong similarity between degus and humans in social, metabolic, biochemical, and cognitive aspects makes it a unique animal model for exploring the mechanisms underlying the behavioral and cognitive deficits related to natural aging. In this study, we examined young adult female degus (12- and 24-months-old) and aged female degus (38-, 56-, and 75-months-old) that were exposed to a battery of cognitive-behavioral tests. Multivariate analyses of data from the Social Interaction test or Novel Object/Local Recognition (to measure short-term recognition memory), and the Barnes maze test (to measure long-term learning and memory) revealed a consistent pattern. Young animals formed a separate group of aged degus for both short- and long-term memories. The association between the first component of the principal component analysis (PCA) from short-term memory with the first component of the PCA from long-term memory showed a significant negative correlation. This suggests age-dependent differences in both memories, with the aged degus having higher values of long-term memory ability but poor short-term recognition memory, whereas in the young degus an opposite pattern was found. Approximately 5% of the young and 80% of the aged degus showed an impaired short-term recognition memory; whereas for long-term memory about 32% of the young degus and 57% of the aged degus showed decreased performance on the Barnes maze test. Throughout this study, we outlined age-dependent cognitive performance decline during natural aging in degus. Moreover, we also demonstrated that the use of a multivariate approach let us explore and visualize complex behavioral variables, and identified specific behavioral patterns that allowed us to make powerful conclusions that will facilitate further the study on the biology of aging. In addition, this study could help predict the onset of the aging process based on behavioral performance.

Highlights

  • From a lifespan perspective, aging is the progressive decline in physiological homeostasis and functional integrity, and is associated with a gradual reduction in the capacity of the brain to transmit signals and self-repair (Amarya et al, 2018; Singh et al, 2019)

  • The first component explained 58.3% of the total variance and was mainly loaded by the total distance traveled and speed, time spent in the central zone (0.77), time spent in the corners (−0.73), and the number of central crossings (0.52); whereas the second component explained 20.2% of the variance and was loaded by the time spent in the corners (0.55), time spent in the central zone (−0.5), total distance traveled, and speed

  • The one-way PERMANOVA test for the principal component analysis (PCA) of the Open Field test showed no significant differences between the aging groups (p > 0.05), suggesting that despite aging all the animals exhibited normal motor activity (Supplementary Figure 1; Supplementary Table 2 (SM))

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Summary

Introduction

From a lifespan perspective, aging is the progressive decline in physiological homeostasis and functional integrity, and is associated with a gradual reduction in the capacity of the brain to transmit signals and self-repair (Amarya et al, 2018; Singh et al, 2019). Cognitive capacities such as the speed of processing, working memory, and long-term memory tended to decline more slowly and to a slighter degree than physical abilities (Erickson and Barnes, 2003; Caserta et al, 2009; Park and Reuter-Lorenz, 2009; Amarya et al, 2018). Naturally old mammals (e.g., aged rodents, primates, and humans) showed spatial memory impairments compared with their younger counterparts (Barnes, 1979; Uttl and Graf, 1993; Rapp et al, 1997; Bach et al, 1999). Changes in memory with age do not occur linearly; instead, it can be variable between individuals, and not all kinds of memory are affected (Markowska et al, 1989; Rapp and Amaral, 1991, 1992; Erickson and Barnes, 2003; Rodefer and Baxter, 2007)

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