Chronic Stress During Adolescence Impairs and Improves Learning and Memory in Adulthood

Abstract

HIGHLIGHTS This study tested the effects of adolescent-stress on adult learning and memory.Adolescent-stressed rats had enhanced reversal learning compared to unstressed rats.Adolescent-stress exposure made working memory more vulnerable to disturbance.Adolescent-stress did not affect adult associative learning or reference memory.Exposure to acute stress can cause a myriad of cognitive impairments, but whether negative experiences continue to hinder individual as they age is not as well understood. We determined how chronic unpredictable stress during adolescence affects multiple learning and memory processes in adulthood. Using male Sprague Dawley rats, we measured learning (both associative and reversal) and memory (both reference and working) starting 110 days after completion of an adolescent-stress treatment. We found that adolescent-stress affected adult cognitive abilities in a context-dependent way. Compared to rats reared without stress, adolescent-stressed rats exhibited enhanced reversal learning, an indicator of behavioral flexibility, but showed no change in associative learning and reference memory abilities. Working memory, which in humans is thought to underpin reasoning, mathematical skills, and reading comprehension, may be enhanced by exposure to adolescent-stress. However, when adolescent-stressed animals were tested after a novel disturbance, they exhibited a 5-fold decrease in working memory performance while unstressed rats continued to exhibit a linear learning curve. These results emphasize the capacity for stress during adolescence to transform the cognitive abilities of adult animals, even after stress exposure has ceased and animals have resided in safe environments for the majority of their lifespans.

Transgenerational transmission of a stress-coping phenotype programmed by early-life stress in the Japanese quail

“…This is in agreement with previous studies in the Japanese quail and others species showing that the pre-natal period is a sensitive period to stress that could result in long-term impacts on the phenotype (human and rodents27845, guinea pig46, birds47, chicken4849, Japanese quail6142450, threespine stickleback1051, guppies52). However, in some other species post-natal experience does have a strong effect on individual phenotype (rat9155354, zebra finch445556575859). It seems that the main difference between the species that are more likely affected by pre-natal or by post-natal stress is the degree of development at birth.…”

“…However, early-life stress is likely to have both benefits and costs. Its potential adaptive outcome may depend on the context within which the phenotypic traits are measured, as well as the life-history stage, the environmental conditions and the generation1461516.…”

Effects of exercise on adolescent and adult hypothalamic and hippocampal neuroinflammation

“…They have different molecular strategies for responding to hippocampal injury (McPherson et al, ). They are highly sensitive to the long‐term effects of stress (Chaby et al, ; Wong and Marinelli, 2016), and, if maintained on a high fat diet, they have exacerbated emotional memory of negative events, while adults do not (Boitard et al, ). Encouragingly, it has also recently been demonstrated that exercise during adolescence can have a lasting positive effect.…”

Early life stress induces long-term changes in limbic areas of a teleost fish: the role of catecholamine systems in stress coping

“…Notably, unpredictable chronic stress during adolescence has been found to have a context dependent long-lasting effect on memory systems. Specifically, it appears that while rats subjected to unpredictable chronic stress showed an enhancement in working memory to the location of a reward at basal levels, this was completely hindered after exposure to a novel acute stressor 7 . Interestingly, all fish groups responded with an increase in bdnf expression to the acute stressor in the Dlv.…”