Programming effects of peripubertal stress on spatial learning
Exposure to adversity during early life can have profound influences on brain function and behavior later in life. The peripubertal period is emerging as an important time-window of susceptibility to stress, with substantial evidence documenting long-term consequences in the emotional and social dom...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2020-11-01
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| Series: | Neurobiology of Stress |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2352289520300722 |
| _version_ | 1819055379088146432 |
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| author | S. Tzanoulinou E. Gantelet C. Sandi C. Márquez |
| author_facet | S. Tzanoulinou E. Gantelet C. Sandi C. Márquez |
| author_sort | S. Tzanoulinou |
| collection | DOAJ |
| description | Exposure to adversity during early life can have profound influences on brain function and behavior later in life. The peripubertal period is emerging as an important time-window of susceptibility to stress, with substantial evidence documenting long-term consequences in the emotional and social domains. However, little is known about how stress during this period impacts subsequent cognitive functioning. Here, we assessed potential long-term effects of peripubertal stress on spatial learning and memory using the water maze task. In addition, we interrogated whether individual differences in stress-induced behavioral and endocrine changes are related to the degree of adaptation of the corticosterone response to repeated stressor exposure during the peripubertal period. We found that, when tested at adulthood, peripubertally stressed animals displayed a slower learning rate. Strikingly, the level of spatial orientation in the water maze completed on the last training day was predicted by the degree of adaptation of the recovery -and not the peak-of the corticosterone response to stressor exposure (i.e., plasma levels at 60 min post-stressor) across the peripubertal stress period. In addition, peripubertal stress led to changes in emotional and glucocorticoid reactivity to novelty exposure, as well as in the expression levels of the plasticity molecule PSA-NCAM in the hippocampus. Importantly, by assessing the same endpoints in another peripubertally stressed cohort tested during adolescence, we show that the observed effects at adulthood are the result of a delayed programming manifested at adulthood and not protracted effects of stress. Altogether, our results support the view that the degree of stress-induced adaptation of the hypothalamus-pituitary-adrenal axis responsiveness at the important transitional period of puberty relates to the long-term programming of cognition, behavior and endocrine reactivity. |
| first_indexed | 2024-12-21T13:06:35Z |
| format | Article |
| id | doaj.art-2b6e4b22788447e283dcfef2c40c4afb |
| institution | Directory Open Access Journal |
| issn | 2352-2895 |
| language | English |
| last_indexed | 2024-12-21T13:06:35Z |
| publishDate | 2020-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Stress |
| spelling | doaj.art-2b6e4b22788447e283dcfef2c40c4afb2022-12-21T19:03:00ZengElsevierNeurobiology of Stress2352-28952020-11-0113100282Programming effects of peripubertal stress on spatial learningS. Tzanoulinou0E. Gantelet1C. Sandi2C. Márquez3Laboratory of Behavioral Genetics, Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandLaboratory of Behavioral Genetics, Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandLaboratory of Behavioral Genetics, Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandLaboratory of Neural Circuits of Social Behavior, Instituto de Neurociencias (Universidad Miguel Hernández-Consejo Superior de Investigaciones Científicas), San Juan de Alicante, Spain; Corresponding author.Exposure to adversity during early life can have profound influences on brain function and behavior later in life. The peripubertal period is emerging as an important time-window of susceptibility to stress, with substantial evidence documenting long-term consequences in the emotional and social domains. However, little is known about how stress during this period impacts subsequent cognitive functioning. Here, we assessed potential long-term effects of peripubertal stress on spatial learning and memory using the water maze task. In addition, we interrogated whether individual differences in stress-induced behavioral and endocrine changes are related to the degree of adaptation of the corticosterone response to repeated stressor exposure during the peripubertal period. We found that, when tested at adulthood, peripubertally stressed animals displayed a slower learning rate. Strikingly, the level of spatial orientation in the water maze completed on the last training day was predicted by the degree of adaptation of the recovery -and not the peak-of the corticosterone response to stressor exposure (i.e., plasma levels at 60 min post-stressor) across the peripubertal stress period. In addition, peripubertal stress led to changes in emotional and glucocorticoid reactivity to novelty exposure, as well as in the expression levels of the plasticity molecule PSA-NCAM in the hippocampus. Importantly, by assessing the same endpoints in another peripubertally stressed cohort tested during adolescence, we show that the observed effects at adulthood are the result of a delayed programming manifested at adulthood and not protracted effects of stress. Altogether, our results support the view that the degree of stress-induced adaptation of the hypothalamus-pituitary-adrenal axis responsiveness at the important transitional period of puberty relates to the long-term programming of cognition, behavior and endocrine reactivity.http://www.sciencedirect.com/science/article/pii/S2352289520300722StressPeripubertal stressWater mazePSA-NCAMDentate gyrusCorticosterone |
| spellingShingle | S. Tzanoulinou E. Gantelet C. Sandi C. Márquez Programming effects of peripubertal stress on spatial learning Neurobiology of Stress Stress Peripubertal stress Water maze PSA-NCAM Dentate gyrus Corticosterone |
| title | Programming effects of peripubertal stress on spatial learning |
| title_full | Programming effects of peripubertal stress on spatial learning |
| title_fullStr | Programming effects of peripubertal stress on spatial learning |
| title_full_unstemmed | Programming effects of peripubertal stress on spatial learning |
| title_short | Programming effects of peripubertal stress on spatial learning |
| title_sort | programming effects of peripubertal stress on spatial learning |
| topic | Stress Peripubertal stress Water maze PSA-NCAM Dentate gyrus Corticosterone |
| url | http://www.sciencedirect.com/science/article/pii/S2352289520300722 |
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