Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats
Rationale : Variations in maternal care in the rat associate with robust differences in hippocampal synaptic plasticity and learning in the offspring. In addition, differences in stress reactivity associate with variations in maternal care. However, the potential influence of stress on hippocampal f...
| Main Author: | |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2012-09-01
|
| Series: | European Journal of Psychotraumatology |
| Subjects: |
| _version_ | 1818256141209042944 |
|---|---|
| author | Rosemary C. Bagot |
| author_facet | Rosemary C. Bagot |
| author_sort | Rosemary C. Bagot |
| collection | DOAJ |
| description | Rationale : Variations in maternal care in the rat associate with robust differences in hippocampal synaptic plasticity and learning in the offspring. In addition, differences in stress reactivity associate with variations in maternal care. However, the potential influence of stress on hippocampal function is often overlooked in studies of effects of early life experience. Previously, we found differential modulation of hippocampal function and plasticity by stress in adult offspring exposed to varying levels of maternal care. N-methyl-D-aspartate receptors (NMDAR) regulate synaptic plasticity, and NMDAR function is modulated by stress and CORT. We hypothesised that altered NMDAR function underlies the interaction of maternal and stress effects on hippocampal synaptic plasticity. Methods : We used electrophysiology to examine NMDAR-dependent LTP and NMDAR synaptic function in adult offspring of mothers that varied in the frequency of pup licking/grooming (LG), i.e., High or Low LG. Results : Under basal conditions, long-term potentiation (LTP) was impaired in the hippocampal dentate gyrus of Low LG offspring relative to High LG offspring. Synaptic NMDAR function was enhanced in Low LG offspring with no change in α-amino-3-hydroxy-methyl-4-isoxazole propionic acid receptor function (AMPAR). NMDAR antagonism by low concentration APV rescued the basal LTP deficit in Low LG offspring and inhibited LTP in High LG offspring. Stress-level CORT (100nM) rapidly enhanced LTP in offspring of Low LG rats and impaired LTP in offspring of High LG rats. CORT robustly increased NMDAR function in High LG offspring, eliminating the maternal effect. CORT did not affect NMDAR function in Low LG offspring. Thus, Low LG offspring exhibit basally elevated NMDAR function coupled with insensitivity to CORT modulation indicative of a chronic alteration of NMDAR. Conclusion : These results suggest that low maternal care exerts a lasting effect on hippocampal plasticity through enhanced function of NMDAR in synapses. The blunted effect of CORT on synaptic NMDAR in Low LG rats could be adaptive in promoting cognitive functioning in challenging conditions, such as the improved contextual fear conditioning previously observed in these rats. |
| first_indexed | 2024-12-12T17:23:02Z |
| format | Article |
| id | doaj.art-f712cabfb5014f13b3ea625e0b9fb986 |
| institution | Directory Open Access Journal |
| issn | 2000-8066 |
| language | English |
| last_indexed | 2024-12-12T17:23:02Z |
| publishDate | 2012-09-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | European Journal of Psychotraumatology |
| spelling | doaj.art-f712cabfb5014f13b3ea625e0b9fb9862022-12-22T00:17:36ZengTaylor & Francis GroupEuropean Journal of Psychotraumatology2000-80662012-09-01301110.3402/ejpt.v3i0.19459Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult ratsRosemary C. BagotRationale : Variations in maternal care in the rat associate with robust differences in hippocampal synaptic plasticity and learning in the offspring. In addition, differences in stress reactivity associate with variations in maternal care. However, the potential influence of stress on hippocampal function is often overlooked in studies of effects of early life experience. Previously, we found differential modulation of hippocampal function and plasticity by stress in adult offspring exposed to varying levels of maternal care. N-methyl-D-aspartate receptors (NMDAR) regulate synaptic plasticity, and NMDAR function is modulated by stress and CORT. We hypothesised that altered NMDAR function underlies the interaction of maternal and stress effects on hippocampal synaptic plasticity. Methods : We used electrophysiology to examine NMDAR-dependent LTP and NMDAR synaptic function in adult offspring of mothers that varied in the frequency of pup licking/grooming (LG), i.e., High or Low LG. Results : Under basal conditions, long-term potentiation (LTP) was impaired in the hippocampal dentate gyrus of Low LG offspring relative to High LG offspring. Synaptic NMDAR function was enhanced in Low LG offspring with no change in α-amino-3-hydroxy-methyl-4-isoxazole propionic acid receptor function (AMPAR). NMDAR antagonism by low concentration APV rescued the basal LTP deficit in Low LG offspring and inhibited LTP in High LG offspring. Stress-level CORT (100nM) rapidly enhanced LTP in offspring of Low LG rats and impaired LTP in offspring of High LG rats. CORT robustly increased NMDAR function in High LG offspring, eliminating the maternal effect. CORT did not affect NMDAR function in Low LG offspring. Thus, Low LG offspring exhibit basally elevated NMDAR function coupled with insensitivity to CORT modulation indicative of a chronic alteration of NMDAR. Conclusion : These results suggest that low maternal care exerts a lasting effect on hippocampal plasticity through enhanced function of NMDAR in synapses. The blunted effect of CORT on synaptic NMDAR in Low LG rats could be adaptive in promoting cognitive functioning in challenging conditions, such as the improved contextual fear conditioning previously observed in these rats.maternal careglucocorticoid regulation synaptic plasticity |
| spellingShingle | Rosemary C. Bagot Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats European Journal of Psychotraumatology maternal care glucocorticoid regulation synaptic plasticity |
| title | Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats |
| title_full | Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats |
| title_fullStr | Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats |
| title_full_unstemmed | Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats |
| title_short | Natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats |
| title_sort | natural variations in maternal care determine sensitivity to glucocorticoid regulation of hippocampal synaptic plasticity and function in adult rats |
| topic | maternal care glucocorticoid regulation synaptic plasticity |
| work_keys_str_mv | AT rosemarycbagot naturalvariationsinmaternalcaredeterminesensitivitytoglucocorticoidregulationofhippocampalsynapticplasticityandfunctioninadultrats |