Long term effects of peripubertal stress on the thalamic reticular nucleus of female and male mice

Adverse experiences during infancy and adolescence have an important and enduring effect on the brain and are predisposing factors for mental disorders, particularly major depression. This impact is particularly notable in regions with protracted development, such as the prefrontal cortex. The inhibitory neurons of this cortical region are altered by peripubertal stress (PPS), particularly in female mice. In this study we have explored whether the inhibitory circuits of the thalamus are impacted by PPS in male and female mice. This diencephalic structure, as the prefrontal cortex, also completes its development during postnatal life and is affected by adverse experiences. The long-term changes induced by PPS were exclusively found in adult female mice. We have found that PPS increases depressive-like behavior and induces changes in parvalbumin-expressing (PV+) cells of the thalamic reticular nucleus (TRN). We observed reductions in the volume of the TRN, together with those of parameters related to structures/molecules that regulate the plasticity and connectivity of PV+ cells: perineuronal nets, matricellular structures surrounding PV+ neurons, and the polysialylated form of the neural cell adhesion molecule (PSA-NCAM). The expression of the GluN1, but not of GluN2C, NMDA receptor subunit was augmented in the TRN after PPS. An increase in the fluorescence intensity of PV+ puncta was also observed in the synaptic output of TRN neurons in the lateral posterior thalamic nucleus. These results demonstrate that the inhibitory circuits of the thalamus, as those of the prefrontal cortex, are vulnerable to the effects of aversive experiences during early life, particularly in females. This vulnerability is probably related to the protracted development of the TRN and might contribute to the development of psychiatric disorders.

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Publication Details

Journal
Neurobiology of Disease
Published
2024-08-22
DOI
https://doi.org/10.1016/j.nbd.2024.106642
Citations
3
Primary Topic
Neuroscience and Neuropharmacology Research
Type
article
Field-Weighted Citation Impact
0.80

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article

Long term effects of peripubertal stress on the thalamic reticular nucleus of female and male mice

Esther Castillo-Gómez, Marta Pérez-Rando, Carmen Sandi, Julia Alcaide et al.
3 citations
Neurobiology of Disease
Neuroscience and Neuropharmacology Research
0.80
article

Long term effects of peripubertal stress on the thalamic reticular nucleus of female and male mice

Esther Castillo-Gómez, Marta Pérez-Rando, Carmen Sandi, Julia Alcaide, Carlos Crespo, Clara Bueno-Fernández, Yaiza Gramuntell, Juan Nácher, Patrycja Klimczak, Erica Garcia-Verellen, Chiara Guicciardini
article en
3 citations

Abstract

Adverse experiences during infancy and adolescence have an important and enduring effect on the brain and are predisposing factors for mental disorders, particularly major depression. This impact is particularly notable in regions with protracted development, such as the prefrontal cortex. The inhibitory neurons of this cortical region are altered by peripubertal stress (PPS), particularly in female mice. In this study we have explored whether the inhibitory circuits of the thalamus are impacted by PPS in male and female mice. This diencephalic structure, as the prefrontal cortex, also completes its development during postnatal life and is affected by adverse experiences. The long-term changes induced by PPS were exclusively found in adult female mice. We have found that PPS increases depressive-like behavior and induces changes in parvalbumin-expressing (PV+) cells of the thalamic reticular nucleus (TRN). We observed reductions in the volume of the TRN, together with those of parameters related to structures/molecules that regulate the plasticity and connectivity of PV+ cells: perineuronal nets, matricellular structures surrounding PV+ neurons, and the polysialylated form of the neural cell adhesion molecule (PSA-NCAM). The expression of the GluN1, but not of GluN2C, NMDA receptor subunit was augmented in the TRN after PPS. An increase in the fluorescence intensity of PV+ puncta was also observed in the synaptic output of TRN neurons in the lateral posterior thalamic nucleus. These results demonstrate that the inhibitory circuits of the thalamus, as those of the prefrontal cortex, are vulnerable to the effects of aversive experiences during early life, particularly in females. This vulnerability is probably related to the protracted development of the TRN and might contribute to the development of psychiatric disorders.

Neurobiology of DiseaseVol. 200
Universitat de València (ES), École Polytechnique Fédérale de Lausanne (CH)
National Science Foundation, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, Generalitat Valenciana, Ministerio de Ciencia e Innovación, Agencia Estatal de Investigación, Conselleria de Cultura, Educación y Ciencia, Generalitat Valenciana
Gender equality
Openalex Percentile: Top 30%
Neuroscience and Neuropharmacology Research
0.80
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