Anxiety-like behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress

Charlotte Laloux, Jérôme Mairesse, Gilles Van Camp, Angela Giovine, Igor Branchi, Sebastien Bouret, Sara Morley-Fletcher, Gabriela Bergonzelli, Marithé Malagodi, Roberto Gradini, Ferdinando Nicoletti, Muriel Darnaudéry, Stefania Maccari

Research output: Contribution to journalArticlepeer-review


Epidemiological studies suggest that emotional liability in infancy could be a predictor of anxiety-related disorders in the adulthood. Rats exposed to prenatal restraint stress (" PRS rats" ) represent a valuable model for the study of the interplay between environmental triggers and neurodevelopment in the pathogenesis of anxious/depressive like behaviours. Repeated episodes of restraint stress were delivered to female Sprague-Dawley rats during pregnancy and male offspring were studied. Ultrasonic vocalization (USV) was assessed in pups under different behavioural paradigms. After weaning, anxiety was measured by conventional tests. Expression of GABAA receptor subunits and metabotropic glutamate (mGlu) receptors was assessed by immunoblotting. Plasma leptin levels were measured using a LINCOplex bead assay kit. The offspring of stressed dams emitted more USVs in response to isolation from their mothers and showed a later suppression of USV production when exposed to an unfamiliar male odour, indicating a pronounced anxiety-like profile. Anxiety like behaviour in PRS pups persisted one day after weaning. PRS pups did not show the plasma peak in leptin levels that is otherwise seen at PND14. In addition, PRS pups showed a reduced expression of the γ2 subunit of GABAA receptors in the amygdala at PND14 and PND22, an increased expression of mGlu5 receptors in the amygdala at PND22, a reduced expression of mGlu5 receptors in the hippocampus at PND14 and PND22, and a reduced expression of mGlu2/3 receptors in the hippocampus at PND22. These data offer a clear-cut demonstration that the early programming triggered by PRS could be already translated into anxiety-like behaviour during early postnatal life.

Original languageEnglish
Pages (from-to)1646-1658
Number of pages13
Issue number10
Publication statusPublished - Oct 2012


  • Anxiety-like behaviour
  • Anxiety-related receptors
  • Infancy
  • Leptin
  • Prenatal restraint stress

ASJC Scopus subject areas

  • Endocrinology
  • Endocrinology, Diabetes and Metabolism
  • Psychiatry and Mental health
  • Biological Psychiatry
  • Endocrine and Autonomic Systems


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