Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

Abstract

Vasopressin (VP) and oxytocin (OT) are involved in modulating basic physiology and numerous social behaviors. Although the anatomical distributions of nonapeptide neurons throughout development have been described, the functional roles of VP and OT neurons during development are surprisingly understudied, and it is unknown whether they exhibit functional changes throughout early development. We utilized an acute social isolation paradigm to determine if VP and OT neural responses in eight nonapeptide cell groups differ at three different stages of early development in prairie voles. We tested pups at ages that are representative of the three rapid growth stages of the developing brain: postnatal day (PND)2 (closed eyes; poor locomotion), PND9 (eye opening; locomotion; peak brain growth spurt), and PND21 (weaning). Neural responses were examined in pups that (1) were under normal family conditions with their parents and siblings, (2) were isolated from their parents and siblings and then reunited, and (3) were isolated from their parents and siblings. We found that VP and OT neural activity (as assessed via Fos co-localization) did not differ in response to social condition across development. However, remarkably rapid VP and OT synthesis in response to social isolation was observed only in the paraventricular nucleus of the hypothalamus (PVN) and only in PND9 pups. These results suggest that PVN nonapeptide neurons exhibit distinct cellular properties during a critical period of development, allowing nonapeptide neurons to rapidly upregulate peptide production in response to stressors on a much shorter timescale than has been observed in adult animals.

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Acknowledgements

We are grateful for statistical help from the Statistics Consulting Center at Cornell University, to Chang Kim for assistance with PCR, and to Jeanne Powell for assistance with cell counts.

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Correspondence to Aubrey M. Kelly.

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The authors acknowledge the support from the National Institutes of Health (Eunice Kennedy Shriver National Institute of Child Health and Human Development HD081959 to AMK and HD079573 to AGO). The authors declare no competing financial interests and no conflicts of interest

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures were approved by and were in compliance with the Institutional Animal Care and Use Committee of Cornell University (2013-0102).

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Kelly, A.M., Hiura, L.C. & Ophir, A.G. Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus. Brain Struct Funct 223, 2547–2560 (2018). https://doi.org/10.1007/s00429-018-1640-2

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Keywords

  • Development
  • Vasopressin
  • Oxytocin
  • Critical period
  • Prairie vole
  • PVN