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The Journal of Neuroscience, March 1, 2006, 26(9):2434-2442; doi:10.1523/JNEUROSCI.4080-05.2006

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Development/Plasticity/Repair
Neuroplasticity of the Hypothalamic–Pituitary–Adrenal Axis Early in Life Requires Recurrent Recruitment of Stress-Regulating Brain Regions

Kristina A. Fenoglio,¹ Yuncai Chen,² and Tallie Z. Baram^1,2

¹Departments of Anatomy/Neurobiology and ²Pediatrics, University of California at Irvine, Irvine, California 92697-4475

Correspondence should be addressed to Dr. Tallie Z. Baram, Medical Sciences I, Zot 4475, University of California at Irvine, Irvine, CA 92697-4475. Email: tallie{at}uci.edu

An eloquent example of experience-induced neuroplasticity involves the enduring effects of daily "handling" of rat pups on the expression of genes regulating hormonal and behavioral responses to stress. Handling-evoked augmentation of maternal care of pups induces long-lasting reduction of hypothalamic corticotropin releasing hormone (CRH) expression and upregulates hippocampal glucocorticoid receptor levels. These changes promote a lifelong attenuation of hormonal stress responses. We have found previously that handling-evoked downregulation of CRH expression occurs already by postnatal day 9, implicating it as an early step in this experience-induced neuroplasticity. Here, we investigated the neuronal pathways and cellular mechanisms involved. CRH mRNA expression in hypothalamic paraventricular nucleus (PVN) diminished after daily handling but not after handling once only, indicating that "recurrent" handling was required for this effect. Return of handled pups to their cage provoked a burst of nurturing behavior in dams that, in turn, induced transient, coordinate Fos expression in selected regions of the pups’ brains. These included central nucleus of the amygdala (ACe) and bed nucleus of the stria terminals (BnST), regions that are afferent to PVN and influence CRH expression there. Whereas handling once sufficed to evoke Fos expression within ACe and BnST, expression in thalamic paraventricular nucleus, a region involved in storing and processing stress-related experience, required recurrent handling. Fos induction in all three regions elicited reduced transcription factor phosphorylation, followed by attenuated activation of CRH gene transcription within the PVN. These studies provide a neurobiological foundation for the profound neuroplasticity of stress-related genes evoked by early-life experience.

Key words: corticotropin releasing hormone; stress; handling; maternal care; thalamic paraventricular nucleus; amygdala

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Received Sept. 26, 2005; revised Jan. 18, 2006; accepted Jan. 21, 2006.

Correspondence should be addressed to Dr. Tallie Z. Baram, Medical Sciences I, Zot 4475, University of California at Irvine, Irvine, CA 92697-4475. Email: tallie{at}uci.edu

Related articles in J. Neurosci.:

Is Neuroplasticity of the Hypothalamic–Pituitary–Adrenal Axis Maternally Mediated?

Bethany C. Reeb and Katherine G. Akers
J. Neurosci. 2006 26: 5589-5590. [Full Text]  

This article has been cited by other articles:

				Y. Chen, C. M. Dube, C. J. Rice, and T. Z. Baram Rapid Loss of Dendritic Spines after Stress Involves Derangement of Spine Dynamics by Corticotropin-Releasing Hormone J. Neurosci., March 12, 2008; 28(11): 2903 - 2911. [Abstract] [Full Text] [PDF]

				B. C. Reeb and K. G. Akers Is Neuroplasticity of the Hypothalamic-Pituitary-Adrenal Axis Maternally Mediated? J. Neurosci., May 24, 2006; 26(21): 5589 - 5590. [Full Text] [PDF]

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