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Articles, Systems/Circuits

Chronic Stress-Induced Alterations of Dendritic Spine Subtypes Predict Functional Decrements in an Hypothalamo–Pituitary–Adrenal-Inhibitory Prefrontal Circuit

Jason J. Radley, Rachel M. Anderson, Bradley A. Hamilton, Jennifer A. Alcock and Sara A. Romig-Martin
Journal of Neuroscience 4 September 2013, 33 (36) 14379-14391; DOI: https://doi.org/10.1523/JNEUROSCI.0287-13.2013
Jason J. Radley
Psychology Department and Neuroscience Program, University of Iowa, Iowa City, Iowa 52242
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Rachel M. Anderson
Psychology Department and Neuroscience Program, University of Iowa, Iowa City, Iowa 52242
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Bradley A. Hamilton
Psychology Department and Neuroscience Program, University of Iowa, Iowa City, Iowa 52242
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Jennifer A. Alcock
Psychology Department and Neuroscience Program, University of Iowa, Iowa City, Iowa 52242
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Sara A. Romig-Martin
Psychology Department and Neuroscience Program, University of Iowa, Iowa City, Iowa 52242
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Abstract

Activation of the hypothalamo–pituitary–adrenal (HPA) axis plays a vital role in promoting adaptation during acute stress, but adverse effects of chronic stress may result from overactivity of this system. Recent evidence highlights a subdivision of GABAergic neurons within anterior bed nuclei of the stria terminalis (aBST) that integrates and relays inhibitory influences to HPA-effector neurons in paraventricular hypothalamus during acute stress, notably from medial prefrontal [prelimbic (PL)] and hippocampal [ventral subiculum (vSUB)] cortical fields. Here we localize the site and candidate mechanism of neuroplasticity within upstream regions of this inhibitory network after chronic variable stress (CVS). Rats bearing retrograde tracer injections in aBST underwent CVS for 14 d. Retrogradely labeled and unlabeled neurons in vSUB and PL were selected for intracellular dye filling, followed by three-dimensional imaging and analysis of dendritic arborization and spine morphometry. Whereas PL neurons displayed decreases in dendritic branching and spine density after CVS, aBST-projecting cells showed a selective loss of mature mushroom-shaped spines. In a follow-up experiment, CVS-treated and control rats were exposed to a novel restraint challenge for assay of HPA activation and engagement of aBST-projecting cortical regions. CVS animals showed enhanced HPA output and decreased Fos activation in aBST-projecting PL neurons compared with acutely stressed controls. In contrast, vSUB failed to show any significant differences in structural plasticity or functional activation patterns after CVS. These findings define a mechanism whereby synaptic destabilization in the PL → aBST pathway may dampen its ability to impart inhibitory control over the HPA axis after chronic stress exposure.

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The Journal of Neuroscience: 33 (36)
Journal of Neuroscience
Vol. 33, Issue 36
4 Sep 2013
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Chronic Stress-Induced Alterations of Dendritic Spine Subtypes Predict Functional Decrements in an Hypothalamo–Pituitary–Adrenal-Inhibitory Prefrontal Circuit
Jason J. Radley, Rachel M. Anderson, Bradley A. Hamilton, Jennifer A. Alcock, Sara A. Romig-Martin
Journal of Neuroscience 4 September 2013, 33 (36) 14379-14391; DOI: 10.1523/JNEUROSCI.0287-13.2013

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Chronic Stress-Induced Alterations of Dendritic Spine Subtypes Predict Functional Decrements in an Hypothalamo–Pituitary–Adrenal-Inhibitory Prefrontal Circuit
Jason J. Radley, Rachel M. Anderson, Bradley A. Hamilton, Jennifer A. Alcock, Sara A. Romig-Martin
Journal of Neuroscience 4 September 2013, 33 (36) 14379-14391; DOI: 10.1523/JNEUROSCI.0287-13.2013
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