BMC Neuroscience | |
Regional differences in acute corticosterone-induced dendritic remodeling in the rat brain and their behavioral consequences | |
Shin Jung Kang2  Ki Soon Shin1  Seokheon Hong2  Kyuhyun Choi1  Jee Hyun Yi1  Hyejin Kim1  | |
[1] Department of Biology, Department of Life and Nanopharmaceutical Sciences, Kyung Hee University, 130-701 Seoul, Republic of Korea;Department of Molecular Biology, Sejong University, 143-747 Seoul, Republic of Korea | |
关键词: Anxiety; Working memory; Stress; Medial prefrontal cortex; Basolateral amygdala; Corticosterone; | |
Others : 799289 DOI : 10.1186/1471-2202-15-65 |
|
received in 2014-02-19, accepted in 2014-05-14, 发布年份 2014 | |
【 摘 要 】
Background
Glucocorticoid released by stressful stimuli elicits various stress responses. Acute treatment with a single dose of corticosterone (CORT; predominant glucocorticoid of rats) alone has previously been shown to trigger anxiety behavior and robust dendritic hypertrophy of neurons in the basolateral amygdala (BLA). Neurons in the medial prefrontal cortex (mPFC) are also known to be highly sensitive to stress and regulate anxiety-like behaviors. Nevertheless, we know less about acute CORT-induced structural changes of other brain regions and their behavioral outcomes. In addition, the temporal profile of acute CORT effects remains to be examined. The current study investigates time course changes of dendritic architectures in the stress vulnerable brain areas, the BLA and mPFC, and their behavioral consequences after acute treatment with a single dose of CORT.
Results
Acute CORT treatment produced delayed onset of dendritic remodeling in the opposite direction in the BLA and mPFC with different time courses. Acute CORT induced dendritic hypertrophy of BLA spiny neurons, which was paralleled by heightened anxiety, both peaked 12 days after the treatment. Meanwhile, CORT-induced dendritic atrophy of mPFC pyramidal neurons peaked on day 6, concomitantly with impaired working memory. Both changed dendritic morphologies and altered behavioral outcomes were fully recovered.
Conclusion
Our results suggest that stress-induced heightened anxiety appears to be a functional consequence of dendritic remodeling of BLA neurons but not that of mPFC. Instead, stress-induced dendritic atrophy of mPFC neurons is relevant to working memory deficit. Therefore, structural changes in the BLA and the mPFC might be specifically associated with distinct behavioral symptoms observed in stress-related mental disorders. Remarkably, stress-induced dendritic remodeling in the BLA as well as mPFC is readily reversible. The related behavioral outcomes also follow the similar time course in a reversible manner. Therefore, further studies on the cellular mechanism for the plasticity of dendrites architecture might provide new insight into the etiological factors for stress-related mental illness such as posttraumatic stress disorder (PTSD).
【 授权许可】
2014 Kim et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140707030641870.pdf | 902KB | download | |
Figure 5. | 32KB | Image | download |
Figure 4. | 60KB | Image | download |
Figure 3. | 35KB | Image | download |
Figure 2. | 57KB | Image | download |
Figure 1. | 38KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
【 参考文献 】
- [1]Tasker JG, Herman JP: Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic-pituitary-adrenal axis. Stress 2011, 14:398-406.
- [2]Smith SM, Vale WW: The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci 2006, 8:383-395.
- [3]McEwen BS: Stress and hippocampal plasticity. Annu Rev Neurosci 1999, 22:105-122.
- [4]Magarinos AM, McEwen BS: Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995, 69:89-98.
- [5]Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H: Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 2012, 39:112-119.
- [6]Akirav I: Cannabinoids and glucocorticoids modulate emotional memory after stress. Neurosci Biobehav Rev 2013, 37:2554-2563.
- [7]Timmermans W, Xiong H, Hoogenraad CC, Krugers HJ: Stress and excitatory synapses: from health to disease. Neuroscience 2013, 248:626-636.
- [8]de Quervain DJ, Aerni A, Schelling G, Roozendaal B: Glucocorticoids and the regulation of memory in health and disease. Front Neuroendocrinol 2009, 30:358-370.
- [9]Bush G, Luu P, Posner MI: Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 2000, 4:215-222.
- [10]Kern S, Oakes TR, Stone CK, McAuliff EM, Kirschbaum C, Davidson RJ: Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor. Psychoneuroendocrinology 2008, 33:517-529.
- [11]Moghaddam B, Jackson M: Effect of stress on prefrontal cortex function. Neurotox Res 2004, 6:73-78.
- [12]Cook SC, Wellman CL: Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 2004, 60:236-248.
- [13]Rauch SL, Shin LM, Segal E, Pitman RK, Carson MA, McMullin K, Whalen PJ, Makris N: Selectively reduced regional cortical volumes in post-traumatic stress disorder. Neuroreport 2003, 14:913-916.
- [14]Yamasue H, Kasai K, Iwanami A, Ohtani T, Yamada H, Abe O, Kuroki N, Fukuda R, Tochigi M, Furukawa S, Sadamatsu M, Sasaki T, Aoki S, Ohtomo K, Asukai N, Kato N: Voxel-based analysis of MRI reveals anterior cingulate gray-matter volume reduction in posttraumatic stress disorder due to terrorism. Proc Natl Acad Sci U S A 2003, 100:9039-9043.
- [15]Diorio D, Viau V, Meaney MJ: The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 1993, 13:3839-3847.
- [16]Wellman CL: Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 2001, 49:245-253.
- [17]Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S: Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci U S A 2005, 102:9371-9376.
- [18]Vyas A, Mitra R, Shankaranarayana RBS, Chattarji S: Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 2002, 22:6810-6818.
- [19]Vyas A, Chattarji S: Modulation of different states of anxiety-like behavior by chronic stress. Behav Neurosci 2004, 118:1450-1454.
- [20]Mitra R, Sapolsky RM: Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc Natl Acad Sci U S A 2008, 105:5573-5578.
- [21]American Psychiatric Association: Diagnostic and Statistical Mental Disorders: DSM-IV-TR. Washington, DC: American Psychiatric Publishing; 2000.
- [22]Yehuda R: Post-traumatic stress disorder. N Engl J Med 2002, 346:108-114.
- [23]Yehuda R, LeDoux J: Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 2007, 56(1):19-32.
- [24]Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB: Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 1995, 52:1048-1060.
- [25]Breslau N, Reboussin BA, Anthony JC, Storr CL: The structure of posttraumatic stress disorder: latent class analysis in 2 community samples. Arch Gen Psychiatry 2005, 62:1343-1351.
- [26]Breslau N, Peterson EL, Poisson LM, Schultz LR, Lucia VC: Estimating post-traumatic stress disorder in the community: lifetime perspective and the impact of typical traumatic events. Psychol Med 2004, 34:889-898.
- [27]McFarlane AC: Posttraumatic stress disorder: a model of the longitudinal course and the role of risk factors. J Clin Psychiatry 2000, 61(Suppl 5):15-20. discussion 21–13
- [28]Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH: Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004, 125:1-6.
- [29]Radley JJ, Rocher AB, Miller M, Janssen WG, Liston C, Hof PR, McEwen BS, Morrison JH: Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 2006, 16:313-320.
- [30]Quirk GJ, Beer JS: Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr Opin Neurobiol 2006, 16:723-727.
- [31]Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS: Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 2006, 26:7870-7874.
- [32]Cerqueira JJ, Pego JM, Taipa R, Bessa JM, Almeida OF, Sousa N: Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 2005, 25:7792-7800.
- [33]Sullivan RM, Gratton A: Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology 2002, 27:99-114.
- [34]Vyas A, Pillai AG, Chattarji S: Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
- [35]Mitra R, Ferguson D, Sapolsky RM: SK2 potassium channel overexpression in basolateral amygdala reduces anxiety, stress-induced corticosterone secretion and dendritic arborization. Mol Psychiatry 2009, 14:847-855. 827
- [36]Morales-Medina JC, Sanchez F, Flores G, Dumont Y, Quirion R: ReMorphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J Chem Neuroanat 2009, 38:266-272.
- [37]Radley JJ, Rocher AB, Rodriguez A, Ehlenberger DB, Dammann M, McEwen BS, Morrison JH, Wearne SL, Hof PR: Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J Comp Neurol 2008, 507:1141-1150.
- [38]Seib LM, Wellman CL: Daily injections alter spine density in rat medial prefrontal cortex. Neurosci Lett 2003, 337:29-32.
- [39]Brown SM, Henning S, Wellman CL: Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 2005, 15:1714-1722.
- [40]Izquierdo A, Wellman CL, Holmes A: Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 2006, 26:5733-5738.
- [41]Cerqueira JJ, Taipa R, Uylings HB, Almeida OF, Sousa N: Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex 2007, 17:1998-2006.
- [42]van Tol MJ, van der Wee NJ, van den Heuvel OA, Nielen MM, Demenescu LR, Aleman A, Renken R, van Buchem MA, Zitman FG, Veltman DJ: Regional brain volume in depression and anxiety disorders. Arch Gen Psychiatry 2010, 67:1002-1011.
- [43]Savitz JB, Drevets WC: Imaging phenotypes of major depressive disorder: genetic correlates. Neuroscience 2009, 164:300-330.
- [44]Hermann A, Schafer A, Walter B, Stark R, Vaitl D, Schienle A: Emotion regulation in spider phobia: role of the medial prefrontal cortex. Soc Cogn Affect Neurosci 2009, 4:257-267.
- [45]Etkin A, Wager TD: Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatr 2007, 164:1476-1488.
- [46]Kalisch R, Salome N, Platzer S, Wigger A, Czisch M, Sommer W, Singewald N, Heilig M, Berthele A, Holsboer F, Landqraf R, Auer DP: High trait anxiety and hyporeactivity to stress of the dorsomedial prefrontal cortex: a combined phMRI and Fos study in rats. Neuroimage 2004, 23:382-391.
- [47]Miller MM, Morrison JH, McEwen BS: Basal anxiety-like behavior predicts differences in dendritic morphology in the medial prefrontal cortex in two strains of rats. Behav Brain Res 2012, 229:280-288.
- [48]Shansky RM, Hamo C, Hof PR, McEwen BS, Morrison JH: Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cereb Cortex 2009, 19:2479-2484.
- [49]Radley JJ, Rocher AB, Janssen WG, Hof PR, McEwen BS, Morrison JH: Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp Neurol 2005, 196:199-203.
- [50]Paxinos R, Watson C: The Rat Brain in Stereotaxic Coordinates. 5th edition. San Diego: Elsevier; 2005.
- [51]Chung HJ, Jan YN, Jan LY: Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc Natl Acad Sci U S A 2006, 103:8870-8875.
- [52]Pellow S, Chopin P, File SE, Briley M: Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167.
- [53]Wall PM, Messier C: Infralimbic kappa opioid and muscarinic M1 receptor interactions in the concurrent modulation of anxiety and memory. Psychopharmacology (Berl) 2002, 160:233-244.