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The Journal of Neuroscience, April 7, 2004, 24(14):3471-3479; doi:10.1523/JNEUROSCI.5740-03.2004

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Behavioral/Systems/Cognitive
Corticotrophin Releasing Factor-Induced Synaptic Plasticity in the Amygdala Translates Stress into Emotional Disorders

Donald G. Rainnie,¹ Richard Bergeron,² Tammy J. Sajdyk,⁴ Madhvi Patil,¹ Donald R. Gehlert,³ and Anantha Shekhar⁴

¹Department of Psychiatry and Center for Behavioral Neuroscience, Emory University, Atlanta, Georgia 30322, ²Department of Psychiatry, Ottawa Health Research Institute, Ottawa, Ontario, Canada, ³Central Nervous System Therapeutic Area, Eli Lilly and Company, Indianapolis, Indiana, and ⁴Department of Psychiatry, Indiana University School of Medicine, Indianapolis, Indiana 46202

The amygdala is involved in the associative processes for both appetitive and aversive emotions, and its function is modulated by stress hormones. The neuropeptide corticotrophin releasing factor (CRF) is released during stress and has been linked to many stress-related behavioral, autonomic, and endocrine responses. In the present study, nonanxiety-inducing doses of a potent CRF type 1 and 2 receptor agonist, urocortin (Ucn), was infused locally into the basolateral amygdala (BLA) of rats. After 5 daily injections of Ucn, the animals developed anxiety-like responses in behavioral tests. Intravenous administration of the anxiogenic agent sodium lactate elicited robust increases in blood pressure, respiratory rate, and heart rate. Furthermore, in the absence of any additional Ucn treatment, these behavioral and autonomic responses persisted for >30 d. Whole-cell patch-clamp recordings from BLA neurons of these hyper-reactive animals revealed a pronounced reduction in both spontaneous and stimulation-evoked IPSPs, leading to a hyperexcitability of the BLA network. This Ucn-induced plasticity appears to be dependent on NMDA receptor and subsequent calcium–calmodulin-dependent protein kinase II (CaMKII) activation, because it is blocked by pretreatment with NMDA receptor antagonists and by coadministration of CaMKII inhibitors. Our results show for the first time a stress peptide-induced behavioral syndrome that can be correlated with cellular mechanisms of neural plasticity, a novel mechanism that may explain the etiological role of stress in several chronic psychiatric and medical disorders.

Key words: urocortin; inhibition; anxiety; basolateral amygdala; in vivo; in vitro

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Received Sep 2, 2003; revised February 20, 2004; accepted February 21, 2004.

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