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The Journal of Neuroscience, April 21, 2004, 24(16):4020-4029; doi:10.1523/JNEUROSCI.5531-03.2004

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Behavioral/Systems/Cognitive
Corticotropin-Releasing Factor and Urocortin I Modulate Excitatory Glutamatergic Synaptic Transmission

Jie Liu,¹ Baojian Yu,¹ Volker Neugebauer,¹ Dimitri E. Grigoriadis,² Jean Rivier,³ Wylie W. Vale,³ Patricia Shinnick-Gallagher,¹ and Joel P. Gallagher¹

¹Department of Pharmacology and Toxicology, University of Texas Medical Branch, Galveston, Texas 77555-1031, ²Neurocrine Biosciences Incorporated, San Diego, California 92121, and ³Clayton Foundation Laboratories for Peptide Biology, The Salk Institute for Biological Studies, Peptide Biology Laboratory, La Jolla, California 92037

Corticotropin-releasing factor (CRF)-related peptides serve as hormones and neuromodulators of the stress response and play a role in affective disorders. These peptides are known to alter complex behaviors and neuronal properties, but their receptor-mediated effects at CNS synapses are not well described. Here we show that excitatory glutamatergic transmission is modulated by two endogenous CRF-related peptide ligands, corticotropin-releasing factor [CRF rat/human (r/h)] and Urocortin I (Ucn I), within the central nucleus of the amygdala (CeA) and the lateral septum mediolateral nucleus (LSMLN). These limbic nuclei are reciprocally innervated, are involved in stress and affective disorders, and have high densities of the CRF receptors CRF₁ and CRF₂. Activation of these receptors exerts diametrically opposed actions on glutamatergic transmission in these nuclei. In the CeA, CRF(r/h) depressed excitatory glutamatergic transmission through a CRF₁-mediated postsynaptic action, whereas Ucn I facilitated synaptic responses through presynaptic and postsynaptic CRF₂-mediated mechanisms. Conversely, in the LSMLN, CRF caused a CRF₁-mediated facilitation of glutamatergic transmission via postsynaptic mechanisms, whereas Ucn I depressed EPSCs by postsynaptic and presynaptic CRF₂-mediated actions. Furthermore, antagonists of these receptors also affected glutamatergic neurotransmission, indicating that endogenous ligands tonically modulated synoptic activity at these synapses.

These data show that CRF receptors in CeA and LSMLN synapses exert and maintain a significant synaptic tone and thereby regulate excitatory glutamatergic transmission. The results also suggest that CRF receptors may provide novel targets in affective disorders and stress.

Key words: CRF; amygdala; lateral septum; glutamatergic synaptic transmission; synaptic homeostasis; urocortin

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Received July 18, 2003; revised March 10, 2004; accepted March 10, 2004.

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