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The Journal of Neuroscience, November 17, 2004, 24(46):10326-10334; doi:10.1523/JNEUROSCI.2758-04.2004

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Behavioral/Systems/Cognitive
Fear-Potentiated Startle in Rats Is Mediated by Neurons in the Deep Layers of the Superior Colliculus/Deep Mesencephalic Nucleus of the Rostral Midbrain through the Glutamate Non-NMDA Receptors

Zuowei Zhao¹ and Michael Davis^1,2

¹Department of Psychiatry and Behavioral Sciences, School of Medicine, and ²The Center for Behavior Neuroscience, Emory University, Atlanta, Georgia 30329

The amygdala sends heavy and broad projections to the rostral midbrain including the periaqueductal gray (PAG), the deep layers of the superior colliculus/deep mesencephalic nucleus (deep SC/DpMe), and the lateral mesencephalic reticular formation (MRF) that in turn project to the nucleus reticularis pontis caudalis (PnC), an obligatory relay in the primary acoustic startle circuit. Chemical lesions or inactivation of these areas blocked fear-potentiated startle, suggesting that these areas serve as a relay between the amygdala and the PnC. In the present study, we tried to determine more precisely which of these sites were critical for fear-potentiated startle and the role of glutamate receptors in this site in mediating fear-potentiated startle. Local infusion of the non-NMDA receptor antagonist 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo(F)-quinoxaline (NBQX) dose-dependently blocked fear-potentiated startle when infused into the deep SC/DpMe before testing but had no effect on baseline startle amplitude. NBQX did not block fear-potentiated startle when infused before training. The same dose of NBQX infused into the dorsal/lateral PAG, the lateral MRF, or the superficial layers of the SC did not affect fear-potentiated startle. However, NBQX tended to reduce contextual freezing when infused into the dorsal/lateral PAG. These findings suggest that the deep SC/DpMe is the site that serves as a critical output relay between the amygdala and the PnC in mediating fear-potentiated startle and that glutamatergic transmission is required for this action.

Key words: amygdala; PnC; PAG; AMPA; NBQX; context

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Received March 18, 2004; revised October 5, 2004; accepted October 5, 2004.

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