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Role of bed nucleus of the stria terminalis and amygdala AMPA receptors in the development and expression of context conditioning and sensitization of startle by prior shock

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Abstract

A core symptom of post-traumatic stress disorder is hyper-arousal—manifest in part by increases in the amplitude of the acoustic startle reflex. Gewirtz et al. (Prog Neuropsychopharmacol Biol Psychiatry 22:625–648, 1998) found that, in rats, persistent shock-induced startle increases were prevented by pre-test electrolytic lesions of the bed nucleus of the stria terminalis (BNST). We used reversible inactivation to determine if similar effects reflect actions on (a) BNST neurons themselves versus fibers-of-passage, (b) the development versus expression of such increases, and (c) associative fear versus non-associative sensitization. Twenty-four hours after the last of three shock sessions, startle was markedly enhanced when rats were tested in a non-shock context. These increases decayed over the course of several days. Decay was unaffected by context exposure, and elevated startle was restored when rats were tested for the first time in the original shock context. Thus, both associative and non-associative components could be measured under different conditions. Pre-test intra-BNST infusions of the AMPA receptor antagonist NBQX (3 μg/side) blocked the non-associative (as did infusions into the basolateral amygdala) but not the associative component, whereas pre-shock infusions disrupted both. NBQX did not affect baseline startle or shock reactivity. These results indicate that AMPA receptors in or very near to the BNST are critical for the expression and development of non-associative shock-induced startle sensitization, and also for context fear conditioning, but not context fear expression. More generally, they suggest that treatments targeting the BNST may be clinically useful for treating trauma-related hyper-arousal and perhaps for retarding its development.

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Acknowledgments

This research was supported by NIMH grants MH 47840 (MD), MH080330 (DW), the National Center for Research Resources P51RR165, and the Office of Research Infrastructure Programs/OD P51OD11132. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The authors acknowledge the able assistance of Ms. Yong Yang who performed all histological procedures.

Conflict of interest

The authors declare that they have no conflict of interest. Portions of these data have previously appeared in abstract form (Walker and Davis 2005) and in a review article (Walker et al. 2009).

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  1. Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, 954 Gatewood Rd NE (Yerkes Neuroscience Bldg), Rm. 5214, Atlanta, USA

    Michael Davis & David L. Walker

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Correspondence to David L. Walker.

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Davis, M., Walker, D.L. Role of bed nucleus of the stria terminalis and amygdala AMPA receptors in the development and expression of context conditioning and sensitization of startle by prior shock. Brain Struct Funct 219, 1969–1982 (2014). https://doi.org/10.1007/s00429-013-0616-5

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