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The Journal of Neuroscience, September 21, 2005, 25(38):8725-8734; doi:10.1523/JNEUROSCI.2260-05.2005

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Behavioral/Systems/Cognitive
Previous Stress Facilitates Fear Memory, Attenuates GABAergic Inhibition, and Increases Synaptic Plasticity in the Rat Basolateral Amygdala

Pablo A. Rodríguez Manzanares,¹ Nora A. Isoardi,¹ Hugo F. Carrer,² and Víctor A. Molina¹

¹Departamento de Farmacología, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, and ²Instituto de Investigación Médica Mercedes y Martín Ferreyra, Consejo Nacional de Investigaciones Científicas y Técnicas, 5016 Córdoba, Argentina

In experiments designed to investigate the relationship between stress and the acquisition of new fear memories, it was found that previous exposure to a restraint session increased fear conditioning in a contextual fear paradigm. Moreover, the infusion of bicuculline, a competitive antagonist of GABA_A receptors, into the basolateral amygdala complex (BLA), but not into the central amygdaloid nucleus, induced the same behavioral effect. Pretreatment with midazolam (MDZ), a positive modulator of GABA_A sites, prevented the facilitating influence on fear memory of both stress and GABA_A receptor blockade in the BLA. These data suggest that facilitation of fear conditioning could be causally related to increased neuronal excitability attributable to depressed GABAergic inhibition in the BLA. To test this hypothesis, evoked potentials were studied in brain slices from stressed animals. Potentials evoked in the BLA by single stimuli applied to the external capsule showed multispike responses, suggestive of GABAergic disinhibition. These multiple responses were no longer evident after the slices were perfused with diazepam or if the stressed animals were pretreated with MDZ. In slices from stressed rats, paired-pulse inhibition (GABA dependent) was suppressed. Also, in stressed animals, long-term potentiation (LTP) was induced with a single train of high-frequency stimulation, which did not induce LTP in control rats. Moreover, MDZ pretreatment prevented the facilitating influence of stress on LTP induction. All of these findings support the hypothesis that previous stress attenuates inhibitory GABAergic control in the BLA, leading to neuronal hyperexcitability and increased plasticity that facilitates fear learning.

Key words: stress; fear memory; basolateral amygdala; GABAergic disinhibition; midazolam; LTP

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Received Dec 20, 2004; revised July 20, 2005; accepted July 20, 2005.

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