Research ReportModulation of auditory-evoked potentials recorded in the inferior colliculus by GABAergic mechanisms in the basolateral and central nuclei of the amygdala in high- and low-anxiety rats

The central nucleus of the inferior colliculus (CIC) is an important relay station for acoustic information that has an aversive connotation. γ-Aminobutyric acid (GABA) mechanisms exert tonic inhibitory control over the neural substrates of aversion in the midbrain tectum. Recent evidence obtained in this laboratory showed that low- (LA) and high-anxiety (HA) rats selected in the elevated plus maze (EPM) exhibit low and high auditory-evoked potential (AEP) amplitudes, respectively, recorded in the CIC when subjected to loud click noises. The present study investigated the eventual top-down regulation exerted by GABA mechanisms in the basolateral (BLA) and central (CeA) nuclei of the amygdala on aversive information processing at the level of the CIC. The GABA inhibitors bicuculline (10 ng/0.2 μl) and semicarbazide (7 μg/0.2 μl) and GABA agonist muscimol (1 nmol/0.2 μl) were locally infused into the CeA and BLA in rats subjected to an AEP recording procedure that used electrodes implanted in the CIC. Freezing behavior induced by these intra-amygdala injections was also measured. The results confirmed that the processing of aversive acoustic information depends on anxiety levels in LA and HA rats. Freezing behavior and the increased AEPs induced by intra-CeA injections of bicuculline and semicarbazide were more pronounced in HA than in LA animals. Intra-CeA injections of muscimol did not change either the basal levels of freezing or AEP amplitudes in LA and HA rats. However, freezing and the enhanced AEPs were of small magnitude following intra-BLA injections of bicuculline and semicarbazide. An unexpected magnitude of freezing and enhanced AEPs was observed following muscimol infusions into the BLA in HA rats. GABA mechanisms in the CeA appear to play a regulatory role in aversive states, and inactivation of the BLA with muscimol produced pro-aversive effects, suggesting that inactivation of the BLA removed the descending inhibitory control of the neural substrates of aversion in the CIC exerted by the BLA. Because the latter effects were observed only in HA rats, a dysfunctional BLA may underlie the differences between trait and state anxiety.

► Low- (LA) and high-anxiety (HA) rats were subjected to measurements of the collicular auditory evoked potentials (AEP). ► The influence of GABAA receptors of the basolateral (BLA) and central (CeA) nuclei of the amygdala on the AEP was analyzed. ► The inactivation of BLA neurons further depress the BLA inhibitory system of HA rats. ► Main differences between trait and state anxiety in rats may result from a dysfunction of the BLA complex.