Neurotoxic Lesions of the Lateral Nucleus of the Amygdala Decrease Conditioned Fear But Not Unconditioned Fear of a Predator Odor: Comparison with Electrolytic Lesions

Abstract

Considerable evidence suggests that the lateral (LA) and basal (BA) nuclei of the amygdala are sites of plasticity and storage of emotional memory. Recent arguments, however, have seriously challenged this view, suggesting that the effects of amygdala lesions are attributable to interference with performance of fear behavior and not learning and memory. One way to address this controversy is to measure the same behavioral response during both conditioned and unconditioned fear. This is done in the present study by measuring fear-related freezing behavior after electrolytic and neurotoxic lesions of the LA or LA/BA nuclei in rats in a contextual fear conditioning paradigm and unconditioned fear to a predator odor. Electrolytic LA lesions attenuated post-shock freezing, retention test freezing, and freezing to the predator odor trimethylthiazoline (TMT). In contrast, excitotoxic NMDA lesions of the LA had no effect on post-shock freezing but significantly attenuated retention test freezing. Furthermore, excitotoxic LA lesions did not diminish freezing to TMT. Larger excitotoxic lesions that included the BA significantly reduced freezing in both the post-shock and retention tests but did not appreciably decrease freezing to TMT. The results suggest that the LA is important for memory of learned fear but not for generation of freezing behavior. In addition, the BA plays a role in freezing in conditioned fear situations but not in unconditioned fear. The studies suggest that the LA and BA play different roles in fear conditioning, but neither of them has a significant role in unconditioned freezing to a predator odor.

Temporary Inactivation of the Bed Nucleus of the Stria Terminalis But Not of the Amygdala Blocks Freezing Induced by Trimethylthiazoline, a Component of Fox Feces

“…Because muscimol works via GABA A receptors, fibers of passage are not inactivated. Therefore, the findings of the present study are in agreement with the explanation offered by Wallace and Rosen (2001). In addition, our study confirmed findings (Wallace and Rosen, 2001) that the lateral nucleus of the amygdala is not necessary for the production of freezing per se.…”

“…This supports the results of Wallace and Rosen (2001) demonstrating an unimpaired freezing response to TMT after neurotoxic lesions of the amygdala. In that study, electrolytic lesions of the amygdala reduced or blocked TMT-induced freezing.…”

“…These studies have established a brain circuitry including the amygdala, the bed nucleus of the stria terminalis (BNST), the periaqueductal gray, as well as several other nuclei, as being responsible for the expression of learned and unlearned fear responses. Wallace and Rosen (2001) demonstrated that neurotoxic lesions of the amygdala did not affect TMT-induced freezing. This finding suggests that other parts of the brain circuitry described above must be responsible for the elicitation of freezing by TMT.…”

Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression

“…A previous report has shown that lesioning the BLA does not effect fear-related behavioral responses to fox odor (Wallace and Rosen, 2001); whereas, other studies demonstrate that lesioning and/or inactivating the BLA alters freezing in response to cat or fox odors (Vazdarjanova et al, 2001;Takahashi et al, 2005;Muller and Fendt, 2006). In addition, exposure to cat odor failed to increase BLA c-fos expression (Dielenberg et al, 2001), but in another study exposure to red fox odor increased BLA c-fos expression (Funk and Amir, 2000).…”

Impairment of Fear Memory Consolidation in Maternally Stressed Male Mouse Offspring: Evidence for Nongenomic Glucocorticoid Action on the Amygdala

“…To examine innate fear, mice were placed in the chamber with a beaker containing 30 l of a synthetic fox feces odor, trimethylthiazoline (TMT; PheroTech), which was reported previously to elicit freezing in rodents (Wallace and Rosen, 2001). TMT-evoked freezing was recorded for 10 min after TMT exposure and scored as a percentage of the time spent in the freezing behavior at 2 min intervals.…”