Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS⁺ and CS⁻

Abstract

In classical fear conditioning, a neutral sensory stimulus (CS) acquires the ability to elicit fear responses after pairing to a noxious unconditioned stimulus (US). As amygdala lesions prevent the acquisition of fear responses and the lateral amygdaloid (LA) nucleus is the main input station of the amygdala for auditory afferents, the effect of auditory fear conditioning on the sensory responsiveness of LA neurons has been examined. Although conditioning was shown to increase CS-evoked LA responses, the specificity of the changes in responsiveness was not tested. Because conditioning might induce nonspecific increases in LA responses to auditory afferents, we re-examined this issue in conscious, head-restrained cats using a differential conditioning paradigm where only one of two tones (CS⁺but not CS⁻) was paired to the US. Differential conditioning increased unit and field responses to the CS⁺, whereas responses to the CS⁻ decreased. Such changes have never been observed in the amygdala except in cases where the CS⁻ had been paired to the US before and fear responses not extinguished. This suggests that fear conditioning is not only accompanied by potentiation of amygdalopetal pathways conveying the CS⁺ but also by the depression of sensory inputs unpaired to noxious stimuli.