Central amygdala lesions block ultrasonic vocalization and freezing as conditional but not unconditional responses

Bilateral amygdala (AM) lesions prevent the acquisition of fear-related conditional responses (CRs) in rats, a result that is most commonly concluded to reflect a learning or memory deficit. An alternative hypothesis is that AM-lesioned animals fail to acquire certain fear CRs simply because they cannot perform these behaviors. This performance-deficit hypothesis is usually invoked in regard to studies in which the CR is freezing, the most commonly measured behavior. Here we explore this interpretation by measuring two different behaviors [freezing and 22 kHz ultrasonic vocalization (USV)] elicited under three conditions (during context conditioning, during subsequent retention testing, and after ejaculation) in experimental rats [that received electrolytic lesions of the central nucleus of the amygdala (ACe)] and control animals (that received a sham operation). If ACe damage produces a discrete motor deficit that specifically renders the animal unable to remain immobile, then freezing should be blocked or impaired when elicited under all three conditions, whereas USV should be spared. Alternatively, if ACe damage selectively interferes with CR formation, maintenance, or expression, then both freezing and USV should be blocked or impaired when elicited as CRs during acquisition and retention testing but spared when evoked as unconditional responses (URs) to ejaculation. ACe damage blocked or severely impaired both freezing and USV elicited as CRs but had no effect on either behavior elicited as URs. We reject the motor-deficit hypothesis and discuss some viable alternatives.