Relationship of freezing and stimulus-evoked heart-rate changes in the acoustic startle habituation paradig

In the acoustic startle paradigm, contextual cues of the startle chamber can become associated with the initially aversive startle stimulus through Pavlovian conditioning. This fear conditioning process is manifested in freezing behavior and enhanced response amplitudes. Changes in heart rate can also index conditioned fear, and are elicited unconditionally by acoustic startle stimuli. The present series of experiments was designed to examine the extent to which heart-rate changes evoked by acoustic startle stimuli are affected by the development of fear. In experiment 1, rats which received presentations of a 120-dB, 100-ms, white noise startle stimulus displayed significantly more freezing and phasic heart-rate accelerations than animals receiving a 92-dB stimulus, whereas heart-rate decelerations did not differ. In Experiment 2, electrolytic amygdala lesions attenuated freezing, phasic heart-rate accelerations and decelerations, and within-session decreases in prestimulus heart rate evoked by a 120-dB stimulus. Amygdala central nucleus lesions were used in conjunction with two levels of stimulus intensity (87 and 120 dB) in Experiment 3 to determine whether or not the central nucleus is differentially involved in responses to intense acoustic stimuli. The lesions reduced all responses induced by the 120-dB stimulus: freezing, phasic heart-rate accelerations and decelerations, and the tonic decrease in prestimulus heart-rate. For the 87-dB stimulus, the lesions attenuated only the phasic heart-rate decelerations. In a continuation of Experiment 3 (3a), the amygdala lesions attenuated phasic cardiac decelerations evoked by a CS-like, 85-dB, 10-s, 1-kHz pure tone. In Experiment 4, sympathetic and parasympathetic blockade were used to characterize the patterns of autonomic activity underlying the heart-rate changes elicited by the 120-dB stimulus. The phasic accelerations were sympathetically mediated, whereas both the tonic and phasic decelerations were parasympathetically mediated. Phasic accelerations still showed a within-session developmental sequence even when the phasic deceleration was pharmacologically blocked. The results of this series of experiments indicate that heart-rate responses to nonsignal stimuli depend critically on an animal's previous experience with those stimuli. The amygdala is involved in the fear-related heart-rate changes, but also in the phasic heart-rate decelerations which showed no influence of fear.