Temporal behavior in auditory fear conditioning: Stimulus property matters

Abstract

The accuracy of time judgments depends upon many factors, including the sensory properties of the to-be-timed stimulus. In auditory Pavlovian fear conditioning, an initially neutral tone (conditioned stimulus, CS) predicts the arrival of an aversive event (unconditioned stimulus, US) at a fixed time interval. The temporal relation between the CS and US events is encoded, leading to the development of a temporal pattern of responding. Little attention has been paid to the potential impact of the characteristics of the tone-CS on the development of this temporal pattern. Here we compared the acquisition of the temporal pattern of conditioned responses of rats to different tone-CS frequencies. Rats were first conditioned to lever press for food. Then, while lever pressing for food, they were presented with 60-s tones of two widely separated frequencies, 1 kHz or 11 kHz, each paired with a foot-shock given 30 s after tone onset. This fear conditioning led to the appearance of CS-induced conditioned suppression of lever pressing, with no observed difference in conditioning to the shock. On probe trials, the tone duration was 60 s, and the reinforcer was omitted. With training, a pattern of suppression evolved during the probe trials, showing a maximum of suppression near the programmed time of the shock-US. However the 11-kHz tone-CS yielded better temporal control than did the 1-kHz tone. A second experiment investigated rats' abilities to discriminate between two times of shock arrival (10 s or 30 s) predicted by the different tone frequencies (1 kHz or 11 kHz). In this experiment, rats showed poorer discriminative timing performance when the lower frequency (1 kHz) was associated with the longer duration (30 s). Our results suggest a strong impact of the CS sensory properties on the expression of temporal learning within the context of auditory fear conditioning in rats.