Perirhinal cortex supports acquired fear of auditory objects

Damage to rat perirhinal cortex (PR) profoundly impairs fear conditioning to 22 kHz ultrasonic vocalizations (USVs), but has no effect on fear conditioning to continuous tones. The most obvious difference between these two sounds is that continuous tones have no internal temporal structure, whereas USVs consist of strings of discrete calls separated by temporal discontinuities. PR was hypothesized to support the fusion or integration of discontinuous auditory segments into unitary representations or auditory objects. This transform was suggested to be necessary for normal fear conditioning to occur. These ideas naturally assume that the effect of PR damage on auditory fear conditioning is not peculiar to 22 kHz USVs. The present study directly tested these ideas by using a different set of continuous and discontinuous auditory cues. Control and PR-damaged rats were fear conditioned to a 53 kHz USV, a 53 kHz continuous tone, or a 53 kHz discontinuous tone. The continuous and discontinuous tones matched the 53 kHz USV in terms of duration, loudness, and principle frequency. The on/off pattern of the discontinuous tone matched the pattern of the individual calls of the 53 kHz USV. The on/off pattern of the 50 kHz USV was very different from the patterns in the 22 kHz USVs that have been comparably examined. Rats with PR damage were profoundly impaired in fear conditioning to both discontinuous cues, but they were unimpaired in conditioning to the continuous cue. The implications of this temporal discontinuity effect are explored in terms of contemporary ideas about PR function. (C) 2009 Elsevier Inc. All rights reserved.