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The Journal of Neuroscience, April 7, 2004, 24(14):3610-3617; doi:10.1523/JNEUROSCI.4839-03.2004

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Behavioral/Systems/Cognitive
Perirhinal Cortex Supports Delay Fear Conditioning to Rat Ultrasonic Social Signals

Derick H. Lindquist,¹ Leonard E. Jarrard,² and Thomas H. Brown¹

¹Department of Psychology, Yale University, New Haven, Connecticut 06520, and ²Department of Psychology, Washington and Lee University, Lexington, Virginia 24450

Auditory information can reach the lateral nucleus of the amygdala (LA) through a monosynaptic thalamic projection or a polysynaptic cortical route. The polymodal input from the perirhinal cortex (PR) is a major informational gateway to the LA and nearby structures. Pretraining PR lesions impair fear conditioning to a context, but there have been no reports that they cause deficits in delay conditioning to an auditory cue. The direct subcortical projection to the LA seems sufficient to support delay conditioning to a tone conditional stimulus (CS). We examined the effect of PR lesions on delay conditioning to two different tone conditional stimuli (4 and 22 kHz tones; both 10 sec duration) and two different rat ultrasonic vocalization (USV) conditional stimuli (10 sec of "22 kHz USVs"). The two USV conditional stimuli were multi-call segments that were recorded (digitized at 100 kHz) from two different rats. One USV CS was a continuous sequence of eight calls, and the other was a portion of a continuous sequence of six calls. PR lesions significantly impaired conditioning to both USV conditional stimuli and to the training context but had no significant effect on conditioning to either tone CS. The role of PR in fear conditioning appears not to be determined by whether the conditional stimuli serve as contexts or cues, but instead by the nature or complexity of the stimuli or stimulus configurations. These cue-specific effects of PR lesions are suggested to reflect differences in the stimulus features that are encoded in the two CS pathways to the LA.

Key words: fear conditioning; medial temporal lobe; perirhinal cortex; ultrasonic vocalization; amygdala; freezing

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Received Oct 28, 2003; revised January 23, 2004; accepted February 17, 2004.

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