Perirhinal Cortex Supports Delay Fear Conditioning to Rat Ultrasonic Social Signals

Abstract

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.

Single-unit responses to 22kHz ultrasonic vocalizations in rat perirhinal cortex

“…The selection of PR as an initial region of interest was partly based on the discovery that damage to this structure impairs fear conditioning to USVs [24,29] but has no significant effect on conditioning to continuous tones [10,24,29,34]. The fact that cortical processing is not necessary for conditioning to continuous tones is commonly interpreted to mean that activity in the subcortical projection from the auditory thalamus to the amygdala is sufficient to represent these relatively simple stimuli [22,34,42,43].…”

“…Similar auditory stimuli have previously been used as cues to support Pavlovian fear conditioning [24]. Experiment 2 used 6 stimuli (including 4 new ones) that were designed to isolate certain features of USVs that may be responsible for eliciting single-unit responses: 2 pre-recorded USVs (~65 dB SPL), which differed markedly from each other in terms of call structure; 2 frequency-and temporally-matched tone segments (10 ms rise/fall time, 65 dB SPL); and 2 frequency-matched continuous tones (10 ms rise/fall time, 65 dB SPL).…”

“…These particular types of stimuli were chosen because they have previously been used as cues to evaluate the role of PR in Pavlovian fear conditioning [24]. Forty-five units (59%) were responsive to one or more of the auditory stimuli (95% CI: 49-70%).…”

“…The anatomical connectivity of PR places this periallocortical region at a pivotal intersection between perceptual processing in neocortex and the declarative and emotional memory systems associated with various medial temporal lobe structures [26,27,39]. Removal of rat PR impairs subsequent fear conditioning to 22 kHz USVs [24,29] but has no significant effect on conditioning to continuous tones cues at the same [24,29] or lower frequencies [10,24,34].…”

The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function

“…Furthermore, a multitude of recent studies have shown that discontinuous tones (including ultrasonic vocalisations) recruit the perirhinal cortex but continuous tones do not (Kholodar-Smith et al, 2008a;Bang and Brown, 2009b). Confirmation of these findings come from electrophysiological data which shows that there are different firing patterns observed in the perirhinal cortex during exposure to discontinuous tones compared to continuous tones (Furtak et al, 2007c) and from lesions of the perirhinal cortex where there is impairment of conditioning to ultrasonic vocalisations but not to continuous tones (Lindquist et al, 2004). These results fit with the data generated from recognition and fear conditioning tasks where the perirhinal cortex is required for processing more complex stimuli and contexts (Corodimas and LeDoux, 1995;Sacchetti et al, 1999;Bucci et al, 2000Bucci et al, , 2002Bussey et al, 2000;Eacott et al, 2001;Burwell et al, 2004a).…”