Single-Unit Firing in Rat Perirhinal Cortex Caused by Fear Conditioning to Arbitrary and Ecological Stimuli

Abstract

Pretraining lesions of rat perirhinal cortex (PR) severely impair pavlovian fear conditioning to a 22 kHz ultrasonic vocalization (USV) cue. However, PR lesions are without significant effect when the cue is a continuous tone at the same or a lower frequency. Here we examined fear-conditioning-produced changes in single-unit firing elicited in rat PR by a 22 kHz tone cue or a 22 kHz USV cue. Chronic recording electrodes were introduced from the lateral surface of the skull. Altogether, 200 well isolated units were studied in 28 rats. Overall, 73% of the recorded single units (145 of 200 units) evidenced statistically significant firing changes in response to the tone or USV conditional stimulus (CS) after it had been paired several times with an aversive unconditional stimulus (US). Interestingly, 33% of units (66 of 200 units) that were initially CS-unresponsive became CS-responsive after conditioning. After conditioning, there were two notable differences between single-unit responses elicited by the USV cue and those elicited by the tone cue. First, 11% of the units (14 of 123 units) recorded from the USV-conditioned group displayed a precisely timed increase in firing rate during the 260 ms interval in which the US had previously occurred. This US-timed response was unique to the USV-conditioned group. Second, the mean latency of cue-elicited firing was ϳ30 ms longer in the USV-conditioned group than in the tone-conditioned group. These cue-specific differences in acquired firing latencies and acquired firing patterns suggest that spectrotemporal properties of a CS can control the essential circuitry or neurophysiological mechanisms underlying fear conditioning.

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).…”

“…Electrophysiological recordings made in the perirhinal cortex during trace conditioning using auditory stimuli (Furtak et al, 2007c) and immediate early gene imaging shows increased levels of c-Fos in the perirhinal cortex following a fear conditioning task (Campeau et al, 1997). Antagonism of perirhinal muscarinic acetylcholinergic receptors using scopolamine has been shown to disrupt trace conditioning using auditory stimuli (Bang and Brown, 2009a).…”

Persistent activity in a cortical-to-subcortical circuit: bridging the temporal gap in trace eyelid conditioning

“…For analysis purposes the average counts for the 10 pre-CS bins were determined for every trial. The statistical reliability of changes in activity during trials over a session was determined using separate paired t-tests for each of the 40 bins following the CS, with the variability across trials as the error term (Furtak et al 2007;Quintana et al 1988;Weible et al 2003;Zhou et al 2007). Each paired t-test compared the counts within a given time bin for each trial with the average counts of the pre-CS bins for that same trial.…”

Two cortical systems for memory-guided behaviour

“…For instance, neural activity in the monkey PRC has been shown to reflect learning about objects that are cues for upcoming rewards 47 , and this learning is abolished following lesions to the PRC 48 or interference with dopamine D2 receptors in the PRC 49 . In rats, PRC lesions impair fear conditioning to complex auditory [50][51][52] or olfactory object cues 53 , and PRC neurons show increased firing during the presentation of auditory objects that have been associated with an aversive, unconditioned stimulus 54 .…”