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The Journal of Neuroscience, November 7, 2007, 27(45):12277-12291; doi:10.1523/JNEUROSCI.1653-07.2007

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

Sharon C. Furtak,¹ Timothy A. Allen,¹ and Thomas H. Brown^1,2

Departments of¹Psychology and ²Cellular and Molecular Physiology, Yale University, New Haven, Connecticut 06520

Correspondence should be addressed to Thomas H. Brown, Department of Psychology, Yale University, 2 Hillhouse Avenue, New Haven, CT 06520. Email: thomas.brown{at}yale.edu

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 30 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.

Key words: timing; medial temporal lobe; ultrasonic vocalization; amygdala; temporal encoding; auditory fear conditioning

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Received April 12, 2007; revised Sept. 17, 2007; accepted Sept. 18, 2007.

Correspondence should be addressed to Thomas H. Brown, Department of Psychology, Yale University, 2 Hillhouse Avenue, New Haven, CT 06520. Email: thomas.brown{at}yale.edu

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