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The Journal of Neuroscience, September 1, 2004, 24(35):7654-7662; doi:10.1523/JNEUROSCI.1644-04.2004

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Behavioral/Systems/Cognitive
Selective Neurotoxic Lesions of Basolateral and Central Nuclei of the Amygdala Produce Differential Effects on Fear Conditioning

Ja Wook Koo,¹ Jung-Soo Han,² and Jeansok J. Kim³

¹Department of Psychology, Yale University, New Haven, Connecticut 06520-8205, ²Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218, and ³Department of Psychology and Program in Neurobiology and Behavior, University of Washington, Seattle, Washington 98195-1525

In the fear conditioning literature, it is generally hypothesized that neurons in the basolateral amygdalar complex (BLA) (lateral and basal nuclei) support the formation of conditioned fear memory and project to neurons in the central nucleus (CeA) for the expression of conditioned fear responses. According to this serial processing-transmission view, damage to either BLA or CeA would comparably disrupt the expression of a variety of conditioned fear responses. In the present study, we further investigated the roles of BLA and CeA in fear conditioning by concurrently assessing freezing and 22 kHz ultrasonic vocalization (USV) as dependent measures of fear in rats. Selective neurotoxins, NMDA for the BLA and ibotenic acid for the CeA, were used to destroy intrinsic neurons [evidenced by thionin dye and NeuN (neuronal nuclei) antibody stainings] without damaging the fibers of passage (confirmed by myelin staining). During the 10 tone-footshock paired training, postshock freezing and USV responses were significantly impaired in BLA-lesioned animals, whereas CeA-lesioned animals exhibited only mild deficits. Similarly, conditioned fear responses assessed 24 hr after training were severely reduced in BLA-lesioned animals but not in CeA-lesioned animals. In contrast to ibotenic lesions of the CeA, small electrolytic lesions of the CeA strongly affected both postshock and conditioned freezing and USV. Together, these results do not support the currently espoused BLA-to-CeA serial processing-transmission view of fear conditioning. Instead, the expression of conditioned fear appears to primarily involve BLA projections that course through the CeA en route to downstream fear response structures.

Key words: emotion; ibotenic acid; learning; memory; NMDA; glutamate

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Received April 29, 2004; revised July 8, 2004; accepted July 9, 2004.

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