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The Journal of Neuroscience, April 14, 2004, 24(15):3810-3815; doi:10.1523/JNEUROSCI.4100-03.2004

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Behavioral/Systems/Cognitive
Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats

Greg D. Gale,1 Stephan G. Anagnostaras,2 Bill P. Godsil,1 Shawn Mitchell,1 Takashi Nozawa,1 Jennifer R. Sage,1 Brian Wiltgen,1 and Michael S. Fanselow1

Departments of 1Psychology and 2Neurobiology, University of California, Los Angeles, Los Angeles, California 90095-1563

The basolateral amygdala (BLA) is intimately involved in the development of conditional fear. Converging lines of evidence support a role for this region in the storage of fear memory but do not rule out a time-limited role in the memory consolidation. To examine this issue, we assessed the stability of BLA contribution to fear memories acquired across the adult lifetime of rats. Fear conditioning consisted of 10 tone–shock pairings in one context (remote memory), followed 16 months later by 10 additional tone–shock pairings with a novel tone in a novel context (recent memory). Twenty-four hours after recent training, rats were given NMDA or sham lesions of the BLA. Contextual and tone freezing were independently assessed in individual test sessions. Sham-lesioned rats showed high and comparable levels of freezing across all context and tone tests. In contrast, BLA-lesioned rats displayed robust freezing deficits across both recent and remote tests. Subsequent open-field testing revealed no effects of BLA lesions on activity patterns in a dark open field or during bright light exposure. Lesioned rats were able to reacquire normal levels of context-specific freezing after an overtraining procedure (76 unsignaled shocks). Together, these findings indicate that BLA lesions do not disrupt freezing behavior by producing hyperactivity, an inability to suppress behavior, or an inability to freeze. Rather, the consistent pattern of freezing deficits at both training-to-lesion intervals supports a role for the BLA in the permanent storage of fear memory.

Key words: behavior; learning; memory; NMDA; retrograde; shock


Received Sep 4, 2003; revised January 7, 2004; accepted January 8, 2004.




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