Abstract
After acquisition, hippocampus-dependent memories undergo a systems consolidation process, during which they become independent of the hippocampus and dependent on the anterior cingulate cortex (ACC) for memory expression. However, consolidated remote memories can become transiently hippocampus-dependent again following memory reactivation. How this systems reconsolidation affects the role of the ACC in remote memory expression is not known. Using contextual fear conditioning, we show that the expression of 30-day-old remote memory can transiently be supported by either the ACC or the dorsal hippocampus following memory reactivation, and that the ACC specifically mediates expression of remote generalized contextual fear memory. We found that suppression of neural activity in the ACC with the AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) impaired the expression of remote, but not recent, contextual fear memory. Fear expression was not affected by this treatment if preceded by memory reactivation 6 h earlier, nor was it affected by suppression of neural activity in the dorsal hippocampus with the GABA-receptor agonist muscimol. However, simultaneous targeting of both the ACC and the dorsal hippocampus 6 h after memory reactivation disrupted contextual fear memory expression. Second, we observed that expression of a 30-day-old generalized contextual fear memory in a novel context was not affected by memory reactivation 6 h earlier. However, intra-ACC CNQX infusion before testing impaired contextual fear expression in the novel context, but not the original training context. Together, these data suggest that although the dorsal hippocampus may be recruited during systems reconsolidation, the ACC remains necessary for the expression of generalized contextual fear memory.
Highlights
Lesions or pharmacological inactivation of the hippocampus preferentially impact recently acquired contextual fear memory (Anagnostaras et al, 1999; de Oliveira Alvares et al, 2012; Goshen et al, 2011; Kitamura et al, 2009; Ward et al, 1999; Wiltgen et al, 2010; Winocur et al, 2009)
We examined the effects of suppressing neural activity in the anterior cingulate cortex (ACC) on fear memory expression during tests of recent and remote memory, and during a test following remote memory reactivation
Fear memory expression on test 2 (P40.05; Figure 1e). These results suggest that following reactivation of 30-dayold remote memory, memory can be transiently expressed without the ACC 6 h later, before returning to an ACC
Summary
Lesions or pharmacological inactivation of the hippocampus preferentially impact recently acquired contextual fear memory (Anagnostaras et al, 1999; de Oliveira Alvares et al, 2012; Goshen et al, 2011; Kitamura et al, 2009; Ward et al, 1999; Wiltgen et al, 2010; Winocur et al, 2009). Recent studies suggest that retrieval can make remote hippocampus-independent contextual fear memory again dependent on the hippocampus for a brief time (Debiec et al, 2002; Winocur et al, 2009) Such renewed dependence on the hippocampus after memory reactivation is called systems reconsolidation. These studies showed that electrolytic lesions of the dorsal hippocampus impaired remote memory only when applied after memory reactivation It remains unclear, whether remote memory reactivation affects the role of the ACC. To examine how remote memory reactivation affects the such as muscimol, are known to suppress neuronal activity brain structures supporting contextual fear memory for longer periods. Muscimol was dissolved in artificial cerebrospinal fluid and injected at 0.5 mg/0.5 ml per side
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