NMDA Receptors in Retrosplenial Cortex Are Necessary for Retrieval of Recent and Remote Context Fear Memory

Corcoran, Kevin A.; Donnan, Michael D.; Tronson, Natalie C.; Guzmán, Yomayra F.; Gao, Can; Jovasevic, Vladimir; Guedea, Anita L.; Radulovic, Jelena

doi:10.1523/jneurosci.2107-11.2011

Cited by 152 publications

(158 citation statements)

References 27 publications

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“…For example, while temporary inactivation of the aRSC effectively hampers IA memory retrieval 21 d after training, pre-test intra-CA1 muscimol impairs IA memory recall up to 14 d posttraining, but not later (Izquierdo and Medina 1997). These findings are consistent with a recent report in mice and in a different fear-motivated memory task (Corcoran et al 2011) and with a meta-analysis of functional MRI studies in humans, showing that the RSC is, indeed, very active during retrieval of recent and remote autobiographical memories (Svoboda et al 2006). In conclusion, the RSC plays an important role in memory processing as a fast learning system that consolidates fear-motivated information and is involved in expression early and also late after acquisition.…”

Section: [Supplemental Materials Is Available For This Article]supporting

confidence: 91%

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Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

Katche¹,

Dorman²,

Slipczuk

et al. 2013

Learn. Mem.

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Memory storage is a temporally graded process involving different phases and different structures in the mammalian brain. Cortical plasticity is essential to store stable memories, but little is known regarding its involvement in memory processing. Here we show that fear memory consolidation requires early post-training macromolecular synthesis in the anterior part of the retrosplenial cortex (aRSC), and that reversible pharmacological inactivation of this cortical region impairs recall of recent as well as of remote memories. These results challenge the generally accepted idea that neocortical areas are slow encoding systems that participate in the retrieval of remote memories only. [Supplemental material is available for this article.]A dominant idea that emerged in the last two decades is that memory consolidation comprises two phases. The initial one, called cellular or synaptic consolidation, is fast, lasting from several hours to a couple of days, and depends on de novo protein and mRNA synthesis required for functional and structural changes in brain regions engaged in the acquisition and early processing of new information, such as the hippocampus and related noncortical structures (Dudai 2002;Dudai and Eisenberg 2004;Morris 2006). The second phase is slower, and would entail the participation of neocortical regions and their interactions with medial temporal lobe structures reorganizing the recently learned material (Squire 1992). It is called systems-level consolidation and seems to begin late after acquisition and last from several days to weeks to months in most learning tasks studied so far (Frankland and Bontempi 2005). However, when recently encoded information interacts with an already stored associative schema, systems-level consolidation may well be very rapid (Tse et al. 2007(Tse et al. , 2011. Consistent with the standard model of memory consolidation, it has been shown that, while the hippocampus is mainly involved in consolidating and recalling recent episodic-like memories, some cortical regions, including prelimbic, orbitofrontal, and anterior cingulate areas, are involved preferentially with remote, well-consolidated memory traces (Frankland et al. 2004;Maviel et al. 2004;Shan et al. 2008;Lesburgueres et al. 2011;Tse et al. 2011).The retrosplenial cortex (RSC) comprises the entire posterior cingulate cortex in rodents (Vogt and Peters 1981) and is one of the largest cortical areas in the rat. Situated at the crossroads between the hippocampal formation and many neocortical areas, it has attracted much attention especially for its involvement in cognition (Vann et al. 2009). Although RSC inactivation produces memory impairments similar to those caused by hippocampal lesions (Cooper and Mizumori 2001;Vann and Aggleton 2004), and it has been shown that RSC is activated during retrieval of contextual information and autobiographical memory (Valenstein et al. 1987, Daselaar et al. 2006), the precise function of this area is poorly understood (Ranganath and Ritchey 2012).To study the precise r...

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Section: [Supplemental Materials Is Available For This Article]supporting

confidence: 91%

“…0.05 vs. Veh; two-tailed Student's t-test, n ¼ 10 -12 per group. NMDA receptors prior to context conditioning did not affect learning (Corcoran et al 2011). Probably, other neurotransmitter receptors are involved in initial steps of memory processing in the RSC.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 76%

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

Katche¹,

Dorman²,

Slipczuk

et al. 2013

Learn. Mem.

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“…For instance, NMDAR stimulation is necessary for the retrieval or expression of spatial, inhibitory avoidance, and trace fear memory (Corcoran et al, 2011;Matus-Amat et al, 2007;Melik et al, 2006;Quinn et al, 2005;Rodrigues et al, 2001), but not contextual fear memory (Fellini et Pound sign represents significant difference relative to all other time points (ANOVA time simple main effect, Tukey test, po0.05). Yoshihara and Ichitani, 2004).…”

Section: Discussionmentioning

confidence: 99%

Role of a Hippocampal Src-Family Kinase-Mediated Glutamatergic Mechanism in Drug Context-Induced Cocaine Seeking

Xie

Arguello

Wells

et al. 2013

Neuropsychopharmacol

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Glutamatergic neurotransmission in the dorsal hippocampus (DH) is necessary for drug context-induced reinstatement of cocaineseeking behavior in an animal model of drug relapse. Furthermore, in vitro studies suggest that the Src family of tyrosine kinases critically regulates glutamatergic cellular functions within the DH. Thus, Src-family kinases in the DH may similarly control contextual cocaineseeking behavior. To test this hypothesis, rats were trained to lever press for un-signaled cocaine infusions in a distinct context followed by extinction training in a different context. Cocaine-seeking behavior (non-reinforced active lever pressing) was then assessed in the previously cocaine-paired and extinction contexts after AP5 (N-methyl-D-aspartate glutamate (NMDA) receptor (NMDAR) antagonist; 0.25 or 2.5 mg/0.5 ml/hemisphere), PP2 (Src-family kinase inhibitor; 6.25 or 62.5 ng/0.5 ml/hemisphere), Ro25-6981 (NR2B subunitcontaining NMDAR antagonist; 0.2 or 2 mg/0.5 ml/hemisphere), or vehicle administration into the DH. Administration of AP5, PP2, or Ro25-6981 into the DH dose-dependently impaired drug context-induced reinstatement of cocaine-seeking behavior relative to vehicle, without altering instrumental behavior in the extinction context or food-reinforced instrumental responding and general motor activity in control experiments. Cocaine-seeking behavior during the first 20 min of the test session in the cocaine-paired context was associated with an increase in NR2B subunit activation, and intra-DH PP2 pretreatment disrupted this relationship. Together, these findings suggest that Src-family kinase activation, NMDAR stimulation, and likely Src-family kinase-mediated NR2B subunit-containing NMDAR activation in the DH are necessary for incentive motivational and/or memory processes that promote contextual cocaine-seeking behavior.

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“…Given that RSC glutamatergic mechanisms of memory retrieval are retained at remote time points (Corcoran et al 2011), we were curious as to whether the same was true for RSC muscarinic signaling. To test this possibility, we fear conditioned two groups of mice and tested them for memory retrieval 35 d later, first drug free to ensure the memory had been retained, and then on vehicle or scopolamine the following day (Fig.…”

Section: Retrieval Of Remotely Acquired Context Memories Requires Rscmentioning

confidence: 99%

“…We selected the retrosplenial cortex (RSC) as our cortical region of interest because of its involvement in both memory formation and retrieval (Keene and Bucci 2008a;Corcoran et al 2011;Cowansage et al 2014;Kwapis et al 2015). We hypothesized that the RSC and dorsal hippocampus (DH) would similarly rely on the excitatory, postsynaptic M 1 /M 3 class of receptors in both memory formation and retrieval, and that conditional knockdown of these individual receptors would delineate the specific contribution of each.…”

mentioning

confidence: 99%

Muscarinic acetylcholine receptors act in synergy to facilitate learning and memory

et al. 2016

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Understanding how episodic memories are formed and retrieved is necessary if we are to treat disorders in which they malfunction. Muscarinic acetylcholine receptors (mAChR) in the hippocampus and cortex underlie memory formation, but there is conflicting evidence regarding their role in memory retrieval. Additionally, there is no consensus on which mAChR subtypes are critical for memory processing. Using pharmacological and genetic approaches, we found that (1) encoding and retrieval of contextual memory requires mAChR in the dorsal hippocampus (DH) and retrosplenial cortex (RSC), (2) memory formation requires hippocampal M 3 and cooperative activity of RSC M 1 and M 3, and (3) memory retrieval is more impaired by inactivation of multiple M 1 -M 4 mAChR in DH or RSC than inactivation of individual receptor subtypes. Contrary to the view that acetylcholine supports learning but is detrimental to memory retrieval, we found that coactivation of multiple mAChR is required for retrieval of both recently and remotely acquired context memories. Manipulations with higher receptor specificity were generally less potent than manipulations targeting multiple receptor subtypes, suggesting that mAChR act in synergy to regulate memory processes. These findings provide unique insight into the development of therapies for amnestic symptoms, suggesting that broadly acting, rather than receptor-specific, mAchR agonists and positive allosteric modulators may be the most effective therapeutic approach.

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NMDA Receptors in Retrosplenial Cortex Are Necessary for Retrieval of Recent and Remote Context Fear Memory

Cited by 152 publications

References 27 publications

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

Role of a Hippocampal Src-Family Kinase-Mediated Glutamatergic Mechanism in Drug Context-Induced Cocaine Seeking

Muscarinic acetylcholine receptors act in synergy to facilitate learning and memory

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