A unified theory for systems and cellular memory consolidation

Dash, Pramod K.; Slee, April; Runyan, Jason D.

doi:10.1016/j.brainresrev.2004.02.001

Cited by 64 publications

(49 citation statements)

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“…This result is functionally analogous to STM, which is formed in or upstream of the mushroom body, probably without the involvement of extrinsic neurons or structures 30,32,37 , and synaptic output from the mushroom body is required specifically for its retrieval, but not its acquisition 38,39 . Taken together, our observations support a model where memory is first acquired in the mushroom body and is then transferred to the ellipsoid body for storage during memory consolidation, in agreement with various observations from other species where memory transfer from one brain region to another may occurr 6,33,36 . Combined with other recent studies, we would propose (i) that acquisition involves an initial association of an odor and shock in and/or upstream of the mushroom body 5,10 , (ii) that STM resides in the mushroom body 30,32,37 , (iii) that MTM is acquired in mushroom body a/b neurons and persists there via recurrent activity involving the mushroom body a¢/b¢ DPM (dorsalpaired medial) neurons and the mushroom body a/b neurons themselves 40 , (iv) that LTM consolidation involves the transference of memory to the ellipsoid body and (v) that LTM retrieval requires neural activity output from the ellipsoid body and from mushroom body neurons 34 .…”

Section: Discussionsupporting

confidence: 91%

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Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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In humans and many other animals, memory consolidation occurs through multiple temporal phases and usually involves more than one neuroanatomical brain system. Genetic dissection of Pavlovian olfactory learning in Drosophila melanogaster has revealed multiple memory phases, but the predominant view holds that all memory phases occur in mushroom body neurons. Here, we demonstrate an acute requirement for NMDA receptors (NMDARs) outside of the mushroom body during long-term memory (LTM) consolidation. Targeted dsRNA-mediated silencing of Nmdar1 and Nmdar2 (also known as dNR1 or dNR2, respectively) in cholinergic R4m-subtype large-field neurons of the ellipsoid body specifically disrupted LTM consolidation, but not retrieval. Similar silencing of functional NMDARs in the mushroom body disrupted an earlier memory phase, leaving LTM intact. Our results clearly establish an anatomical site outside of the mushroom body involved with LTM consolidation, thus revealing both a distributed brain system subserving olfactory memory formation and the existence of a system-level memory consolidation in Drosophila.Pavlovian olfactory learning in Drosophila creates an elemental associative memory in a simple, accessible insect brain. This form of behavioral plasticity requires the normal function of NMDARs 1 , as is the case in other invertebrate and vertebrate species 2,3 . Memory formation in flies thereafter proceeds through several temporal phases and involves multiple biochemical cascades, which is again similar to findings from other animal models 4-6 . In particular, spaced training produces stronger, longer-lasting memory than massed training, which is a common property of memory formation 7,8 . Contrary to the fact that memory storage involves multiple anatomical regions in other animal models 9 , olfactory memory has been proposed to be stored predominantly in the mushroom body neurons 5,10 .The mushroom body is a prominent neuropillar structure in the insect central brain. Intrinsic mushroom body cells send neurites ventrally into the calyx, a region of dendritic arborization that is innervated by efferents from several different regions, including projection neurons from the antennal lobes 11 . Mushroom body axons project rostrally as a densely packed and stalk-like structure called the pedunculus to the anterior face of the brain, where they split and give rise to the dorsally projecting a and a¢ lobes and the medially projecting b, b¢ and g lobes 12 . Output neurons from the mushroom body project to many parts of the central brain. Another prominent neuropil is the central complex, which consists of four substructures, the ellipsoid body, the fan-shaped body, the nodulii and the protocerebral bridge. The central complex lies in the central brain between the pedunculi of the mushroom body and is bounded laterally by the two antennoglomerular tracts, dorsally by the pars intercerebralis, ventrally by the esophagus and the great commissure and frontally by the median bundle and the b-lobes of the mushroom bodies fronta...

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Section: Discussionsupporting

confidence: 91%

“…Consistent and complementary to this notion, consolidation of LTM remains normal when NMDAR function is disrupted in the mushroom body (Table 1). Thus, the transference of memory from one anatomical location to another as consolidation progresses to LTM appears to occur in Drosophila, as in various other species 6,9,33 .…”

Section: Discussionmentioning

confidence: 96%

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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“…However, recent experimental findings indicate that, in addition to the hippocampus, long-term memory is stored in the neocortex at the time of training ). Our findings suggest that ERK-mediated synaptic plasticity in the hippocampus and PFC is required for memory storage, and are consistent with a theoretical model (the C theory) proposed by Dash et al (2004) that long-term memory storage takes place both in the hippocampus and in the neocortex at the time of training.…”

Section: Discussionsupporting

confidence: 76%

Dopamine D1 receptors regulate protein synthesis-dependent long-term recognition memory via extracellular signal-regulated kinase 1/2 in the prefrontal cortex

Nagai¹,

Takuma²,

Kamei³

et al. 2007

Learn. Mem.

174

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Several lines of evidence suggest that extracellular signal-regulated kinase1/2 (ERK1/2) and dopaminergic system is involved in learning and memory. However, it remains to be determined if the dopaminergic system and ERK1/2 pathway contribute to cognitive function in the prefrontal cortex (PFC). The amount of phosphorylated ERK1/2 was increased in the PFC immediately after exposure to novel objects in the training session of the novel object recognition test. An inhibitor of ERK kinase impaired long-term recognition memory 24 h after the training although short-term memory tested 1 h after the training was not affected by the treatment. The dopamine D1 receptor agonist increased ERK1/2 phosphorylation in the PFC in vivo as well as in cortical neurons in vitro. Microinjection of the dopamine D1 receptor antagonist into the PFC impaired long-term recognition memory whereas the D2 receptor antagonist had no effect. Immunohistochemistry revealed that exposure to novel objects resulted in an increase in c-Fos expression in the PFC. Microinjection of the protein synthesis inhibitor anisomycin into the PFC impaired the long-term recognition memory. These results suggest that the activation of ERK1/2 following the stimulation of dopamine D1 receptors is necessary for the protein synthesis-dependent long-term retention of recognition memory in the PFC.

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“…There is significant interest in identifying the extrahippocampal substrates underlying remote memories that have become independent of the hippocampus (Hoffman and McNaughton 2002;Dash et al 2004;Frankland et al 2004;Wiltgen et al 2004;Bontempi 2005, 2006;Teixeira et al 2006;Tse et al 2007;Restivo et al 2009;Gusev and Gubin 2010;Wang and Morris 2010;Vetere et al 2011). In particular, the medial prefrontal cortex (mPFC) supports long-term expression of memories that initially depended upon the hippocampus (Takehara et al 2002(Takehara et al , 2003Takehara-Nishiuchi et al 2006;Quinn et al 2008;Takehara-Nishiuchi and McNaughton 2008).…”

mentioning

confidence: 99%

Hippocampus and medial prefrontal cortex contributions to trace and contextual fear memory expression over time

et al. 2013

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Previous work has shown that damage to the dorsal hippocampus (DH) occurring at recent, but not remote, timepoints following acquisition produces a deficit in trace conditioned fear memory expression. The opposite pattern has been observed with lesions to the medial prefrontal cortex (mPFC). The present studies address: (1) whether these lesion effects are observable within 30 d of training; (2) whether lesions of the ventral hippocampus (VH) produce temporally graded retrograde amnesia similar to DH lesions; and (3) whether the lesion-to-test interval critically contributes to these lesion deficits. In Experiment 1, excitotoxic lesions of the DH, VH, or mPFC were made at 1 or 30 d following trace fear conditioning. DH and VH lesioned animals showed a deficit in freezing to the tone at the recent, but not remote, timepoint. Medial PFC lesioned animals showed the opposite pattern. In Experiment 2, lesions to DH, VH, or mPFC were made 1 d following training, while testing occurred 30 d later. There were no deficits in freezing to the tone in any lesion condition compared to controls. These results suggest that systems consolidation of trace fear memory occurs within 30 d of acquisition, but does not depend on hippocampus -mPFC interactions during this period.

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A unified theory for systems and cellular memory consolidation

Cited by 64 publications

References 53 publications

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

Dopamine D1 receptors regulate protein synthesis-dependent long-term recognition memory via extracellular signal-regulated kinase 1/2 in the prefrontal cortex

Hippocampus and medial prefrontal cortex contributions to trace and contextual fear memory expression over time

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