Altered AMPA receptor expression plays an important role in inducing bidirectional synaptic plasticity during contextual fear memory reconsolidation

Bhattacharya, Subhrajit; Kimble, Whitney; Buabeid, Manal; Bhattacharya, Dwipayan; Bloemer, Jenna; Alhowail, Ahmad; Reed, Miranda N.; Dhanasekaran, Muralikrishnan; Escobar, Martha; Suppiramaniam, Vishnu

doi:10.1016/j.nlm.2016.12.013

Cited by 30 publications

(36 citation statements)

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“…The action of Aβ oligomers on LTP is mediated through the potentiation of extrasynaptic NMDA receptors and consecutive calcium influx, which is associated with a loss of AMPA receptors at the synapse [53, 54]. In addition, researchers in several studies reported that loss of memory is associated with reductions of expression of AMPA receptor family members [55]. Therefore, we investigated the relationship between the OLE and ARA diets and the expression levels of these receptors in Western blotting and ELISA experiments.…”

Section: Discussionmentioning

confidence: 99%

Dietary arachidonic acid increases deleterious effects of amyloid-β oligomers on learning abilities and expression of AMPA receptors: putative role of the ACSL4-cPLA2 balance

et al. 2017

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BackgroundPolyunsaturated fatty acids play a crucial role in neuronal function, and the modification of these compounds in the brain could have an impact on neurodegenerative diseases such as Alzheimer’s disease. Despite the fact that arachidonic acid is the second foremost polyunsaturated fatty acid besides docosahexaenoic acid, its role and the regulation of its transfer and mobilization in the brain are poorly known.MethodsTwo groups of 39 adult male BALB/c mice were fed with an arachidonic acid-enriched diet or an oleic acid-enriched diet, respectively, for 12 weeks. After 10 weeks on the diet, mice received intracerebroventricular injections of either NaCl solution or amyloid-β peptide (Aβ) oligomers. Y-maze and Morris water maze tests were used to evaluate short- and long-term memory. At 12 weeks on the diet, mice were killed, and blood, liver, and brain samples were collected for lipid and protein analyses.ResultsWe found that the administration of an arachidonic acid-enriched diet for 12 weeks induced short-term memory impairment and increased deleterious effects of Aβ oligomers on learning abilities. These cognitive alterations were associated with modifications of expression of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors, postsynaptic density protein 95, and glial fibrillary acidic protein in mouse cortex or hippocampus by the arachidonic acid-enriched diet and Aβ oligomer administration. This diet also led to an imbalance between the main ω-6 fatty acids and the ω-3 fatty acids in favor of the first one in erythrocytes and the liver as well as in the hippocampal and cortical brain structures. In the cortex, the dietary arachidonic acid also induced an increase of arachidonic acid-containing phospholipid species in phosphatidylserine class, whereas intracerebroventricular injections modified several arachidonic acid- and docosahexaenoic acid-containing species in the four phospholipid classes. Finally, we observed that dietary arachidonic acid decreased the expression of the neuronal form of acyl-coenzyme A synthetase 4 in the hippocampus and increased the cytosolic phospholipase A2 activation level in the cortices of the mice.ConclusionsDietary arachidonic acid could amplify Aβ oligomer neurotoxicity. Its consumption could constitute a risk factor for Alzheimer’s disease in humans and should be taken into account in future preventive strategies. Its deleterious effect on cognitive capacity could be linked to the balance between arachidonic acid-mobilizing enzymes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13195-017-0295-1) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Dietary arachidonic acid increases deleterious effects of amyloid-β oligomers on learning abilities and expression of AMPA receptors: putative role of the ACSL4-cPLA2 balance

et al. 2017

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“…When induced by presentation of a novel object, reconsolidation mediates integration of new information into the reactivated ORM trace and is controlled by BDNF (Radiske et al, 2017b) and accompanied by a brief early post-RA depotentiation period followed by a late stage of synaptic efficacy enhancement (Clarke et al, 2010). Because PKM controls the facilitatory effect of BDNF on hippocampal LTP (Mei et al, 2011) and both PKM and BDNF regulate AMPAR surface expression during synaptic potentiation (Caldeira et al, 2007;Yao et al, 2008;Jourdi and Kabbaj, 2013), which seems necessary for reconsolidation (Rao-Ruiz et al, 2011;Bhattacharya et al, 2017), we hypothesized that PKM modulates ORM reconsolidation by mediating the interplay between BDNF and AMPAR recycling, so its inhibition after retrieval in the presence of a novel object impairs ORM reconsolidation and causes amnesia by deleting the reactivated recognition memory trace.…”

Section: Introductionmentioning

confidence: 99%

PKMζ Inhibition Disrupts Reconsolidation and Erases Object Recognition Memory

et al. 2019

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Object recognition memory (ORM) confers the ability to discriminate the familiarity of previously encountered items. Reconsolidation is the process by which reactivated memories become labile and susceptible to modifications. The hippocampus is specifically engaged in reconsolidation to integrate new information into the original ORM through a mechanism involving activation of brain-derived neurotrophic factor (BDNF) signaling and induction of LTP. It is known that BDNF can control LTP maintenance through protein kinase M (PKM), an atypical protein kinase C isoform that is thought to sustain memory storage by modulating glutamatergic neurotransmission. However, the potential involvement of PKM in ORM reconsolidation has never been studied. Using a novel ORM task combined with pharmacological, biochemical, and electrophysiological tools, we found that hippocampal PKM is essential to update ORM through reconsolidation, but not to maintain the inactive recognition memory trace stored over time, in adult male Wistar rats. Our results also indicate that hippocampal PKM acts downstream of BDNF and controls AMPAR synaptic insertion to elicit reconsolidation and suggest that blocking PKM activity during this process deletes active ORM.

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“…The process involved in the retrieval and subsequent reconsolidation of the drug memories involves AMPARs trafficking and functional synaptic plasticity ( Van den Oever et al , 2008 ). In the studies on retrieval of contextual fear memory, it has been reported that GluA2 undergoes endocytosis, a process associated with a decrease in AMPAR miniature excitatory postsynaptic currents ( Rao-Ruiz et al , 2011 ) and an enhancement of LTD ( Bhattacharya et al , 2016 ). In a study on cue-induced reinstatement of heroin seeking, it has been reported that this reinstatement causes GluA2 endocytosis and a decrease in AMPA/NMDA current ratios in the mPFC ( Van den Oever et al , 2008 ).…”

Section: Discussionmentioning

confidence: 99%

Role of Glutamatergic Projections from the Ventral CA1 to Infralimbic Cortex in Context-Induced Reinstatement of Heroin Seeking

Wang

Cui

et al. 2017

Neuropsychopharmacol.

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The prelimbic cortex (PL) and infralimbic cortex (IL) play a role in context-induced reinstatement of heroin seeking in an animal model of drug relapse. Both the PL and IL receive direct glutamatergic projections from the ventral CA1 (vCA1), which is also involved in context-induced reinstatement of cocaine and heroin seeking. Here we studied the role of vCA1-PL and vCA1-IL projections in context-induced reinstatement of heroin seeking by using electrophysiological, neuropharmacological, chemogenetic, and molecular methods. We showed that context-induced reinstatement of heroin seeking caused selective activation of the vCA1-IL but not vCA1-PL glutamatergic projections, decreased synaptosomal GluA2 expression in the IL, impaired basal synaptic transmission, and facilitation of long-term depression (LTD) in the vCA1-IL pathway. Additionally, chemogenetic inactivation of the vCA1-IL but not vCA1-PL pathway decreased context-induced reinstatement of heroin seeking. Inactivation of the vCA1-IL pathway also reversed synaptosomal GluA2 downregulation and basal transmission reduction, and blocked LTD induction. Taken together, our results demonstrate a critical role of the vCA1-IL glutamatergic projection in context-induced reinstatement of heroin seeking in a rat model of drug relapse.

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Altered AMPA receptor expression plays an important role in inducing bidirectional synaptic plasticity during contextual fear memory reconsolidation

Cited by 30 publications

References 45 publications

Dietary arachidonic acid increases deleterious effects of amyloid-β oligomers on learning abilities and expression of AMPA receptors: putative role of the ACSL4-cPLA2 balance

Dietary arachidonic acid increases deleterious effects of amyloid-β oligomers on learning abilities and expression of AMPA receptors: putative role of the ACSL4-cPLA2 balance

PKMζ Inhibition Disrupts Reconsolidation and Erases Object Recognition Memory

Role of Glutamatergic Projections from the Ventral CA1 to Infralimbic Cortex in Context-Induced Reinstatement of Heroin Seeking

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