Differential role of insular cortex muscarinic and NMDA receptors in one-trial appetitive taste learning

Parkes, Shauna L.; Cruz, Vanesa De la; Bermúdez‐Rattoni, Federico; Coutureau, Étienne; Ferreira, Guillaume

doi:10.1016/j.nlm.2014.09.008

Cited by 19 publications

(15 citation statements)

References 34 publications

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“…In order to dissociate between these possibilities, we investigated the role of NMDAR and CaMKIIa in non-associative incidental and associative CTA learning by micro-infusing the NMDAR antagonist APV (10 mg/1 ml/hemisphere) or CaMKIIa inhibitor TatCN21 (0.3 nM/1 ml/ hemisphere (Buard et al, 2010)) bilaterally into the IC. Consistent with the literature, our data reveal that NDMAR in the IC is dispensable for incidental taste learning but necessary for CTA learning (Figure 3-figure supplement 1) (Rosenblum et al, 1997;Barki-Harrington et al, 2009;Parkes et al, 2014). We also found that CaMKIIa in the IC is dispensable for incidental taste learning but necessary for CTA learning (Figure 3-figure supplement 1,2).…”

Section: Resultssupporting

confidence: 90%

“…It is possible that NMDAR activation is upstream to CaMKIIa phosphorylation, because activation of NMDAR in the IC is crucial for taste-malaise association and NMDAR regulates CaMKIIa phosphorylation (Rosenblum et al, 1997;Ferreira et al, 2002;Sanhueza et al, 2011;Halt et al, 2012;Parkes et al, 2014). Therefore, we examined if NMDAR activation is necessary for novel taste-dependent CaMKIIa activation.…”

Section: Resultsmentioning

confidence: 99%

“…It is important to note that NMDAR-CaMKIIa-AMPAR in the IC are not necessary for incidental taste learning and memory, whereas muscarinic receptors are critical for incidental taste learning (Ferreira et al, 2002;Parkes et al, 2014). It is interesting that different molecular mechanisms take place in the same cortex, the insular cortex, to mediate associative and non-associative taste learning and memory.…”

Section: Resultsmentioning

confidence: 99%

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Author response: A molecular mechanism underlying gustatory memory trace for an association in the insular cortex

Adaikkan

Rosenblum

2015

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Events separated in time are associatively learned in trace conditioning, recruiting more neuronal circuits and molecular mechanisms than in delay conditioning. However, it remains unknown whether a given sensory memory trace is being maintained as a unitary item to associate. Here, we used conditioned taste aversion learning in the rat model, wherein animals associate a novel taste with visceral nausea, and demonstrate that there are two parallel memory traces of a novel taste: a short-duration robust trace, lasting approximately 3 hr, and a parallel long-duration weak one, lasting up to 8 hr, and dependent on the strong trace for its formation. Moreover, only the early robust trace is maintained by a NMDAR-dependent CaMKII-AMPAR pathway in the insular cortex. These findings suggest that a memory trace undergoes rapid modifications, and that the mechanisms underlying trace associative learning differ when items in the memory are experienced at different time points.

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Section: Resultssupporting

confidence: 90%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Author response: A molecular mechanism underlying gustatory memory trace for an association in the insular cortex

Adaikkan

Rosenblum

2015

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“…Importantly, gustatory cortical neurons can also exhibit anticipatory responses preceding the unavoidable delivery of a pleasant or unpleasant tastant following classical conditioning (Gardner and Fontanini 2014). The circuit mechanisms underlying this physiological plasticity remain poorly understood, but cholinergic projections to the GC are necessary for the taste aversion learning to occur (Gutierrez et al 2003;Parkes et al 2014). As in the auditory system, there is growing evidence that the gustatory thalamus also exhibits associative plasticity and may mediate the learned responses to taste-predictive auditory cues in the GC (Samuelsen et al 2013).…”

Section: Associative Plasticity In Other Sensory Systemsmentioning

confidence: 99%

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

McGann

2015

Learn. Mem.

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Historically, the body's sensory systems have been presumed to provide the brain with raw information about the external environment, which the brain must interpret to select a behavioral response. Consequently, studies of the neurobiology of learning and memory have focused on circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulus-specific changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. This review synthesizes evidence across sensory modalities to report emerging themes, including the systems' flexibility to emphasize different aspects of a sensory stimulus depending on its predictive features and ability of different forms of learning to produce similar plasticity in sensory structures. Potential functions of this learning-induced neuroplasticity are discussed in relation to the challenges faced by sensory systems in changing environments, and evidence for absolute changes in sensory ability is considered. We also emphasize that this plasticity may serve important nonsensory functions, including balancing metabolic load, regulating attentional focus, and facilitating downstream neuroplasticity.

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“…Therefore, we suggest that NMDA receptors activity is not involved in the expression of taste aversion but instead trigger other memory events, like reconsolidation and information updating during CTA retrieval. In this regard, the activation of NMDA receptors is required for the establishment (Ferreira et al 2005, Parkes et al 2014, consolidation (Escobar and Bermú dez-Rattoni 2000;Guzmán-Ramos et al 2010), and reconsolidation (Garcia-Delatorre et al 2014) of CTA memory. Moreover, it has been observed that NMDA receptors activation in the IC is necessary to maintain the short taste memory trace for the ulterior association with gastric malaise (Adaikkan and Rosenblum 2015).…”

Section: Discussionmentioning

confidence: 99%

Memory trace reactivation and behavioral response during retrieval are differentially modulated by amygdalar glutamate receptors activity: interaction between amygdala and insular cortex

2016

Self Cite

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The insular cortex (IC) is required for conditioned taste aversion (CTA) retrieval. However, it remains unknown which cortical neurotransmitters levels are modified upon CTA retrieval. Using in vivo microdialysis, we observed that there were clear elevations in extracellular glutamate, norepinephrine, and dopamine in and around the center of the gustatory zone of the IC during CTA retrieval. Additionally, it has been reported that the amygdala-IC interaction is highly involved in CTA memory establishment. Therefore, we evaluated the effects of infusions of an AMPA receptor antagonist (CNQX) and a NMDA receptor antagonist (APV) into the amygdala on CTA retrieval and IC neurotransmitter levels. Infusion of APV into the amygdala impaired glutamate augmentation within the IC, whereas dopamine and norepinephrine levels augmentation persisted and a reliable CTA expression was observed. Conversely, CNQX infusion into the amygdala impaired the aversion response, as well as norepinephrine and dopamine augmentations in the IC. Interestingly, CNQX infusion did not affect glutamate elevation in the IC. To evaluate the functional meaning of neurotransmitters elevations within the IC on CTA response, we infused specific antagonists for the AMPA, NMDA, D1, and β-adrenergic receptor before retrieval. Results showed that activation of AMPA, D1, and β-adrenergic receptors is necessary for CTA expression, whereas NMDA receptors are not involved in the aversion response.

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Differential role of insular cortex muscarinic and NMDA receptors in one-trial appetitive taste learning

Cited by 19 publications

References 34 publications

Author response: A molecular mechanism underlying gustatory memory trace for an association in the insular cortex

Author response: A molecular mechanism underlying gustatory memory trace for an association in the insular cortex

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

Memory trace reactivation and behavioral response during retrieval are differentially modulated by amygdalar glutamate receptors activity: interaction between amygdala and insular cortex

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