Taste memory: The role of protein synthesis in gustatory cortex

Rosenblum, Kobi; Meiri, Noam; Dudai, Yadin

doi:10.1016/0163-1047(93)91145-d

Cited by 278 publications

(306 citation statements)

References 22 publications

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“…This proposal agrees with conditioned taste aversion data in the adult where the amnesic effect of protein synthesis inhibition is always obtained with treatment delivered before the end of training (Tucker and Oei 1982;Rosenblum et al 1993;Houpt and Berlin 1999;Berman and Dudai 2001). These data, taken together with the results of the present experiments, suggest that the trainingto-treatment time window for impairing long-term memory of conditioned aversion is very short in the adult.…”

Section: Discussionsupporting

confidence: 81%

The temporal dynamics of consolidation and reconsolidation decrease during postnatal development

Languille¹,

Gruest²,

Richer³

et al. 2008

Learn. Mem.

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The temporal dynamics of consolidation and reconsolidation of taste/odor aversion memory are evaluated during rat pup growth at postnatal days 3, 10, and 18. This is assessed through the temporal gradients of efficacy of a protein synthesis inhibitor (anisomycin) in inducing amnesia after either acquisition (consolidation) or reactivation (reconsolidation). The results show a progressive reduction with age of the delay during which the inhibitor is able to induce amnesia. Control experiments rule out a reduction of anisomycin efficacy due to blood brain barrier growth or decrease in protein synthesis inhibition. Thus, these results present the first evidence that the protein synthesis-dependent phase of memory stabilization requires less time with age. This decrease occurs in parallel for consolidation and reconsolidation. Such changes in the dynamics of memory processing could contribute to the cognitive improvement associated with development.Neurobiological changes occurring during development have been extensively explored, but the functional consequences of these changes for cognition are still not well understood. Research on cognitive development has demonstrated very early learning capacities in vertebrates; different kinds of associative learning may be acquired by neonates and even by the fetus (Smotherman et al. 1982;Kehoe and Blass 1986;Cheslock et al. 2000;Sullivan 2001;Smotherman 2002;Gruest et al. 2004a;Shionoya et al. 2006). Some of these early acquisitions have been shown to be retained in the long term, but the characteristics of long-term memory in the course of development are still poorly known, particularly concerning its stabilization.In the adult, it is well known that memory stabilization is not instantaneous but requires time for the biological processes involved. To be stored in the long term, the memory trace must be consolidated (McGaugh 1966(McGaugh , 2000 and this consolidation requires new protein synthesis (Davis and Squire 1984). Thus, protein synthesis inhibitors given at the time of acquisition, or just afterward, cause amnesia by blocking consolidation. Recently, numerous experiments have enriched this notion by showing that retrieval of a previously consolidated memory induces a new period of lability and that stabilization of the memory in the long term requires a new wave of protein synthesis (for reviews, see Despite the theoretical importance of consolidation and reconsolidation, little is known about the emergence of these characteristics of memory during development. We have recently shown that consolidation and reconsolidation can be detected in the neonate and so may be considered as innate properties of memory processing (Gruest et al. 2004b). However, that does not rule out any possibilities of ontogenetic modifications of these memory characteristics. An indication of this possibility is that retrograde amnesia may be induced in the pup one hour after conditioned aversion training, a delay which has never been observed in the adult in the same kind of learning. Th...

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Section: Discussionsupporting

confidence: 81%

The temporal dynamics of consolidation and reconsolidation decrease during postnatal development

Languille¹,

Gruest²,

Richer³

et al. 2008

Learn. Mem.

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“…Doses of anisomycin (Sigma) were selected on the basis of previous findings (43), showing >90% inhibition of protein synthesis in cortex for 2 h. Anisomycin was dissolved in a solution of 40% DMSO, brought to pH 7, and then diluted with 0.9% saline solution. The doses used in this experiment were 25, 50, and 100 μg per side.…”

Section: Methodsmentioning

confidence: 99%

Ventral striatal plasticity and spatial memory

Ferretti

Roullet

Sargolini

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Spatial memory formation is a dynamic process requiring a series of cellular and molecular steps, such as gene expression and protein translation, leading to morphological changes that have been envisaged as the structural bases for the engram. Despite the role suggested for medial temporal lobe plasticity in spatial memory, recent behavioral observations implicate specific components of the striatal complex in spatial information processing. However, the potential occurrence of neural plasticity within this structure after spatial learning has never been investigated. In this study we demonstrate that blockade of cAMP response element binding protein-induced transcription or inhibition of protein synthesis or extracellular proteolytic activity in the ventral striatum impairs longterm spatial memory. These findings demonstrate that, in the ventral striatum, similarly to what happens in the hippocampus, several key molecular events crucial for the expression of neural plasticity are required in the early stages of spatial memory formation. T he formation of long-term memories is believed to involve a dynamic process by which a labile memory is progressively converted into a more stable and potentially permanent trace. Evidence for such a time-dependent process comes from studies demonstrating that electroconvulsive shock produces amnesia only if delivered shortly after learning, whereas the same treatment is ineffective when delivered several hours later (1). Long-term memory is accompanied by changes in neuronal morphology and connectivity, and these alterations are thought to be essential for the stabile encoding of new information (2). This transformation has been suggested to depend upon plastic changes that involve a sequence of specific and coordinated cellular processes. These begin with neurotransmitter receptor activation that induces shortterm changes in synaptic efficacy based on receptor phosphorylation and trafficking (3, 4). Subsequently, alterations in gene expression and protein synthesis occur that are the basis for longterm structural modifications (5, 6).A key issue in the study of memory in vertebrates is the brain site at which these processes occur. Clinical evidence in humans suggests that structures within the medial temporal lobe (MTL) play a prominent role in long-term memories. MTL lesions induce profound deficits in the formation of long-lasting declarative memories while sparing the acquisition of nondeclarative memories such as visual-motor skills (7,8). Such findings suggest that the hippocampus might be an essential site where plasticity occurs in the initial steps of declarative memory stabilization. Accordingly, those molecular events thought to be crucial for the long-term encoding of memories such as regulation of gene expression and protein synthesis, as well as structural changes, have been described in the hippocampus after spatial learning (6, 9, 10).Recent experimental evidence, however, demonstrates that structures different from the hippocampus might also be involved in ...

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“…Arguing against this notion is an accumulating literature which shows that CTA learning has fundamental similarities with other associative learning paradigms, including a short-term and long-term memory phase (25,26) and heavy reliance on signaling pathways such as cAMP response element-binding (CREB) protein (27) and protein kinase A (PKA) (28) in the amygdala. Interestingly, the lateral amygdala has been proposed as the site of CS-US association in another adaptive, defensive associative learning task, cued fear conditioning (2,6,29,30), suggesting that a population of glutamatergic neurons in this region of the amygdala has specialized properties that support rapid neuronal plasticity.…”

Section: Us Responses Are Enhanced For Forward-conditioned (Cs-us) Anmentioning

confidence: 99%

Visualizing stimulus convergence in amygdala neurons during associative learning

Barot

Kyono

Clark

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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A central feature of models of associative memory formation is the reliance on information convergence from pathways responsive to the conditioned stimulus (CS) and unconditioned stimulus (US). In particular, cells receiving coincident input are held to be critical for subsequent plasticity. Yet identification of neurons in the mammalian brain that respond to such coincident inputs during a learning event remains elusive. Here we use Arc cellular compartmental analysis of temporal gene transcription by fluorescence in situ hybridization (catFISH) to locate populations of neurons in the mammalian brain that respond to both the CS and US during training in a one-trial learning task, conditioned taste aversion (CTA). Individual neurons in the basolateral nucleus of the amygdala (BLA) responded to both the CS taste and US drug during conditioning. Coincident activation was not evident, however, when stimulus exposure was altered so as to be ineffective in promoting learning (backward conditioning, latent inhibition). Together, these data provide clear visualization of neurons in the mammalian brain receiving convergent information about the CS and US during acquisition of a learned association.Arc ͉ memory ͉ novelty ͉ plasticity ͉ taste aversion conditioning A central issue in behavioral neuroscience is how alterations in neural activity mediate the durable behavioral changes involved in learning. Current concepts of associative memory formation are based on the premise that plasticity relies on convergence of information from pathways responsive to the conditioned stimulus (CS) and the unconditioned stimulus (US) (1-3). Yet despite impressive progress in defining underlying neuronal circuitry and probable sites of association for several associative learning models (2, 4-6), identification of neuronal populations where convergent activation actually occurs during learning remains elusive. Electrophysiological studies have made inroads toward this goal, but are hampered by limited sampling ability, especially when the targets are convergent neurons, which are likely to be sparsely distributed during any single training trial. In those studies where convergent activation was recorded, animals were either anesthetized or had already reached asymptotic performance on a learning task (5-7).The imaging method known as cellular compartmental analysis of temporal gene transcription by fluorescence in situ hybridization (catFISH) can circumvent several of the technical limitations that have made it difficult to sample broad regions of the mammalian brain with high cellular and temporal resolution during a learning event (8). In particular, catFISH serves as a functional imager that allows investigators to distinguish neuronal populations activated by two distinct behavioral experiences. CatFISH utilizes Arc (or Arg 3.1), an immediate early gene (IEG) that is expressed in forebrain glutamatergic neurons after periods of enhanced activation (9, 10). The innovative features of catFISH rely on the time course of Arc mRNA locali...

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Taste memory: The role of protein synthesis in gustatory cortex

Cited by 278 publications

References 22 publications

The temporal dynamics of consolidation and reconsolidation decrease during postnatal development

The temporal dynamics of consolidation and reconsolidation decrease during postnatal development

Ventral striatal plasticity and spatial memory

Visualizing stimulus convergence in amygdala neurons during associative learning

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