Mammalian intermediate-term memory: New findings in neonate rat

Grimes, Matthew T.; Smith, Melissa; Li, Xuqin; Darby‐King, Andrea; Harley, Carolyn W.; McLean, John H.

doi:10.1016/j.nlm.2011.01.012

Cited by 18 publications

(14 citation statements)

References 45 publications

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“…Conditioning to an odor involved placing the pup on peppermint-scented bedding (300 mL peppermint extract/500 mL bedding) for 10 min (Sullivan et al 1991;Grimes et al 2011).…”

Section: Drug Injections/infusions and Odor Trainingmentioning

confidence: 99%

Epac activation initiates associative odor preference memories in the rat pup

et al. 2015

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Here we examine the role of the exchange protein directly activated by cAMP (Epac) in b-adrenergic-dependent associative odor preference learning in rat pups. Bulbar Epac agonist (8-pCPT-2-O-Me-cAMP, or 8-pCPT) infusions, paired with odor, initiated preference learning, which was selective for the paired odor. Interestingly, pairing odor with Epac activation produced both short-term (STM) and long-term (LTM) odor preference memories. Training using b-adrenergic-activation paired with odor recruited rapid and transient ERK phosphorylation consistent with a role for Epac activation in normal learning. An ERK antagonist prevented intermediate-term memory (ITM) and LTM, but not STM. Epac agonist infusions induced ERK phosphorylation in the mitral cell layer, in the inner half of the dendritic external plexiform layer, in the glomeruli and, patchily, among granule cells. Increased CREB phosphorylation in the mitral and granule cell layers was also seen. Simultaneous blockade of both ERK and CREB pathways prevented any long-term b-adrenergic activated odor preference memory, while LTM deficits associated with blocking only one pathway were prevented by stronger b-adrenergic activation. These results suggest that Epac and PKA play parallel and independent, as well as likely synergistic, roles in creating cAMP-dependent associative memory in rat pups. They further implicate a novel ERK-independent pathway in the mediation of STM by Epac.

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“…Conditioning to an odor involved placing the pup on peppermint-scented bedding (300 mL peppermint extract/500 mL bedding) for 10 min (Sullivan et al 1991;Grimes et al 2011).…”

Section: Drug Injections/infusions and Odor Trainingmentioning

confidence: 99%

Epac activation initiates associative odor preference memories in the rat pup

et al. 2015

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“…Established behavioral paradigms enable insight into the changing form as well as the persistence of odor representations over time, and physiological studies enable measurements of direct correspondence between environmental changes, behavioral performance, and the synaptic and molecular changes that occur in neural circuitry (Abraham et al, 2012, 2014; Qiu et al, 2014). In particular, odor learning exhibits varying memory durations that are related to behavioral task parameters and depend on evolving physiological substrates for short-term memory (Figure 4; McNamara et al, 2008), intermediate-term memory (Grimes et al, 2011), and long-term memory (Figure 5; Lazarini and Lledo, 2011). …”

Section: Learning In the Olfactory Bulbmentioning

confidence: 99%

“…It is characterized primarily by its dependence on protein translation but not on transcription (Sutton et al, 2001, 2002), although a separate, mechanistically distinct form of ITM in Aplysia also has been described (Sutton et al, 2004). Though the timescales of these memory phases in Aplysia differ from their mammalian analogs, a translation-dependent, transcription-independent ITM for conditioned odor preference also has been identified in neonatal rat OB (Grimes et al, 2011). Infusion of anisomycin, a translation blocker, immediately after conditioning had no effect on odor memory when the rat pups were tested one or 3 h later, but eliminated the memory when tested 5 or 20 h after conditioning.…”

Section: Molecular and Structural Mechanisms Of Learning And Memorymentioning

confidence: 99%

Properties and mechanisms of olfactory learning and memory

Tong

Peace

Cleland

2014

Front. Behav. Neurosci.

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Memories are dynamic physical phenomena with psychometric forms as well as characteristic timescales. Most of our understanding of the cellular mechanisms underlying the neurophysiology of memory, however, derives from one-trial learning paradigms that, while powerful, do not fully embody the gradual, representational, and statistical aspects of cumulative learning. The early olfactory system—particularly olfactory bulb—comprises a reasonably well-understood and experimentally accessible neuronal network with intrinsic plasticity that underlies both one-trial (adult aversive, neonatal) and cumulative (adult appetitive) odor learning. These olfactory circuits employ many of the same molecular and structural mechanisms of memory as, for example, hippocampal circuits following inhibitory avoidance conditioning, but the temporal sequences of post-conditioning molecular events are likely to differ owing to the need to incorporate new information from ongoing learning events into the evolving memory trace. Moreover, the shapes of acquired odor representations, and their gradual transformation over the course of cumulative learning, also can be directly measured, adding an additional representational dimension to the traditional metrics of memory strength and persistence. In this review, we describe some established molecular and structural mechanisms of memory with a focus on the timecourses of post-conditioning molecular processes. We describe the properties of odor learning intrinsic to the olfactory bulb and review the utility of the olfactory system of adult rodents as a memory system in which to study the cellular mechanisms of cumulative learning.

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“…Blocking mRNA transcription in the first hour posttraining, but not after, prevents 24 h LTM, while blocking mRNA translation in the first hour, but not after, prevents both intermediate-term memory (∼5 h) and 24 h LTM. Short-term memory for odor preference (<3 h) does not require protein synthesis (Grimes et al 2011).…”

mentioning

confidence: 99%

“…Here we use LMD of an OB area (see Fig. 1) that contains peppermint-responsive mitral cells (McLean et al 1999) and microarray analysis of mRNA expression near the end of the 1-h protein synthesis-sensitive period (Grimes et al 2011) to identify putative mitral cell mRNA mediators of 24 h peppermint odor memory. We examined training-related mRNA transcription occurring near the end of the first hour posttraining (50 min posttraining) at a time when protein synthesis inhibitors prevent intermediate and long-term memory expression while allowing maximal time for training-related transcription events to have been initiated (Fig.…”

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confidence: 99%

Learning-induced mRNA alterations in olfactory bulb mitral cells in neonatal rats

et al. 2020

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In the olfactory bulb, a cAMP/PKA/CREB-dependent form of learning occurs in the first week of life that provides a unique mammalian model for defining the epigenetic role of this evolutionarily ancient plasticity cascade. Odor preference learning in the week-old rat pup is rapidly induced by a 10-min pairing of odor and stroking. Memory is demonstrable at 24 h, but not 48 h, posttraining. Using this paradigm, pups that showed peppermint preference 30 min posttraining were sacrificed 20 min later for laser microdissection of odor-encoding mitral cells. Controls were given odor only. Microarray analysis revealed that 13 nonprotein-coding mRNAs linked to mRNA translation and splicing and 11 protein-coding mRNAs linked to transcription differed with odor preference training. MicroRNA23b, a translation inhibitor of multiple plasticity-related mRNAs, was down-regulated. Protein-coding transcription was up-regulated for Sec23b, Clic2, Rpp14, Dcbld1, Magee2, Mstn, Fam229b, RGD1566265, and Mgst2. Gng12 and Srcg1 mRNAs were down-regulated. Increases in Sec23b, Clic2, and Dcbld1 proteins were confirmed in mitral cells in situ at the same time point following training. The protein-coding changes are consistent with extracellular matrix remodeling and ryanodine receptor involvement in odor preference learning. A role for CREB and AP1 as triggers of memory-related mRNA regulation is supported. The small number of gene changes identified in the mitral cell input/output link for 24 h memory will facilitate investigation of the nature, and reversibility, of changes supporting temporally restricted long-term memory.

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Mammalian intermediate-term memory: New findings in neonate rat

Cited by 18 publications

References 45 publications

Epac activation initiates associative odor preference memories in the rat pup

Epac activation initiates associative odor preference memories in the rat pup

Properties and mechanisms of olfactory learning and memory

Learning-induced mRNA alterations in olfactory bulb mitral cells in neonatal rats

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