The fate of hippocampal synapses depends on the sequence of plasticity-inducing events

Pulin, Mauro; Gee, Christine E.; Oertner, Thomas G.

doi:10.7554/elife.39151

Cited by 25 publications

(26 citation statements)

References 55 publications

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“…Neuroarchitectural changes would provide a substrate for the construction of longer-term dynamic memory support with repeated spaced training. A distinction between transient functional changes and more enduring structural changes with LTP has A B1 B2 recently been proposed in another model plasticity system (Wiegert et al 2018). The week-old rat pup OB offers a highly tractable model for illuminating the biology of mammalian learning and memory.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

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

et al. 2020

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“…LTP is thought to result from faciliatory stimulation protocols, such as 10 Hz rTMS, whereas LTD seems to result from inhibitory protocols, such as cTBS. A recently published study ( Wiegert et al, 2018 ) showed that optogenetically induced LTP in rat hippocampus enhances synaptic stability over days, whereas long-term depression (LTD) destabilizes synapses. Most potentiated synapses are resistant to depression suggesting that synaptic transmission strength depends on the sequence of plasticity-inducing stimulations ( Wiegert et al, 2018 ).…”

Section: Discussionmentioning

confidence: 99%

“…A recently published study ( Wiegert et al, 2018 ) showed that optogenetically induced LTP in rat hippocampus enhances synaptic stability over days, whereas long-term depression (LTD) destabilizes synapses. Most potentiated synapses are resistant to depression suggesting that synaptic transmission strength depends on the sequence of plasticity-inducing stimulations ( Wiegert et al, 2018 ). High stimulation load induced by multiple rTMS/tDCS sessions may enhance the stabilizing effect on synaptic transmission in stimulated cortical areas, such as the DLPFC, with potentially larger effects on corresponding behavior.…”

Section: Discussionmentioning

confidence: 99%

Invasive and Non-invasive Stimulation of the Obese Human Brain

Pleger

2018

Front. Neurosci.

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Accumulating evidence suggests that non-invasive and invasive brain stimulation may reduce food craving and calorie consumption rendering these techniques potential treatment options for obesity. Non-invasive transcranial direct current stimulation (tDCS) or repetitive transcranial magnet stimulation (rTMS) are used to modulate activity in superficially located executive control regions, such as the dorsolateral prefrontal cortex (DLPFC). Modulation of the DLPFC’s activity may alter executive functioning and food reward processing in interconnected dopamine-rich regions such as the striatum or orbitofrontal cortex. Modulation of reward processing can also be achieved by invasive deep brain stimulation (DBS) targeting the nucleus accumbens. Another target for DBS is the lateral hypothalamic area potentially leading to improved energy expenditure. To date, available evidence is, however, restricted to few exceptional cases of morbid obesity. The vagal nerve plays a crucial role in signaling the homeostatic demand to the brain. Invasive or non-invasive vagal nerve stimulation (VNS) is thus assumed to reduce appetite, rendering VNS another possible treatment option for obesity. Based on currently available evidence, the U.S. Food and Drug Administration recently approved VNS for the treatment of obesity. This review summarizes scientific evidence regarding these techniques’ efficacy in modulating food craving and calorie intake. It is time for large controlled clinical trials that are necessary to translate currently available research discoveries into patient care.

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“…The majority of excitatory synapses on neuronal dendrites are located on small membranous protrusions called dendritic spines. Spines are highly dynamic structures that can undergo extensive morphological changes, appear, disappear or become stabilized over long periods of time (weeks and months), depending on the type of synaptic input they receive (Wiegert et al, 2018). The structural plasticity of dendritic spines depends on the tight regulation of spinous Ca 2+ -signaling, and on local, activity-dependent protein and membrane turnover.…”

Section: Introductionmentioning

confidence: 99%

Synaptic anchoring of the endoplasmic reticulum depends on myosin V and caldendrin activity

Konietzny

Grendel

Hertrich

et al. 2020

Preprint

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Excitatory synapses of principal hippocampal neurons are frequently located on dendritic spines. The dynamic strengthening or weakening of individual inputs results in a great structural and molecular diversity of dendritic spines. Active spines with large Ca2+ transients are frequently invaded by a single protrusion from the endoplasmic reticulum (ER), which is dynamically transported into and out of spines by the actin-based motor myosin V. An increase in synaptic strength often correlates with stable anchoring of the ER, followed by the formation of the spine apparatus organelle. Here we show that synaptic ER stabilization depends on the interplay of two Ca2+-binding proteins: calmodulin serves as a light chain of myosin V and activates the motor function, whereas caldendrin acts as an inhibitor which transforms myosin into a stationary F-actin tether. Together, they provide a Ca2+-sensing module for fine-tuning myosin V activity and thereby regulate the formation of the spine apparatus in a subset of active dendritic spines.

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The fate of hippocampal synapses depends on the sequence of plasticity-inducing events

Cited by 25 publications

References 55 publications

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

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

Invasive and Non-invasive Stimulation of the Obese Human Brain

Synaptic anchoring of the endoplasmic reticulum depends on myosin V and caldendrin activity

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