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Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Neurobiology".

Deadline for manuscript submissions: closed (30 April 2022) | Viewed by 19548

Special Issue Editors

Prof. Dr. Efthimios M. C. Skoulakis

E-Mail Website
Guest Editor
Institute for Fundamental Biomedical Research, Biomedical Sciences Research Center “Alexander Fleming”, 16672 Vari, Greece
Interests: mechanisms of habituation; associative learning and memory in Drosophila and mice; pharmacogenetics of neurodegenerative tauopathies; learning disabilities and psychiatric conditions in Drosophila models
Special Issues, Collections and Topics in MDPI journals
Prof. Dr. Antonis Stamatakis

E-Mail Website
Guest Editor
Biology-Biochemistry Lab, Faculty of Nursing, National and Kapodistrian University of Athens, Athens, Greece
Interests: behavioural neuroscience; behaviour (using rodents as experimental animals); mechanisms of learning and memory, maternal behaviour, sex differences in stress responses, epigenetic effects of early life experiences on neonatal and adult brain structure

Special Issue Information

Dear Colleagues,

Learning and memory are sub-served by distinct processes, such as encoding, consolidation storage, retrieval and modulation of the mnemonic engram. Although the cellular and molecular events underlying these processes have been extensively studied, the precise mechanisms differentiating them and the neural codes employed are currently, at best, fragmentary.

The circuitry and molecular mechanisms potentially differentially engaged, and hence characterizing distinct types of learning and memory forms (e.g., episodic, emotional, procedural, working, non-associative), are little understood to date. The role of neuronal population oscillatory dynamics, the orchestration of activities of different neurotransmitters and neuromodulators—including the effects of stress or gonadal hormones—the intracellular signaling pathways engaged, or the epigenetic and epitranscriptomic modifications imposed by learning and being connected with memory are intensely studied, but much remains unexplored.

We invite contributions of original research papers, computational models, and reviews, as well as position/theoretical papers. Studies combining experimental approaches, including genetic/epigenetic interventions, cellular, biochemical, molecular, –omics analyses, optogenetic manipulations or behavioral assays, are encouraged. Reviews and position/theoretical papers addressing their themes in a comparative approach, across memory types, neuronal modalities or experimental species, are welcome.

Prof. Efthimios M.C. Skoulakis
Prof. Dr. Antonis Stamatakis
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. There is an Article Processing Charge (APC) for publication in this open access journal. For details about the APC please see here. Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • learning
  • memory
  • neuronal
  • neurotransmitters
  • neuromodulators
  • epigenetic
  • epitranscriptomic modifications

Published Papers (7 papers)

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Editorial

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2 pages, 158 KiB  
Editorial
Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory
by Antonis Stamatakis and Efthimios M. C. Skoulakis
Int. J. Mol. Sci. 2023, 24(1), 206; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24010206 - 22 Dec 2022
Viewed by 839
Abstract
The ability to learn from the consequences of one’s actions, extracting useful information from threatening, painful or rewarding encounters and developing the skill of predicting probable events from pre-experienced stimuli, is essential for survival and reproductive success [...] Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)

Research

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22 pages, 4275 KiB  
Article
Impact of Autophagy Impairment on Experience- and Diet-Related Synaptic Plasticity
by Ulyana Lalo, Ioannis P. Nezis and Yuriy Pankratov
Int. J. Mol. Sci. 2022, 23(16), 9228; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23169228 - 17 Aug 2022
Cited by 4 | Viewed by 1664
Abstract
The beneficial effects of diet and exercise on brain function are traditionally attributed to the enhancement of autophagy, which plays a key role in neuroprotection via the degradation of potentially harmful intracellular structures. The molecular machinery of autophagy has also been suggested to [...] Read more.
The beneficial effects of diet and exercise on brain function are traditionally attributed to the enhancement of autophagy, which plays a key role in neuroprotection via the degradation of potentially harmful intracellular structures. The molecular machinery of autophagy has also been suggested to influence synaptic signaling via interaction with trafficking and endocytosis of synaptic vesicles and proteins. Still, the role of autophagy in the regulation of synaptic plasticity remains elusive, especially in the mammalian brain. We explored the impact of autophagy on synaptic transmission and homeostatic and acute synaptic plasticity using transgenic mice with induced deletion of the Beclin1 protein. We observed down-regulation of glutamatergic and up-regulation of GABAergic synaptic currents and impairment of long-term plasticity in the neocortex and hippocampus of Beclin1-deficient mice. Beclin1 deficiency also significantly reduced the effects of environmental enrichment, caloric restriction and its pharmacological mimetics (metformin and resveratrol) on synaptic transmission and plasticity. Taken together, our data strongly support the importance of autophagy in the regulation of excitatory and inhibitory synaptic transmission and synaptic plasticity in the neocortex and hippocampus. Our results also strongly suggest that the positive modulatory actions of metformin and resveratrol in acute and homeostatic synaptic plasticity, and therefore their beneficial effects on brain function, occur via the modulation of autophagy. Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)
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7 pages, 2874 KiB  
Communication
Cold Shock Disrupts Massed Training-Elicited Memory in Drosophila
by Anna Bourouliti and Efthimios M. C. Skoulakis
Int. J. Mol. Sci. 2022, 23(12), 6407; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23126407 - 08 Jun 2022
Cited by 2 | Viewed by 1371
Abstract
Memory consolidation is a time-dependent process occurring over hours, days, or longer in different species and requires protein synthesis. An apparent exception is a memory type in Drosophila elicited by a single olfactory conditioning episode, which ostensibly consolidates quickly, rendering it resistant to [...] Read more.
Memory consolidation is a time-dependent process occurring over hours, days, or longer in different species and requires protein synthesis. An apparent exception is a memory type in Drosophila elicited by a single olfactory conditioning episode, which ostensibly consolidates quickly, rendering it resistant to disruption by cold anesthesia a few hours post-training. This anesthesia-resistant memory (ARM), is independent of protein synthesis. Protein synthesis independent memory can also be elicited in Drosophila by multiple massed cycles of olfactory conditioning, and this led to the prevailing notion that both of these operationally distinct training regimes yield ARM. Significantly, we show that, unlike bona fide ARM, massed conditioning-elicited memory remains sensitive to the amnestic treatment two hours post-training and hence it is not ARM. Therefore, there are two protein synthesis-independent memory types in Drosophila. Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)
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18 pages, 4437 KiB  
Article
The G Protein-Coupled Serotonin 1A Receptor Augments Protein Kinase Cε-Mediated Neurogenesis in Neonatal Mouse Hippocampus—PKCε-Mediated Signaling in the Early Hippocampus
by Sreyashi Samaddar, Sudarshana Purkayastha, Souleymane Diallo, Subramanyam J. Tantry, Ryan Schroder, Pranavan Chanthrakumar, Michael J. Flory and Probal Banerjee
Int. J. Mol. Sci. 2022, 23(4), 1962; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23041962 - 10 Feb 2022
Cited by 1 | Viewed by 1769
Abstract
The neurotransmitter serotonin (5-HT) plays an important role in mood disorders. It has been demonstrated that 5-HT signaling through 5-HT1A receptors (5-HT1A-R) is crucial for early postnatal hippocampal development and later-life behavior. Although this suggests that 5-HT1A-R signaling [...] Read more.
The neurotransmitter serotonin (5-HT) plays an important role in mood disorders. It has been demonstrated that 5-HT signaling through 5-HT1A receptors (5-HT1A-R) is crucial for early postnatal hippocampal development and later-life behavior. Although this suggests that 5-HT1A-R signaling regulates early brain development, the mechanistic underpinnings of this process have remained unclear. Here we show that stimulation of the 5-HT1A-R at postnatal day 6 (P6) by intrahippocampal infusion of the agonist 8-OH-DPAT (D) causes signaling through protein kinase Cε (PKCε) and extracellular receptor activated kinase ½ (ERK1/2) to boost neuroblast proliferation in the dentate gyrus (DG), as displayed by an increase in bromodeoxy-uridine (BrdU), doublecortin (DCX) double-positive cells. This boost in neuroproliferation was eliminated in mice treated with D in the presence of a 5-HT1A-R antagonist (WAY100635), a selective PKCε inhibitor, or an ERK1/2-kinase (MEK) inhibitor (U0126). It is believed that hippocampal neuro-progenitors undergoing neonatal proliferation subsequently become postmitotic and enter the synaptogenesis phase. Double-staining with antibodies against bromodeoxyuridine (BrdU) and neuronal nuclear protein (NeuN) confirmed that 5-HT1A-R → PKCε → ERK1/2-mediated boosted neuroproliferation at P6 also leads to an increase in BrdU-labeled granular neurons at P36. This 5-HT1A-R-mediated increase in mature neurons was unlikely due to suppressed apoptosis, because terminal deoxynucleotidyl transferase dUTP nick-end labeling analysis showed no difference in DNA terminal labeling between vehicle and 8-OH-DPAT-infused mice. Therefore, 5-HT1A-R signaling through PKCε may play an important role in micro-neurogenesis in the DG at P6, following which many of these new-born neuroprogenitors develop into mature neurons. Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)
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28 pages, 4275 KiB  
Article
Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis
by Jennifer L. Myers, Maria Porter, Nicholas Narwold, Krishna Bhat, Brigitte Dauwalder and Gregg Roman
Int. J. Mol. Sci. 2021, 22(23), 12967; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222312967 - 30 Nov 2021
Cited by 12 | Viewed by 3257
Abstract
Drosophila’s white gene encodes an ATP-binding cassette G-subfamily (ABCG) half-transporter. White is closely related to mammalian ABCG family members that function in cholesterol efflux. Mutants of white have several behavioral phenotypes that are independent of visual defects. This study characterizes a novel [...] Read more.
Drosophila’s white gene encodes an ATP-binding cassette G-subfamily (ABCG) half-transporter. White is closely related to mammalian ABCG family members that function in cholesterol efflux. Mutants of white have several behavioral phenotypes that are independent of visual defects. This study characterizes a novel defect of white mutants in the acquisition of olfactory memory using the aversive olfactory conditioning paradigm. The w1118 mutants learned slower than wildtype controls, yet with additional training, they reached wildtype levels of performance. The w1118 learning phenotype is also found in the wapricot and wcoral alleles, is dominant, and is rescued by genomic white and mini-white transgenes. Reducing dietary cholesterol strongly impaired olfactory learning for wildtype controls, while w1118 mutants were resistant to this deficit. The w1118 mutants displayed higher levels of cholesterol and cholesterol esters than wildtype under this low-cholesterol diet. Increasing levels of serotonin, dopamine, or both in the white mutants significantly improved w1118 learning. However, serotonin levels were not lower in the heads of the w1118 mutants than in wildtype controls. There were also no significant differences found in synapse numbers within the w1118 brain. We propose that the w1118 learning defect may be due to inefficient biogenic amine signaling brought about by altered cholesterol homeostasis. Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)
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Review

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14 pages, 653 KiB  
Review
Anesthesia Resistant Memories in Drosophila, a Working Perspective
by Anna Bourouliti and Efthimios M. C. Skoulakis
Int. J. Mol. Sci. 2022, 23(15), 8527; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23158527 - 31 Jul 2022
Viewed by 1957
Abstract
Memories are lasting representations over time of associations between stimuli or events. In general, the relatively slow consolidation of memories requires protein synthesis with a known exception being the so-called Anesthesia Resistant Memory (ARM) in Drosophila. This protein synthesis-independent memory type survives amnestic [...] Read more.
Memories are lasting representations over time of associations between stimuli or events. In general, the relatively slow consolidation of memories requires protein synthesis with a known exception being the so-called Anesthesia Resistant Memory (ARM) in Drosophila. This protein synthesis-independent memory type survives amnestic shocks after a short, sensitive window post training, and can also emerge after repeated cycles of training in a negatively reinforced olfactory conditioning task, without rest between cycles (massed conditioning—MC). We discussed operational and molecular mechanisms that mediate ARM and differentiate it from protein synthesis-dependent long-term memory (LTM) in Drosophila. Based on the notion that ARM is unlikely to specifically characterize Drosophila, we examined protein synthesis and MC-elicited memories in other species and based on intraspecies shared molecular components and proposed potential relationships of ARM with established memory types in Drosophila and vertebrates. Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)
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15 pages, 518 KiB  
Review
The Medial Prefrontal Cortex and Fear Memory: Dynamics, Connectivity, and Engrams
by Lucie Dixsaut and Johannes Gräff
Int. J. Mol. Sci. 2021, 22(22), 12113; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222212113 - 09 Nov 2021
Cited by 20 | Viewed by 7897
Abstract
It is becoming increasingly apparent that long-term memory formation relies on a distributed network of brain areas. While the hippocampus has been at the center of attention for decades, it is now clear that other regions, in particular the medial prefrontal cortex (mPFC), [...] Read more.
It is becoming increasingly apparent that long-term memory formation relies on a distributed network of brain areas. While the hippocampus has been at the center of attention for decades, it is now clear that other regions, in particular the medial prefrontal cortex (mPFC), are taking an active part as well. Recent evidence suggests that the mPFC—traditionally implicated in the long-term storage of memories—is already critical for the early phases of memory formation such as encoding. In this review, we summarize these findings, relate them to the functional importance of the mPFC connectivity, and discuss the role of the mPFC during memory consolidation with respect to the different theories of memory storage. Owing to its high functional connectivity to other brain areas subserving memory formation and storage, the mPFC emerges as a central hub across the lifetime of a memory, although much still remains to be discovered. Full article
(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)
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