Temporal Gating of Synaptic Competition in the Amygdala by Cannabinoid Receptor Activation

Madeira, Natália; Drumond, Ana; Fonseca, Rosalina

doi:10.1093/cercor/bhaa026

Title: Temporal Gating of Synaptic Competition in the Amygdala by Cannabinoid Receptor Activation

Journal Article · 12 March 2020 · Cerebral Cortex

DOI: https://doi.org/10.1093/cercor/bhaa026 · OSTI ID:1604472

Madeira, Natália ^[1]; Drumond, Ana ^[2]; Fonseca, Rosalina ^[3]

Cellular and Systems Neurobiology, Chronic Diseases Research Center (CEDOC), NOVA Medical School, Universidade Nova de Lisboa, Lisboa 1169-056, Portugal
Instituto Gulbenkian de Ciência, Oeiras 2780-156, Portugal
Cellular and Systems Neurobiology, Chronic Diseases Research Center (CEDOC), NOVA Medical School, Universidade Nova de Lisboa, Lisboa 1169-056, Portugal, Instituto Gulbenkian de Ciência, Oeiras 2780-156, Portugal

Abstract The acquisition of fear memories involves plasticity of the thalamic and cortical pathways to the lateral amygdala (LA). In turn, the maintenance of synaptic plasticity requires the interplay between input-specific synaptic tags and the allocation of plasticity-related proteins. Based on this interplay, weakly activated synapses can express long-lasting forms of synaptic plasticity by cooperating with strongly activated synapses. Increasing the number of activated synapses can shift cooperation to competition. Synaptic cooperation and competition can determine whether two events, separated in time, are associated or whether a particular event is selected for storage. The rules that determine whether synapses cooperate or compete are unknown. We found that synaptic cooperation and competition, in the LA, are determined by the temporal sequence of cortical and thalamic stimulation and that the strength of the synaptic tag is modulated by the endocannabinoid signaling. This modulation is particularly effective in thalamic synapses, supporting a critical role of endocannabinoids in restricting thalamic plasticity. Also, we found that the availability of synaptic proteins is activity-dependent, shifting competition to cooperation. Our data present the first evidence that presynaptic modulation of synaptic activation, by the cannabinoid signaling, functions as a temporal gating mechanism limiting synaptic cooperation and competition.

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Sponsoring Organization:: USDOE Office of Nuclear Energy (NE), Nuclear Fuel Cycle and Supply Chain

OSTI ID:: 1604472

Journal Information:: Cerebral Cortex, Journal Name: Cerebral Cortex Journal Issue: 7 Vol. 30; ISSN 1047-3211

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (42)

Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP Frey, U.; Morris, R. G. M. Neuropharmacology, Vol. 37, Issue 4-5 https://doi.org/10.1016/S0028-3908(98)00040-9	journal	April 1998
Expression of Constitutively Active CREB Protein Facilitates the Late Phase of Long-Term Potentiation by Enhancing Synaptic Capture Barco, Angel; Alarcon, Juan M.; Kandel, Eric R. Cell, Vol. 108, Issue 5 https://doi.org/10.1016/S0092-8674(02)00657-8	journal	March 2002
Complementary distribution of vesicular glutamate transporters in the central nervous system Kaneko, Takeshi; Fujiyama, Fumino Neuroscience Research, Vol. 42, Issue 4 https://doi.org/10.1016/S0168-0102(02)00009-3	journal	April 2002
Memory engram storage and retrieval Tonegawa, Susumu; Pignatelli, Michele; Roy, Dheeraj S. Current Opinion in Neurobiology, Vol. 35 https://doi.org/10.1016/j.conb.2015.07.009	journal	December 2015
Competing for Memory Fonseca, Rosalina; Nägerl, U. Valentin; Morris, Richard G. M. Neuron, Vol. 44, Issue 6 https://doi.org/10.1016/j.neuron.2004.10.033	journal	December 2004
A Balance of Protein Synthesis and Proteasome-Dependent Degradation Determines the Maintenance of LTP Fonseca, Rosalina; Vabulas, Ramunas M.; Hartl, F. Ulrich Neuron, Vol. 52, Issue 2 https://doi.org/10.1016/j.neuron.2006.08.015	journal	October 2006
The Dendritic Branch Is the Preferred Integrative Unit for Protein Synthesis-Dependent LTP Govindarajan, Arvind; Israely, Inbal; Huang, Shu-Ying Neuron, Vol. 69, Issue 1 https://doi.org/10.1016/j.neuron.2010.12.008	journal	January 2011
Consolidation and Reconsolidation: Two Lives of Memories? McKenzie, Sam; Eichenbaum, Howard Neuron, Vol. 71, Issue 2 https://doi.org/10.1016/j.neuron.2011.06.037	journal	July 2011
Neurons Are Recruited to a Memory Trace Based on Relative Neuronal Excitability Immediately before Training Yiu, Adelaide P.; Mercaldo, Valentina; Yan, Chen Neuron, Vol. 83, Issue 3 https://doi.org/10.1016/j.neuron.2014.07.017	journal	August 2014
Cannabinoids modulate neuronal firing in the rat basolateral amygdala: evidence for CB1- and non-CB1-mediated actions Pistis, Marco; Perra, Simona; Pillolla, Giuliano Neuropharmacology, Vol. 46, Issue 1 https://doi.org/10.1016/j.neuropharm.2003.08.003	journal	January 2004
Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD Sajikumar, S. Neurobiology of Learning and Memory, Vol. 82, Issue 1 https://doi.org/10.1016/j.nlm.2004.03.003	journal	July 2004
Endocannabinoid signaling and memory dynamics: A synaptic perspective Drumond, Ana; Madeira, Natália; Fonseca, Rosalina Neurobiology of Learning and Memory, Vol. 138 https://doi.org/10.1016/j.nlm.2016.07.031	journal	February 2017
Synaptic clustering within dendrites: An emerging theory of memory formation Kastellakis, George; Cai, Denise J.; Mednick, Sara C. Progress in Neurobiology, Vol. 126 https://doi.org/10.1016/j.pneurobio.2014.12.002	journal	March 2015
VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate Fremeau, Robert T.; Voglmaier, Susan; Seal, Rebecca P. Trends in Neurosciences, Vol. 27, Issue 2 https://doi.org/10.1016/j.tins.2003.11.005	journal	February 2004
A synaptic model of memory: long-term potentiation in the hippocampus Bliss, T. V. P.; Collingridge, G. L. Nature, Vol. 361, Issue 6407 https://doi.org/10.1038/361031a0	journal	January 1993
Synaptic tagging and long-term potentiation Frey, Uwe; Morris, Richard G. M. Nature, Vol. 385, Issue 6616 https://doi.org/10.1038/385533a0	journal	February 1997
A shared neural ensemble links distinct contextual memories encoded close in time Cai, Denise J.; Aharoni, Daniel; Shuman, Tristan Nature, Vol. 534, Issue 7605 https://doi.org/10.1038/nature17955	journal	May 2016
Targeting the endocannabinoid system in the treatment of fragile X syndrome Busquets-Garcia, Arnau; Gomis-González, Maria; Guegan, Thomas Nature Medicine, Vol. 19, Issue 5 https://doi.org/10.1038/nm.3127	journal	March 2013
Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling Puighermanal, Emma; Marsicano, Giovanni; Busquets-Garcia, Arnau Nature Neuroscience, Vol. 12, Issue 9 https://doi.org/10.1038/nn.2369	journal	August 2009
Synaptic correlates of fear extinction in the amygdala Amano, Taiju; Unal, Cagri T.; Paré, Denis Nature Neuroscience, Vol. 13, Issue 4 https://doi.org/10.1038/nn.2499	journal	March 2010
Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system Ehlers, Michael D. Nature Neuroscience, Vol. 6, Issue 3 https://doi.org/10.1038/nn1013	journal	February 2003
Neuronal activity determines the protein synthesis dependence of long-term potentiation Fonseca, Rosalina; Nägerl, U. Valentin; Bonhoeffer, Tobias Nature Neuroscience, Vol. 9, Issue 4 https://doi.org/10.1038/nn1667	journal	March 2006
Reversible Gating of Endocannabinoid Plasticity in the Amygdala by Chronic Stress: A Potential Role for Monoacylglycerol Lipase Inhibition in the Prevention of Stress-Induced Behavioral Adaptation Sumislawski, Joshua J.; Ramikie, Teniel S.; Patel, Sachin Neuropsychopharmacology, Vol. 36, Issue 13 https://doi.org/10.1038/npp.2011.166	journal	August 2011
Asymmetrical Synaptic Cooperation between Cortical and Thalamic Inputs to the Amygdale Fonseca, Rosalina Neuropsychopharmacology, Vol. 38, Issue 13 https://doi.org/10.1038/npp.2013.178	journal	July 2013
Dissociation of the Pharmacological Effects of THC by mTOR Blockade Puighermanal, Emma; Busquets-Garcia, Arnau; Gomis-González, Maria Neuropsychopharmacology, Vol. 38, Issue 7 https://doi.org/10.1038/npp.2013.31	journal	January 2013
Making memories last: the synaptic tagging and capture hypothesis Redondo, Roger L.; Morris, Richard G. M. Nature Reviews Neuroscience, Vol. 12, Issue 1 https://doi.org/10.1038/nrn2963	journal	December 2010
The endocannabinoid system in guarding against fear, anxiety and stress Lutz, Beat; Marsicano, Giovanni; Maldonado, Rafael Nature Reviews Neuroscience, Vol. 16, Issue 12 https://doi.org/10.1038/nrn4036	journal	November 2015
The interplay between neuronal activity and actin dynamics mimic the setting of an LTD synaptic tag Szabó, Eszter C.; Manguinhas, Rita; Fonseca, Rosalina Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33685	journal	September 2016
Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain: CB1 expression in murine forebrain Marsicano, Giovanni; Lutz, Beat European Journal of Neuroscience, Vol. 11, Issue 12 https://doi.org/10.1046/j.1460-9568.1999.00847.x	journal	December 1999
Competition between recently potentiated synaptic inputs reveals a winner-take-all phase of synaptic tagging and capture Sajikumar, S.; Morris, R. G. M.; Korte, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33 https://doi.org/10.1073/pnas.1403643111	journal	August 2014
Mammalian Target of Rapamycin (mTOR) Tagging Promotes Dendritic Branch Variability through the Capture of Ca ²⁺ /Calmodulin-dependent Protein Kinase II α (CaMKIIα) mRNAs by the RNA-binding Protein HuD Sosanya, Natasha M.; Cacheaux, Luisa P.; Workman, Emily R. Journal of Biological Chemistry, Vol. 290, Issue 26 https://doi.org/10.1074/jbc.M114.599399	journal	May 2015
Endogenous cannabinoids trigger the depolarization-induced suppression of excitation in the lateral amygdala Kodirov, S. A.; Jasiewicz, J.; Amirmahani, P. Learning & Memory, Vol. 17, Issue 1 https://doi.org/10.1101/lm.1663410	journal	December 2009
Activation of the Cannabinoid Receptor Type 1 Decreases Glutamatergic and GABAergic Synaptic Transmission in the Lateral Amygdala of the Mouse Azad, S. C. Learning & Memory, Vol. 10, Issue 2 https://doi.org/10.1101/lm.53303	journal	March 2003
Increasing CREB in the auditory thalamus enhances memory and generalization of auditory conditioned fear Han, J. -H.; Yiu, A. P.; Cole, C. J. Learning & Memory, Vol. 15, Issue 6 https://doi.org/10.1101/lm.993608	journal	May 2008
Activity-dependent actin dynamics are required for the maintenance of long-term plasticity and for synaptic capture: Role of actin dynamics in synaptic-capture Fonseca, Rosalina European Journal of Neuroscience, Vol. 35, Issue 2 https://doi.org/10.1111/j.1460-9568.2011.07955.x	journal	January 2012
Competition between engrams influences fear memory formation and recall Rashid, A. J.; Yan, C.; Mercaldo, V. Science, Vol. 353, Issue 6297 https://doi.org/10.1126/science.aaf0594	journal	July 2016
The Endocannabinoid System and the Brain Mechoulam, Raphael; Parker, Linda A. Annual Review of Psychology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-psych-113011-143739	journal	January 2013
Endocannabinoid-Mediated Control of Synaptic Transmission Kano, Masanobu; Ohno-Shosaku, Takako; Hashimotodani, Yuki Physiological Reviews, Vol. 89, Issue 1 https://doi.org/10.1152/physrev.00019.2008	journal	January 2009
Discriminative Auditory Fear Learning Requires Both Tuned and Nontuned Auditory Pathways to the Amygdala Antunes, R.; Moita, M. A. Journal of Neuroscience, Vol. 30, Issue 29 https://doi.org/10.1523/JNEUROSCI.1037-10.2010	journal	July 2010
Involvement of Protein Synthesis and Degradation in Long-Term Potentiation of Schaffer Collateral CA1 Synapses Karpova, A. Journal of Neuroscience, Vol. 26, Issue 18 https://doi.org/10.1523/JNEUROSCI.4573-05.2006	journal	May 2006
Identification of Compartment- and Process-Specific Molecules Required for "Synaptic Tagging" during Long-Term Potentiation and Long-Term Depression in Hippocampal CA1 Sajikumar, S.; Navakkode, S.; Frey, J. U. Journal of Neuroscience, Vol. 27, Issue 19 https://doi.org/10.1523/JNEUROSCI.4940-06.2007	journal	May 2007
Signal transduction of the CB1 cannabinoid receptor Turu, Gábor; Hunyady, László Journal of Molecular Endocrinology, Vol. 44, Issue 2 https://doi.org/10.1677/JME-08-0190	journal	July 2009

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