RIM1α is required for presynaptic long-term potentiation

Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP

de Rooij, J., Zwartkruis, F. J. T., Verheijen, M. H. G., Cool, R. H., Nijman, S. M. B., Wittinghofer, A., & Bos, J. L. (1998) · Nature · doi:10.1038/24884 · Cited by 1,970

Short-Term Synaptic Plasticity

Zucker, R. S. (1989) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.12.030189.000305 · Cited by 1,450

A Family of cAMP-Binding Proteins That Directly Activate Rap1

Kawasaki, H., Springett, G. M., Mochizuki, N., Toki, S., Nakaya, M., Matsuda, M., Housman, D. E., & Graybiel, A. M. (1998) · Science · doi:10.1126/science.282.5397.2275 · Cited by 1,386

Contrasting properties of two forms of long-term potentiation in the hippocampus

Nicoll, R. A., & Malenka, R. C. (1995) · Nature · doi:10.1038/377115a0 · Cited by 861

Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion

Wang, Y., Okamoto, M., Schmitz, F., Hofmann, K., & Südhof, T. C. (1997) · Nature · doi:10.1038/41580 · Cited by 684

Mediation of Hippocampal Mossy Fiber Long-Term Potentiation by Cyclic AMP

Weisskopf, M. G., Castillo, P. E., Zalutsky, R. A., & Nicoll, R. A. (1994) · Science · doi:10.1126/science.7916482 · Cited by 618

RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone

Schoch, S., Castillo, P. E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R. C., & Südhof, T. C. (2002) · Nature · doi:10.1038/415321a · Cited by 579

cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase

Huang, Y.-Y., Li, X.-C., & Kandel, E. R. (1994) · Cell · doi:10.1016/0092-8674(94)90401-4 · Cited by 490

cAMP-GEFII is a direct target of cAMP in regulated exocytosis

Ozaki, N., Shibasaki, T., Kashima, Y., Miki, T., Takahashi, K., Ueno, H., Sunaga, Y., Yano, H., Matsuura, Y., Iwanaga, T., et al. (2000) · Nature Cell Biology · doi:10.1038/35041046 · Cited by 481

Cyclic AMP Mediates a Presynaptic Form of LTP at Cerebellar Parallel Fiber Synapses

Salin, P. A., Malenka, R. C., & Nicoll, R. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80099-9 · Cited by 443

The Synaptic Basis of Activity-Dependent Eye-Specific Competition

Zhang, C., Yadav, S., & Speer, C. M. (2022) · Cell Reports · doi:10.1016/j.celrep.2023.112085 · Cited by 9

Type 1 metalloproteinase is selectively expressed in adult rat brain and can be rapidly up-regulated by kainate

Ierusalimsky, V. N., & Balaban, P. M. (2013) · Acta Histochemica · doi:10.1016/j.acthis.2013.04.001 · Cited by 9

Involvement of Group II mGluRs in mossy fiber LTD

Wostrack, M., & Dietrich, D. (2009) · Synapse · doi:10.1002/syn.20692 · Cited by 9

RIM3γ is a postsynaptic protein in the rat central nervous system

Liang, F., Zhang, B., Tang, J., Guo, J., Li, W., Ling, E., Chu, H., Wu, Y., Chan, Y. G., & Cao, Q. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21403 · Cited by 9

The Multiple Faces of RIM

Pernía‐Andrade, A. J., & Jónás, P. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.010 · Cited by 9

A Conceptual Review of the Psychosocial Genomics of Expectancy and Surprise: Neuroscience Perspectives about the Deep Psychobiology of Therapeutic Hypnosis

Rossi, E. L. (2002) · American Journal of Clinical Hypnosis · doi:10.1080/00029157.2002.10403508 · Cited by 10

The activation of mGluR4 rescues parallel fiber synaptic transmission and LTP, motor learning and social behavior in a mouse model of Fragile X Syndrome

Martín, R., Suárez-Pinilla, A. S., García-Font, N., Laguna-Luque, M. L., López, J. C., Oset‐Gasque, M. J., Gruart, A., Delgado-Garcia, J. M., Torres, M., & Sánchez‐Prieto, J. (2023) · Molecular Autism · doi:10.1186/s13229-023-00547-4 · Cited by 9

GABAB-receptor modulation of short-term synaptic depression at an excitatory input to murine hippocampal CA3 pyramidal neurons

Hoskison, M. M., Connor, J. A., & Shuttleworth, C. W. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.04.050 · Cited by 8

Control of Munc13-1 Activity by Autoinhibitory Interactions Involving the Variable N-terminal Region

Xu, J., Esser, V., Gołębiowska-Mendroch, K., Bolembach, A. A., & Rizo, J. (2024) · Journal of Molecular Biology · doi:10.1016/j.jmb.2024.168502 · Cited by 8

Presynaptic recycling pool density regulates spontaneous synaptic vesicle exocytosis rate and is upregulated in the presence of β-amyloid

Wilson, P., Kim, N., Cotter, R., Parkes, M., Cmelak, L., Reed, M. N., & Gramlich, M. W. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115410 · Cited by 7

Nanoscaled RIM clustering at presynaptic active zones revealed by endogenous tagging

Mrestani, A., Dannhäuser, S., Pauli, M., Kollmannsberger, P., Hübsch, M., Morris, L., Langenhan, T., Heckmann, M., & Paul, M. M. (2023) · Life Science Alliance · doi:10.26508/lsa.202302021 · Cited by 7

A Comparative Analysis of the Molecular Mechanisms Contributing to Implicit and Explicit Memory Storage in Aplysia and in the Hippocampus ☆

Hawkins, R. D., Mayford, M. R., & Kandel, E. R. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21095-x · Cited by 6

Redundant functions of RIM1α and RIM2α in Ca2+-triggered neurotransmitter release

Mittelstaedt, T., Lin, W., Padgett, D., Feldmann, N., Castillo, P., Han, W., Schmitz, F., Kaeser, P. S., Südhof, T. C., & Schoch, S. (2007) · Brill | Schöningh eBooks · doi:10.30965/9783657764082_032 · Cited by 6

Social isolation-induced transcriptomic changes in mouse hippocampus impact the synapse and show convergence with human genetic risk for neurodevelopmental phenotypes

Laighneach, A., Kelly, J. P., Desbonnet, L., Holleran, L., Kerr, D. M., McKernan, D. P., Donohoe, G. J., & Morris, D. W. (2023) · PLoS ONE · doi:10.1371/journal.pone.0295855 · Cited by 5

CK2α regulates the transcription of BRP in Drosophila

Wairkar, Y. P., Trivedi, D., Natarajan, R., Barnes, K., Dolores, L. K., & Cho, P. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.09.025 · Cited by 5

Ionotropic Glutamate Receptors in Synaptic Plasticity

Pelkey, K. A., & McBain, C. J. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-055-3_5 · Cited by 5

Genetic and Genomic Strategies in Learning and Memory

Sforza, D., & Smith, D. (2003) · Current Genomics · doi:10.2174/1389202033490259 · Cited by 6

Neocortical layer-5 tLTD relies on non-ionotropic presynaptic NMDA receptor signalingPreprint

Thomazeau, A., Rannio, S., Brock, J. A., Wong, H. H., & Sjöström, P. J. (2025) · eLife · doi:10.7554/elife.106284.3 · Cited by 5

Long-Term Measurements

Graziane, N., & Dong, Y. (2015) · Neuromethods · doi:10.1007/978-1-4939-3274-0_12 · Cited by 3

Presynaptic Mechanisms in Plasticity and Memory

Powell, C. M., & Castillo, P. E. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00038-3 · Cited by 4

Long-term potentiation in the brain: a synaptic memory mechanism

Moreno, A. R., & Paulsen, O. (2026) · Physiological Reviews · doi:10.1152/physrev.00028.2025 · Cited by 2

Neuronal Exocytosis

Sankaranarayanan, S., & Ryan, T. A. (2007) · Elsevier eBooks · doi:10.1016/b978-012369437-9/50010-4 · Cited by 2

DYRK1A Up-Regulation Specifically Impairs a Presynaptic Form of Long-Term Potentiation

Lepagnol-Bestel, A.-M., Haziza, S., Viard, J., Salin, P. A., Crépel, V., Duchon, A., Hérault, Y., & Simonneau, M. (2025) · Life · doi:10.3390/life15020149 · Cited by 2

Studying synaptic efficiency by post-hoc immunolabelling

Ramírez‐Franco, J., Alonso, B., Bartolomé‐Martín, D., Sánchez‐Prieto, J., & Torres, M. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-127 · Cited by 2

Overview: Presynaptic Terminal Proteins Orchestrate Stepwise Synaptic Vesicle Phases

Mochida, S. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_1 · Cited by 2

Molecular Architecture of Ca2+ Channel Complexes Organized by CaVβ Subunits in Presynaptic Active Zones

Nakao, A., Hirano, M., Takada, Y., Kiyonaka, S., & Mori, Y. (2013) · Springer eBooks · doi:10.1007/978-94-007-6334-0_4 · Cited by 2

Reciprocal Regulation of Neuronal Calcium Channels by Synaptic Proteins

Weiss, N., & Zamponi, G. W. (2013) · Springer eBooks · doi:10.1007/978-94-007-6334-0_3 · Cited by 2

Mossy Fiber LTP: A Presynaptic cAMP-Dependent Form of Plasticity ☆

Fernandes, H. B., & Contractor, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.02780-2 · Cited by 2

RIM1αβ Are Required at the Corticostriatal Synapses for Habit Formation

Hidalgo, S. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0896-19.2019 · Cited by 2

Coordinated bi-directional trafficking of synaptic vesicle and active zone proteins in peripheral nerves

Juranek, J. K., Mukherjee, K., Jahn, R., & Li, J. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.04.041 · Cited by 2

Presynaptic Mechanisms of Plasticity and Memory in Aplysia and Other Learning-Related Experimental Systems

Hawkins, R. D., Bailey, C. H., & Kandel, E. R. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21111-5 · Cited by 1

The flexible synapse – How mossy fiber architecture adapts to changing needs

Bruentgens, F., Schmitz, D., & Orlando, M. (2026) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2026.102882 · Cited by 1

Screening Candidate Genes for Body Size Traits in Dongfeng Sika Deer Bucks Based on Genome-Wide Association Analysis

Zhang, Y., Zhang, X., Zhao, L., Zhang, Z., Zhao, Y., Qian, W., Gai, G., Bai, H., Du, P., & Han, H. (2026) · Biology · doi:10.3390/biology15030227 · Cited by 1

HCAR1-mediated lactate signaling modulates motor behavior and regulates spontaneous firing in Purkinje cells

Binda, F., Buscemi, L., Gurtner, N., Hirt, L., & Chatton, J. (2026) · iScience · doi:10.1016/j.isci.2026.116930 · Cited by 1

Chromosomal Abnormalities and Putative Susceptibility Genes in Autism Spectrum Disorders

Gilling, M. (2015) · Cited by 1

Hippocampal circuits

Mandyam, C. D. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-823453-2.00006-0 · Cited by 1

Paroxysmal dystonia results from the loss of RIM4 in Purkinje cells

Kim, H.-T., Melliti, N., Breithausen, E., Michel, K., Colomer, S. F., Poguzhelskaya, E., Nemcova, P., Ewell, L. A., Blaess, S., Becker, A. J., et al. (2024) · Brain · doi:10.1093/brain/awae081 · Cited by 1

Synaptic Vesicle Recycling as a Substrate for Neural Plasticity

Virmani, T., & Kavalali, E. T. (2005) · Springer eBooks · doi:10.1007/0-387-25443-9_16 · Cited by 1

UNC-10/SYD-2 links kinesin-3 to RAB-3-containing vesicles in the absence of the motor’s PH domainPreprint

Bayansan, O., Bhan, P., Chang, C.-Y., Barmaver, S. N., Shen, C.-P., & Wagner, O. I. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/723247 · Cited by 1

Microglia Depletion Selectively Eliminates a Singular Form of Hippocampal Long-Term PotentiationPreprint

Chavez, J., Le, A. A., Quintanilla, J., Tagne, A. M., Piomelli, D., LYNCH, G. S., & Gall, C. M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.29.501926 · Cited by 1

Transgenic Mouse Models in the Analysis of Neurotransmitter Release Mechanisms

Brose, N., & Rettig, J. (2004) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-18934-0_8

Rab3A Interacting Molecules (RIMs)

Kaeser, P. S., & Powell, C. M. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.01353-x

Pre-synaptic terminal dynamics in the hippocampus

Paola, V. D. (2003) · edoc (University of Basel) · doi:10.5451/unibas-003686969

The Role of EPAC Signaling in Memory Consolidation and Sleep Deprivation

Ma, N. (2011) · ScholarlyCommons (University of Pennsylvania)

Redundant Neuromodulatory Mechanisms That Control Fear Memory Consolidation

Young, M. B. (2013) · Scholarly Commons (University of Pennsylvania)

Presynaptic mechanisms determining the dynamic range of neurotransmitter release in the lateral amygdala

Fourcaudot, E. (2008) · edoc (University of Basel) · doi:10.5451/unibas-004662818

FUNCTIONAL PLASTICITY OF HIPPOCAMPAL GLUTAMATERGIC SYNAPSES IN DEVELOPMENT AND DISEASE

Peng, X. (2011) · ScholarlyCommons (University of Pennsylvania)

Zur synaptischen Transmission und Plastizität in kortikalen Hirnschnittpräparaten

Wozny, C. (2014) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-4687

Genetic dissections of active zone proteins

Liu, K. S. Y. (2012) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-5898

FUSION PORE OF CALCIUM TRIGGERED EXOCYTOSIS

Han, X. (2004)

Kobe University Repository : Kernel

Shibasaki, T., & Takahashi, H. (2015)

Regulation of Active Zone Ca2+ Channels

Leal, K., & Mochida, S. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_9

Annual Report 2002 PhD-Programme 2000 of the International Max Planck Research School for Molecular Cell Biology and Bioengineering Dresden

Erler, F. (2002)

UNC-10 Regulates The Docking Step of DCV Exocytosis in C. elegans*

Wan-Juan, F. E. N. G., Zhou, W., Zhang, Y., Wu, Z., & Xu, T. (2012) · PROGRESS IN BIOCHEMISTRY AND BIOPHYSICS · doi:10.3724/sp.j.1206.2011.00374

Presynaptic Terminal Differentiation

Zhen, M. (2007) · Elsevier eBooks · doi:10.1016/b978-012369437-9/50008-6

Role of CaMKII and the GluN2B subunit of the NMDAR in dorsal striatal glutamatergic synaptic transmission, MSN morphology and striatal-based behaviors

Klug, J. R. (2012)

Regulation of SNARE Complex Assembly by Second Messengers: Roles of Phospholipases, Munc13 and Munc18

Groffen, A. J. A., Verhage, M., & Regazzi, R. (2006) · Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam)

Unraveling the Molecular Mechanisms of Munc18 and Munc13 in Mast Cell Exocytosis

Bin, N. (2017) · TSpace (University of Toronto)

In Silico Edgetic Profiling and Network Analysis of Human Genetic Variants, with an Application to Disease Module Detection

Cui, H. (2020) · Digital WPI

Roles of the ELKS/CAST Family and SAD Kinase in Neurotransmitter Release

Ohtsuka, T., & Takai, Y. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-481-0_8

Regulation of SNARE Complex Assembly by Second Messengers

Groffen, A. J. A., & Verhage, M. (2008) · Springer eBooks · doi:10.1007/978-0-387-39961-4_2

Faculty Opinions recommendation of Rabphilin regulates SNARE-dependent re-priming of synaptic vesicles for fusion.

Takai, Y. (2006) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1033825.387877

Neurotransmitter Release: Priming at Presynaptic Active Zones

Kawabe, H., Varoqueaux, F., & Brose, N. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_3954

Rab3

Schlüter, O. M. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.01367-x

Active Zone☆

Wong, M. Y., & Kaeser, P. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.04486-x · Cited by 1

The Neuroscientist Comments

(2002) · The Neuroscientist · doi:10.1177/1073858402008003001

Absolute Threshold

(2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_14

Rab3 Interacting Molecules (RIMs)☆

de Jong, A. P. H., & Kaeser, P. S. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.04743-7

Increased Transforming Growth Factor-β1 Modulates Hippocampal Glutamatergic Synaptic Protein Expression and Synaptic Transmission

Bae, J. J. (2010) · TSpace (University of Toronto)

The Hippocampus and Addiction: Focus on Plasticity and Circuitry in the Hippocampus

Mandyam, C. D. (2022) · Springer eBooks · doi:10.1007/978-3-030-67928-6_24-1

Long-Term Measurements

Graziane, N., & Dong, Y. (2022) · Neuromethods · doi:10.1007/978-1-0716-2589-7_12

The Hippocampus and Addiction: Focus on Plasticity and Circuitry in the Hippocampus

Mandyam, C. D. (2022) · Springer eBooks · doi:10.1007/978-3-030-92392-1_24

Neocortical Layer-5 tLTD Relies on Non-Ionotropic Presynaptic NMDA Receptor SignalingPreprint

Thomazeau, A., Rannio, S., Brock, J. A., Wong, H. H., & Sjöström, P. J. (2025) · eLife · doi:10.7554/elife.106284.1

Neocortical Layer-5 tLTD Relies on Non-Ionotropic Presynaptic NMDA Receptor SignalingPreprint

Thomazeau, A., Rannio, S., Brock, J. A., Wong, H. H., & Sjöström, P. J. (2025) · eLife · doi:10.7554/elife.106284.2

Author response: Neocortical layer-5 tLTD relies on non-ionotropic presynaptic NMDA receptor signaling

Thomazeau, A., Rannio, S., Brock, J. A., Wong, H. H., & Sjöström, P. J. (2025) · eLife · doi:10.7554/elife.106284.3.sa3

Overview: Spatial and Temporal Regulation of Ca2+ Channels

Mochida, S. (2013) · Springer eBooks · doi:10.1007/978-94-007-6334-0_1

Presynaptic Substrates Mediating Fos- and Jun-dependent Plasticity at the Drosophila Neuromuscular Junction

Kim, S. M. (2007) · UA Campus Repository (The University of Arizona)

An unexpected specialization of the active zone scaffold RIM at high release synapsesPreprint

Stark, R., Patel, P., Dong, W., Dehn, C., & Dickman, D. K. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.20.713218

Role of the actomyosin cytoskeleton on the synaptic effects of the type-1 cannabinoid receptor (CB1R)

McFadden, M. H. (2018) · theses.fr (ABES) · doi:10.70675/036294d9z53a4z495ez9221ze4fba667c298

Investigating the molecular pathways driving the sumoylation/desumoylation balance in rat hippocampal synapses

Schorova, L. (2018) · theses.fr (ABES) · doi:10.70675/a30a505az5e81z4089za24azcf43d27e33ce

Pathophysiological consequences of a Fragile X missense mutation

Garcia, M. P. (2020) · theses.fr (ABES) · doi:10.70675/b8e86263z5926z4a83zbaf6z0f61bf2d15f9

Dissecting the propensity of RIM1 subdomains to form phase condensates

Kersten, L., Galkov, M., Nemcova, P., Mostafa, A. H. D., Quatraccioni, A., Dietrich, D., & Schoch, S. (2026) · Scientific Reports · doi:10.1038/s41598-026-56567-6

Expression and function of Rab3 interacting molecules and clarin-1 in inner hair cells

Oshima-Takago, T. (2013) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-4010

Long-Term Potentiation (LTP): Mossy Fiber cAMP-Dependent Presynaptic LTP

Contractor, A. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.01206-7

Molecular Mechanisms for Presynaptic Long-term Potentiation

Yang, Y. (2011) · DukeSpace (Duke University)

Genetic evidence for a protein-kinase-A-mediated presynaptic component in NMDA-receptor-dependent forms of long-term synaptic potentiation

Huang, Y.-Y., Zakharenko, S. S., Schoch, S., Kaeser, P. S., Janz, R., Südhof, T. C., Siegelbaum, S. A., & Kandel, E. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503777102 · Cited by 65

Rab3A is essential for mossy fibre long-term potentiation in the hippocampus

Castillo, P. E., Janz, R., Sdhof, T. C., Tzounopoulos, T., Malenka, R. C., & Nicoll, R. A. (1997) · Nature · doi:10.1038/41574 · Cited by 356

AcuteIn VivoGenetic Rescue Demonstrates That Phosphorylation of RIM1α Serine 413 Is Not Required for Mossy Fiber Long-Term Potentiation

Yang, Y., & Calakos, N. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4285-09.2010 · Cited by 19

RIM function in short- and long-term synaptic plasticity

Kaeser, P. S., & Südhof, T. C. (2005) · Biochemical Society Transactions · doi:10.1042/bst20051345 · Cited by 82