Rapid, activity-independent turnover of vesicular transmitter content at a mixed glycine/GABA synapse
Open accessAbstract
The release of neurotransmitter via the fusion of transmitter-filled, presynaptic vesicles is the primary means by which neurons relay information. However, little is known regarding the molecular mechanisms that supply neurotransmitter destined for vesicle filling, the endogenous transmitter concentrations inside presynaptic nerve terminals, or the dynamics of vesicle refilling after exocytosis. We addressed these issues by recording from synaptically coupled pairs of glycine/GABA coreleasing interneurons (cartwheel cells) of the mouse dorsal cochlear nucleus. We find that the plasma membrane transporter GlyT2 and the intracellular enzyme glutamate decarboxylase supply the majority of glycine and GABA, respectively. Pharmacological block of GlyT2 or glutamate decarboxylase led to rapid and complete rundown of transmission, whereas increasing GABA synthesis via intracellular glutamate uncaging dramatically potentiated GABA release within 1 min. These effects were surprisingly independent of exocytosis, indicating that prefilled vesicles re-equilibrated upon acute changes in cytosolic transmitter. Titration of cytosolic transmitter with postsynaptic responses indicated that endogenous, nonvesicular glycine/GABA levels in nerve terminals are 5-7 mm, and that vesicular transport mechanisms are not saturated under basal conditions. Thus, cytosolic transmitter levels dynamically set the strength of inhibitory synapses in a release-independent manner.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Packaging GABA and/or glycine into vesicles largely depends on their intracellular intraaxonal concentrations, controlled by GAD1/2 synthesis or GlyT1/2 transporters.
“Therefore, packaging GABA and/or glycine into vesicles is largely dependent on their intracellular (intraaxonal) concentration, which are controlled by either intracellular synthesis (glutamate decarboxylase [GAD] 1/2) or plasma membrane transporters (GlyT1/2), respectively.51”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [51]
Synaptic potency depends not only on postsynaptic receptor number but also on presynaptic transmitter concentrations and vesicular loading.
“These results suggest that the potency of a synapse depends not only on the number of postsynaptic receptors but also on the concentrations of presynaptic transmitter and how much transmitter is loaded into the vesicle.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [51]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Efron, B., & Tibshirani, R. (1986) · Statistical Science · doi:10.1214/ss/1177013815 · Cited by 6,033 · see citing works
Identification and characterization of the vesicular GABA transporter
McIntire, S. L., Reimer, R. J., Schuske, K. R., Edwards, R. H., & Jørgensen, E. M. (1997) · Nature · doi:10.1038/39908 · Cited by 867 · see citing works
Corelease of Two Fast Neurotransmitters at a Central Synapse
Jonas, P., Bischofberger, J., & Sandkühler, J. (1998) · Science · doi:10.1126/science.281.5375.419 · Cited by 784 · see citing works
Glycine transporters are differentially expressed among CNS cells
Zafra, F., Aragón, C., Olivares, L., Danbolt, N. C., Giménez, C., & Storm‐Mathisen, J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03952.1995 · Cited by 521 · see citing works
The Neurotransmitter Cycle and Quantal Size
Edwards, R. H. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.001 · Cited by 363 · see citing works
Synthesis, storage and release of [14C]acetylcholine in isolated rat diaphragm muscles
Potter, L. T. (1970) · The Journal of Physiology · doi:10.1113/jphysiol.1970.sp009003 · Cited by 359 · see citing works
Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex
Wenthold, R. J., Huie, D., Altschuler, R. A., & Reeks, K. A. (1987) · Neuroscience · doi:10.1016/0306-4522(87)92968-x · Cited by 309 · see citing works
Gomeza, J., Ohno, K., Hülsmann, S., Armsen, W., Eulenburg, V., Richter, D. W., Laube, B., & Betz, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00673-1 · Cited by 298 · see citing works
Target-Dependent Use of Coreleased Inhibitory Transmitters at Central Synapses
Dugué, G. P., Dumoulin, A., Triller, A., & Dieudonné, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1500-05.2005 · Cited by 245 · see citing works
Jin, H., Wu, H., Osterhaus, G., Wei, J., Davis, K., Sha, D., Floor, E., Hsu, C.-C., Kopke, R. D., & Wu, J.-Y. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0730698100 · Cited by 243 · see citing works
Developmental switch from GABA to glycine release in single central synaptic terminals
Nabekura, J., Katsurabayashi, S., Kakazu, Y., Shibata, S., Matsubara, A., Jinno, S., Mizoguchi, Y., Sasaki, A., & Ishibashi, H. (2004) · Nature Neuroscience · doi:10.1038/nn1170 · Cited by 228 · see citing works
Otis, T., Wu, Y., & Trussell, L. O. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01634.1996 · Cited by 228 · see citing works
Self-citationChéry, N., & Koninck, Y. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07342.1999 · Cited by 226 · see citing works
Neuronal Glutamate Uptake Contributes to GABA Synthesis and Inhibitory Synaptic Strength
Mathews, G. C., & Diamond, J. S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02040.2003 · Cited by 204 · see citing works
Dynamic Regulation of Synaptic GABA Release by the Glutamate-Glutamine Cycle in Hippocampal Area CA1
Liang, S., Carlson, G. C., & Coulter, D. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0329-06.2006 · Cited by 203 · see citing works
GABA and glycine in synaptic vesicles: storage and transport characteristics
Burger, P. M., Hell, J. W., Mehl, E., Krasel, C., Lottspeich, F., & Jahn, R. (1991) · Neuron · doi:10.1016/0896-6273(91)90267-4 · Cited by 193 · see citing works
MEASUREMENT OF γ‐AMINOBUTYRIC ACID IN ISOLATED NERVE CELLS OF CAT CENTRAL NERVOUS SYSTEM
Otsuka, M., Obata, K., Miyata, Y., & Tanaka, Y. (1971) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1971.tb00567.x · Cited by 188 · see citing works
Axon Initial Segment Ca2+ Channels Influence Action Potential Generation and Timing
Bender, K. J., & Trussell, L. O. (2009) · Neuron · doi:10.1016/j.neuron.2008.12.004 · Cited by 180 · see citing works
Self-citationA Single Packet of Transmitter Does Not Saturate Postsynaptic Glutamate Receptors
Ishikawa, T., Sahara, Y., & Takahashi, T. (2002) · Neuron · doi:10.1016/s0896-6273(02)00692-x · Cited by 176 · see citing works
Intracellular Patch Electrochemistry: Regulation of Cytosolic Catecholamines in Chromaffin Cells
Mosharov, E. V., Gong, L., Khanna, B., Sulzer, D. L., & Lindau, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05835.2003 · Cited by 145 · see citing works
Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices.
Vincent, P., & Marty, A. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021484 · Cited by 139 · see citing works
Staggered development of GABAergic and glycinergic transmission in the MNTB
Awatramani, G. B., Turecek, R., & Trussell, L. O. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00798.2004 · Cited by 138 · see citing works
Self-citationGlycinergic Transmission Shaped by the Corelease of GABA in a Mammalian Auditory Synapse
Lu, T., Rubio, M. E., & Trussell, L. O. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.010 · Cited by 123 · see citing works
Self-citationWhy glycine transporters have different stoichiometries
Supplisson, S., & Roux, M. J. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03251-9 · Cited by 122 · see citing works
Ji, F., Kanbara, N., & Obata, K. (1999) · Neuroscience Research · doi:10.1016/s0168-0102(99)00011-5 · Cited by 118 · see citing works
Self-inhibition of olfactory bulb neurons
Smith, T. C., & Jahr, C. E. (2002) · Nature Neuroscience · doi:10.1038/nn882 · Cited by 105 · see citing works
Plasticity of rat central inhibitory synapses through GABA metabolism
Engel, D., Pahner, I., Schulze, K., Frahm, C., Jarry, H., Ahnert‐Hilger, G., & Draguhn, A. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00473.x · Cited by 104 · see citing works
Calcium- and Syntaxin 1-mediated Trafficking of the Neuronal Glycine Transporter GLYT2
Geerlings, A., Núñez, E., López‐Corcuera, B., & Aragón, C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010602200 · Cited by 98 · see citing works
Rousseau, F., Aubrey, K. R., & Supplisson, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0509-08.2008 · Cited by 97 · see citing works
Mugnaini, E., Berrebi, A. S., Dahl, A. L., & Morgan, J. I. (1987) · PubMed · Cited by 95 · see citing works
Bradaïa, A., Schlichter, R., & Trouslard, J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.068858 · Cited by 84 · see citing works
der Kloot, W. V. (2003) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2003.10.003 · Cited by 84 · see citing works
Dynamic Storage of Dopamine in Rat Brain Synaptic Vesicles In Vitro
Floor, E., Leventhal, P. S., Wang, Y., Meng, L., & Chen, W. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.64020689.x · Cited by 79 · see citing works
Rubio, M. E. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20248 · Cited by 77 · see citing works
Kinetics of Synaptic Vesicle Refilling with Neurotransmitter Glutamate
Hori, T., & Takahashi, T. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.013 · Cited by 74 · see citing works
Diana, M. A., & Marty, A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05906.2003 · Cited by 73 · see citing works
Post-translational Regulation of l-Glutamic Acid Decarboxylase in the Brain
Wei, J., & Wu, J. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9600-5 · Cited by 73 · see citing works
Kirmse, K., & Kirischuk, S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0589-06.2006 · Cited by 72 · see citing works
Kanaani, J., El-Husseini, A., Aguilera-Moreno, A., Diacovo, J. M., Bredt, D. S., & Bækkeskov, S. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200205053 · Cited by 71 · see citing works
The Time Course of Transmitter at Glycinergic Synapses onto Motoneurons
Beato, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0581-08.2008 · Cited by 70 · see citing works
A neuroprotective role for polyamines in a Xenopus tadpole model of epilepsy
Bell, M. R., Belarde, J. A., Johnson, H. F., & Aizenman, C. D. (2011) · Nature Neuroscience · doi:10.1038/nn.2777 · Cited by 67 · see citing works
How Does a Vesicle Know It Is Full?
Williams, J. H. (1997) · Neuron · doi:10.1016/s0896-6273(00)80308-6 · Cited by 59 · see citing works
Roberts, M. T., & Trussell, L. O. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00312.2010 · Cited by 57 · see citing works
Self-citationKuo, S. P., & Trussell, L. O. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.039 · Cited by 57 · see citing works
Self-citationUptake of Glycine into Synaptic Vesicles Isolated from Rat Spinal Cord
Christensen, H., Fykse, E. M., & Fonnum, F. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb01941.x · Cited by 56 · see citing works
Drug-induced GABA transporter currents enhance GABA release to induce opioid withdrawal behaviors
Bagley, E. E., Hacker, J., Chefer, V. I., Mallet, C., McNally, G. P., Chieng, B. C. H., Perroud, J., Shippenberg, T. S., & Christie, M. J. (2011) · Nature Neuroscience · doi:10.1038/nn.2940 · Cited by 53 · see citing works
Inhibition of γ-aminobutyrate and glycine uptake into synaptic vesicles
Christensen, H., Fykse, E. M., & Fonnum, F. (1991) · European Journal of Pharmacology Molecular Pharmacology · doi:10.1016/s0922-4106(05)80040-9 · Cited by 51 · see citing works
The concentration of GABA within inhibitory nerve terminals
Fonnum, F., & Walberg, F. (1973) · Brain Research · doi:10.1016/0006-8993(73)90724-5 · Cited by 49 · see citing works
Conductance states activated by glycine and GABA in rat cultured spinal neurones
Smith, S. M., Zorec, R., & McBurney, R. N. (1989) · The Journal of Membrane Biology · doi:10.1007/bf01870424 · Cited by 48 · see citing works
Ágoston, D. V., Kosh, J. W., Lisziewicz, J., & Whittaker, V. P. (1985) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1985.tb07144.x · Cited by 47 · see citing works
Readily releasable pool of synaptic vesicles measured at single synaptic contacts
Trigo, F. F., Sakaba, T., Ogden, D., & Marty, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209798109 · Cited by 46 · see citing works
P2Y Purinergic Regulation of the Glycine Neurotransmitter Transporters
Jiménez, E., Zafra, F., Pérez‐Sen, R., Delicado, E. G., Miras‐Portugal, M. T., Aragón, C., & López‐Corcuera, B. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.167056 · Cited by 45 · see citing works
Searl, T. J., Prior, C., & Marshall, I. G. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018868 · Cited by 45 · see citing works
Two Distinct Types of Inhibition Mediated by Cartwheel Cells in the Dorsal Cochlear Nucleus
Mancilla, J. G., & Manis, P. B. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91272.2008 · Cited by 41 · see citing works
Whittaker, V. P. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb27185.x · Cited by 38 · see citing works
Inhibitors of GlyT1 and GlyT2 differentially modulate inhibitory transmission
Xu, T., Gong, N., & Xu, T. (2005) · Neuroreport · doi:10.1097/00001756-200508010-00019 · Cited by 37 · see citing works
Fidelity of Complex Spike-Mediated Synaptic Transmission between Inhibitory Interneurons
Roberts, M. T., Bender, K. J., & Trussell, L. O. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2226-08.2008 · Cited by 37 · see citing works
Self-citationCabeza, R. D. J., & Collier, B. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb13237.x · Cited by 37 · see citing works
Porter, T. G., & Martin, D. L. (1985) · Biochemical Pharmacology · doi:10.1016/0006-2952(85)90207-2 · Cited by 32 · see citing works
Fornés, A., Núñez, E., Alonso‐Torres, P., Aragón, C., & López‐Corcuera, B. (2008) · Biochemical Journal · doi:10.1042/bj20071018 · Cited by 32 · see citing works
Development of synaptic inhibition in glycine transporter 2 deficient mice
Latal, A. T., Kremer, T., Gomeza, J., Eulenburg, V., & Hülsmann, S. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.04.005 · Cited by 27 · see citing works
Determination of gamma‐aminobutyric acid in single nerve cells of cat central nervous system
Obata, K., Otsuka, M., & Tanaka, Y. (1970) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1970.tb00550.x · Cited by 27 · see citing works
Chang, Y., Xie, Y., & Weiss, D. S. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0471c.xd · Cited by 24 · see citing works
Gene Transfer to the Developing Mouse Inner Ear by In Vivo Electroporation
Wang, L., Jiang, H., & Brigande, J. V. (2012) · Journal of Visualized Experiments · doi:10.3791/3653 · Cited by 24 · see citing works
Transmitter Metabolism as a Mechanism of Synaptic Plasticity: A Modeling Study
Axmacher, N., Stemmler, M., Engel, D., Draguhn, A., & Ritz, R. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00797.2003 · Cited by 23 · see citing works
Dericioğlu, N., Garganta, C. L., Petroff, O. A. C., Mendelsohn, D., & Williamson, A. (2008) · Neurochemistry International · doi:10.1016/j.neuint.2008.04.006 · Cited by 17 · see citing works
Beato, M., Burzomato, V., & Sivilotti, L. G. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.126888 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mechanisms and functions of GABA co-release
Tritsch, N. X., Granger, A. J., & Sabatini, B. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.21 · Cited by 261 · see citing works
Dual-transmitter neurons: functional implications of co-release and co-transmission
Vaaga, C. E., Borisovska, M., & Westbrook, G. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.04.010 · Cited by 221 · see citing works
The Role of Amino Acids in Neurotransmission and Fluorescent Tools for Their Detection
Dalangin, R., Kim, A., & Campbell, R. E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176197 · Cited by 211 · see citing works
Tritsch, N. X., Oh, W., Gu, C., & Sabatini, B. L. (2014) · eLife · doi:10.7554/elife.01936 · Cited by 197 · see citing works
The role of co-neurotransmitters in sleep and wake regulation
Oh, J. Y., Petersen, C., Walsh, C. M., Bittencourt, J. C., Neylan, T. C., & Grinberg, L. T. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0291-2 · Cited by 87 · see citing works
Serotonergic Regulation of Excitability of Principal Cells of the Dorsal Cochlear Nucleus
Tang, Z., & Trussell, L. O. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4825-14.2015 · Cited by 82 · see citing works
Self-citationIntrinsic Circuits in the Lateral Central Amygdala
Hunt, S., Sun, Y., Kucukdereli, H., Klein, R., & Sah, P. (2017) · eNeuro · doi:10.1523/eneuro.0367-16.2017 · Cited by 74 · see citing works
Tien, N.-W., Kim, T., & Kerschensteiner, D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.025 · Cited by 67 · see citing works
Egashira, Y., Takase, M., Watanabe, S., Ishida, J., Fukamizu, A., Kaneko, R., Yanagawa, Y., & Takamori, S. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604527113 · Cited by 62 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Pietrancosta, N., Djibo, M., Daumas, S., Mestikawy, S. E., & Erickson, J. D. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01912-7 · Cited by 59 · see citing works
Corelease of Inhibitory Neurotransmitters in the Mouse Auditory Midbrain
Moore, L. A., & Trussell, L. O. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1125-17.2017 · Cited by 53 · see citing works
Self-citationDicken, M. S., Hughes, A. R., & Hentges, S. T. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13076 · Cited by 51 · see citing works
Regulation of interneuron excitability by gap junction coupling with principal cells
Apostolides, P. F., & Trussell, L. O. (2013) · Nature Neuroscience · doi:10.1038/nn.3569 · Cited by 48 · see citing works
Self-citationGlycine Transporters and Its Coupling with NMDA Receptors
Zafra, F., Ibáñez, I., Bartolomé‐Martín, D., Piniella, D., Arribas-Blázquez, M., & Giménez, C. (2017) · Advances in neurobiology · doi:10.1007/978-3-319-55769-4_4 · Cited by 48 · see citing works
Nerlich, J., Kuenzel, T., Keine, C., Korenić, A., Rübsamen, R., & Milenković, I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0719-14.2014 · Cited by 41 · see citing works
Gephyrin and the regulation of synaptic strength and dynamics at glycinergic inhibitory synapses
Álvarez, F. J. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.09.003 · Cited by 40 · see citing works
de Juan‐Sanz, J., Núñez, E., Villarejo-López, L., Pérez-Hernández, D., Rodriguez-Fraticelli, A., López‐Corcuera, B., Vázquez, J., & Aragón, C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1532-13.2013 · Cited by 39 · see citing works
Cytosolic Transmitter Concentration Regulates Vesicle Cycling at Hippocampal GABAergic Terminals
Wang, L., Tu, P., Bonet, L., Aubrey, K. R., & Supplisson, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.021 · Cited by 37 · see citing works
Spontaneous Activity Defines Effective Convergence Ratios in an Inhibitory Circuit
Lu, H.-W., & Trussell, L. O. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3499-15.2016 · Cited by 32 · see citing works
Self-citationArribas-González, E., de Juan‐Sanz, J., Aragón, C., & López‐Corcuera, B. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.587055 · Cited by 31 · see citing works
Presynaptic control of inhibitory neurotransmitter content in VIAAT containing synaptic vesicles
Aubrey, K. R. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.06.002 · Cited by 30 · see citing works
de Juan‐Sanz, J., Núñez, E., Zafra, F., Berrocal, M., Corbacho‐Cuello, I., Ibáñez, I., Arribas-González, E., Marcos, D., López‐Corcuera, B., Mata, A. M., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.586966 · Cited by 30 · see citing works
Heterogeneous Signaling at GABA and Glycine Co-releasing Terminals
Aubrey, K. R., & Supplisson, S. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00040 · Cited by 27 · see citing works
Jappy, D., Valiullina, F., Draguhn, A., & Rozov, A. V. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00004 · Cited by 25 · see citing works
Fischer, A. U., Müller, N. I. C., Deller, T., Turco, D. D., Fisch, J. O., Griesemer, D., Kattler, K., Maraslioglu-Sperber, A., Roemer, V., Xu‐Friedman, M. A., et al. (2019) · The Journal of Physiology · doi:10.1113/jp277566 · Cited by 24 · see citing works
Brill, S. E., Maraslioglu-Sperber, A., Kurz, C., Kramer, F., Fuhr, M. F., Singh, A., & Friauf, E. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.560008 · Cited by 23 · see citing works
Vesicular GABA Uptake Can Be Rate Limiting for Recovery of IPSCs from Synaptic Depression
Yamashita, M., Kawaguchi, S., Hori, T., & Takahashi, T. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.080 · Cited by 23 · see citing works
Excitation by Axon Terminal GABA Spillover in a Sound Localization Circuit
Weisz, C. J. C., Rubio, M. E., Givens, R. S., & Kandler, K. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1132-15.2016 · Cited by 22 · see citing works
Activity-dependent modulation of inhibitory synaptic kinetics in the cochlear nucleus
Nerlich, J., Keine, C., Ruebsamen, R., Burger, R. M., & Milenković, I. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00145 · Cited by 20 · see citing works
Superficial stellate cells of the dorsal cochlear nucleus
Apostolides, P. F., & Trussell, L. O. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00063 · Cited by 18 · see citing works
Self-citationStefanescu, R. A., & Shore, S. E. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00075 · Cited by 17 · see citing works
Chemical synaptic transmission onto superficial stellate cells of the mouse dorsal cochlear nucleus
Apostolides, P. F., & Trussell, L. O. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00821.2013 · Cited by 16 · see citing works
Self-citationP2X receptors up-regulate the cell-surface expression of the neuronal glycine transporter GlyT2
Villarejo-López, L., Jiménez, E., Bartolomé‐Martín, D., Zafra, F., Lapunzina, P. D., Aragón, C., & López‐Corcuera, B. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.07.018 · Cited by 15 · see citing works
E3 ubiquitin ligases LNX1 and LNX2 are major regulators of the presynaptic glycine transporter GlyT2
de la Rocha‐Muñoz, A., Núñez, E., Arribas-González, E., López‐Corcuera, B., Aragón, C., & de Juan‐Sanz, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-51301-x · Cited by 15 · see citing works
Glycine transporters GlyT1 and GlyT2 are differentially modulated by glycogen synthase kinase 3β
Jiménez, E., Núñez, E., Ibáñez, I., Zafra, F., Aragón, C., & Giménez, C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.09.023 · Cited by 14 · see citing works
Jarvie, B. C., King, C. M., Hughes, A. R., Dicken, M. S., Dennison, C. S., & Hentges, S. T. (2016) · The Journal of Physiology · doi:10.1113/jp273020 · Cited by 14 · see citing works
Effects of cochlear ablation on amino acid levels in the rat cochlear nucleus and superior olive
Godfrey, D. A., Jin, Y., Liu, X., & Godfrey, M. A. (2013) · Hearing Research · doi:10.1016/j.heares.2013.11.005 · Cited by 14 · see citing works
Turecek, J., & Regehr, W. G. (2020) · eLife · doi:10.7554/elife.61672 · Cited by 13 · see citing works
Fischl, M. J., Weimann, S. R., Kearse, M. G., & Burger, R. M. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00640.2013 · Cited by 12 · see citing works
Glycine Transporters in Glia Cells: Structural Studies
López‐Corcuera, B., Benito-Muñoz, C., & Aragón, C. (2017) · Advances in neurobiology · doi:10.1007/978-3-319-55769-4_2 · Cited by 11 · see citing works
Flux coupling, not specificity, shapes the transport and phylogeny of SLC6 glycine transporters
Guellec, B. L., Rousseau, F., Bied, M., & Supplisson, S. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2205874119 · Cited by 11 · see citing works
Developmental Shift of Inhibitory Transmitter Content at a Central Auditory Synapse
Nerlich, J., Rübsamen, R., & Milenković, I. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00211 · Cited by 10 · see citing works
Activity and Cytosolic Na + Regulate Synaptic Vesicle Endocytosis
Zhu, Y. F., Li, D., & Huang, H. Y. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0119-20.2020 · Cited by 10 · see citing works
Supraspinal glycinergic neurotransmission in pain: A scoping review of current literature
Fenech, C. E., Winters, B. L., Otsu, Y., & Aubrey, K. R. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16191 · Cited by 9 · see citing works
Glycinergic transmission modulates GABAergic inhibition in the avian auditory pathway
Fischl, M. J., & Burger, R. M. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00019 · Cited by 9 · see citing works
Ngodup, T., Irie, T., Elkins, S. P., & Trussell, L. O. (2023) · eLife · doi:10.7554/elife.89520 · Cited by 8 · see citing works
Self-citationThe presynaptic glycine transporter GlyT2 is regulated by the Hedgehog pathway in vitro and in vivo
de la Rocha‐Muñoz, A., Núñez, E., Vishwanath, A. A., Gomez‐Lopez, S., Dhanasobhon, D., Rebola, N., López‐Corcuera, B., de Juan‐Sanz, J., & Aragón, C. (2021) · Communications Biology · doi:10.1038/s42003-021-02718-6 · Cited by 8 · see citing works
Dumontier, D., Mailhes‐Hamon, C., Supplisson, S., & Dieudonné, S. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1060189 · Cited by 8 · see citing works
Identification of Amacrine Neurons with a Glycinergic and Gabaergic Phenotype in the Mouse Retina
Pérez-León, J. A., Espinal‐Centeno, A., Mendoza-Gonzalez, Z., Camacho, A., Lopez, A. B., Perez, R. A., & Miranda, M. (2022) · Medical Research Archives · doi:10.18103/mra.v10i1.2624 · Cited by 7 · see citing works
McKarns, S. C. (2022) · Current Clinical Pharmacology · doi:10.2174/2772432817666220301104118 · Cited by 7 · see citing works
Using Cortical Neuron Markers to Target Cells in the Dorsal Cochlear Nucleus
Malfatti, T., Ciralli, B., Hilscher, M. M., Edwards, S. J., Kullander, K., Leão, R. N., & Leão, K. E. (2021) · eNeuro · doi:10.1523/eneuro.0413-20.2020 · Cited by 7 · see citing works
The Cochlear Nucleus as a Generator of Tinnitus-Related Signals
Kaltenbach, J. A., & Godfrey, D. A. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190849061.013.8 · Cited by 6 · see citing works
Godfrey, D. A., Mikesell, N. L., Godfrey, T. G., & Kaltenbach, J. A. (2019) · Hearing Research · doi:10.1016/j.heares.2019.107841 · Cited by 4 · see citing works
Thomas, J. A., Morris, P. A., & Seigel, E. (2018) · World Journal of Neuroscience · doi:10.4236/wjns.2018.82019 · Cited by 4 · see citing works
Mafa-dependent GABAergic activity promotes mouse neonatal apneas
Lecoin, L., Dempsey, B., Garancher, A., Bourane, S., Ruffault, P.-L., Morin‐Surun, M., Rocques, N., Goulding, M., Eychène, A., Pouponnot, C., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30825-3 · Cited by 4 · see citing works
Al-Yaari, M., Onogi, C., Yamada, R., Adachi, R., Kondo, D., & Kuba, H. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0884-21.2021 · Cited by 3 · see citing works
Effects of brainstem lesions on amino acid levels in the rat cochlear nucleus
Godfrey, D. A., Farms, W. B., Polensek, S. H., Dunn, J. D., & Godfrey, T. G. (2021) · Hearing Research · doi:10.1016/j.heares.2021.108187 · Cited by 3 · see citing works
Heterogeneous distribution and utilization of inhibitory neurotransmitter transporters
(2015) · Neurotransmitter · doi:10.14800/nt.491 · Cited by 3 · see citing works
Ngodup, T., Irie, T., Elkins, S. P., & Trussell, L. O. (2023) · eLife · doi:10.7554/elife.89520.1 · Cited by 2 · see citing works
Self-citationPizzi, E., Hofmann, L. N., Singh, A., & Friauf, E. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1625868 · Cited by 1 · see citing works
Valiullina, F., Jappy, D., & Rozov, A. V. (2016) · BioNanoScience · doi:10.1007/s12668-016-0310-1 · Cited by 1 · see citing works
Russo, A. D., Riva, S. I., Catto, V., Casella, M., Dessanai, M., Pizzamiglio, F., Majocchi, B., Cellucci, S., Vettor, G., Fassini, G. M., et al. (2017) · European Heart Journal · doi:10.1093/eurheartj/ehx502.p1533
Development and Function of Inhibitory Circuitry in the Avian Auditory Brainstem
Burger, R. M. (2017) · Springer handbook of auditory research · doi:10.1007/978-3-319-21530-3_5
Ngodup, T., Irie, T., Elkins, S. P., & Trussell, L. O. (2023) · eLife · doi:10.7554/elife.89520.2.sa4
Self-citationLee, J., Brockway, B., & Kandler, K. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2520749123
- Authors
- Apostolides, P. F., & Trussell, L. O.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-03-13
- Volume
- 33
- Issue
- 11
- Pages
- 4768-4781
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3639006
- OpenAlex
- W2055623289
- Cited by
- 77
- References
- 66
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 10 · 2022: 4 · 2021: 5 · 2020: 4 · 2019: 4 · 2018: 5 · 2017: 9 · 2016: 10 · 2015: 4 · 2014: 12 · 2013: 5
- FWCI
- 5.07
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Deafness and Other Communication Disorders (F31DC012222, P30DC005983, R01DC004450)
- National Institute of Neurological Disorders and Stroke (R01NS028901)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Keywords
- glycine transporter 2, glutamic acid decarboxylase, cartwheel cells, dorsal cochlear nucleus, glutamate uncaging, inhibitory synapses, neurotransmitter transporters
- MeSH terms
- Channelrhodopsins, Animals, Benzamides, Biophysics, Electric Stimulation, Female, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Glutamates, Glycine, Indoles, Interneurons, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Mice, Transgenic, Models, Neurological, Neural Inhibition, Synaptic Transmission, Pregnancy, Pyridazines, Strychnine, Synapses, Synaptic Vesicles, Tetrodotoxin, Time Factors, Cochlear Nucleus, Patch-Clamp Techniques, Glycine Agents, Excitatory Amino Acid Antagonists, GABA Antagonists, Sodium Channel Blockers, Glycine Plasma Membrane Transport Proteins, Mice, Inhibitory Postsynaptic Potentials, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
