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Staggered Development of GABAergic and Glycinergic Transmission in the MNTB
Abstract
Maturation of some brain stem and spinal inhibitory systems is characterized by a shift from GABAergic to glycinergic transmission. Little is known about how this transition is expressed in terms of individual axonal inputs and synaptic sites. We have explored this issue in the rat medial nucleus of the trapezoid body (MNTB). Synaptic responses at postnatal days 5-7 (P5-P7) were small, slow, and primarily mediated by GABA(A) receptors. By P8-P12, an additional, faster glycinergic component emerged. At these ages, GABA(A), glycine, or both types of receptors mediated transmission, even at single synaptic sites. Thereafter, glycinergic development greatly accelerated. By P25, evoked inhibitory postsynaptic currents (IPSCs) were 10 times briefer and 100 times larger than those measured in the youngest group, suggesting a proliferation of synaptic inputs activating fast-kinetic receptors. Glycinergic miniature IPSCs (mIPSCs) increased markedly in size and decay rate with age. GABAergic mIPSCs also accelerated, but declined slightly in amplitude. Overall, the efficacy of GABAergic inputs showed little maturation between P5 and P20. Although gramicidin perforated-patch recordings revealed that GABA or glycine depolarized P5-P7 cells but hyperpolarized P14-P15 cells, the young depolarizing inputs were not suprathreshold. In addition, vesicle-release properties of inhibitory axons also matured: GABAergic responses in immature rats were highly asynchronous, while in older rats, precise, phasic glycinergic IPSCs could transmit even with 500-Hz stimuli. Thus development of inhibition is characterized by coordinated modifications to transmitter systems, vesicle release kinetics, Cl- gradients, receptor properties, and numbers of synaptic inputs. The apparent switch in GABA/glycine transmission was predominantly due to enhanced glycinergic function.
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“By adulthood, both transmitters are inhibitory, activating their cognate chloride permeable ligand-gated ion channels, and hyperpolarizing their postsynaptic targets.48”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [48]
Citations
Cites
Excitatory actions of gaba during development: the nature of the nurture
Ben-Ari, Y. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn920 · Cited by 2,448
Giant synaptic potentials in immature rat CA3 hippocampal neurones.
Ben‐Ari, Y., Cherubini, E., Corradetti, R., & Gaiarsa, J. L. (1989) · The Journal of Physiology · doi:10.1113/jphysiol.1989.sp017762 · Cited by 1,317
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
Ganguly, K., Schinder, A. F., Wong, S. T., & Poo, M. (2001) · Cell · doi:10.1016/s0092-8674(01)00341-5 · Cited by 719
Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain.
Malosio, M. L., Marquèze‐Pouey, B., Kuhse, J., & Betz, H. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07779.x · Cited by 557
Two components of transmitter release at a central synapse.
Goda, Y., & Stevens, C. F. (1994) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.91.26.12942 · Cited by 529
Taschenberger, H., & von Gersdorff, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09162.2000 · Cited by 486
Optimizing Synaptic Architecture and Efficiency for High-Frequency Transmission
Taschenberger, H., Leão, R. M., Rowland, K. C., Spirou, G. A., & von Gersdorff, H. (2002) · Neuron · doi:10.1016/s0896-6273(02)01137-6 · Cited by 389
Short-term plasticity at the calyx of held
von Gersdorff, H., & Borst, J. G. G. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn705 · Cited by 388
Glycine receptor heterogeneity in rat spinal cord during postnatal development.
Becker, C., Hoch, W., & Betz, H. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb03255.x · Cited by 379
Sätzler, K., Söhl, L. F., Bollmann, J. H., Borst, J. G., Frotscher, M., Sakmann, B., & Lübke, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10567.2002 · Cited by 358
Contribution of the Kv3.1 potassium channel to high‐frequency firing in mouse auditory neurones
Wang, L., Gan, L., Forsythe, I. D., & Kaczmarek, L. K. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.183bo.x · Cited by 357
Vicini, S., Ferguson, C., Prybylowski, K., Kralic, J. E., Morrow, A. L., & Homanics, G. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03009.2001 · Cited by 309
Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse
Tureček, R., & Trussell, L. O. (2001) · Nature · doi:10.1038/35079084 · Cited by 305
Pre‐ and postnatal development of efferent connections of the cochlear nucleus in the rat
Kandler, K., & Friauf, E. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903280202 · Cited by 291
Glycine-receptor activation is required for receptor clustering in spinal neurons
Kirsch, J., & Betz, H. (1998) · Nature · doi:10.1038/33694 · Cited by 263
Development of Glycinergic Synaptic Transmission to Rat Brain Stem Motoneurons
Singer, J. H., Talley, E. M., Bayliss, D. A., & Berger, A. J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.5.2608 · Cited by 256
Regulation of Intracellular Chloride by Cotransporters in Developing Lateral Superior Olive Neurons
Kakazu, Y., Akaike, N., Komiyama, S., & Nabekura, J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-08-02843.1999 · Cited by 253
Delayed Release of Neurotransmitter from Cerebellar Granule Cells
Atluri, P. P., & Regehr, W. G. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08214.1998 · Cited by 250
A Developmental Shift from GABAergic to Glycinergic Transmission in the Central Auditory System
Kotak, V. C., Korada, S., Schwartz, I. R., & Sanes, D. H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04646.1998 · Cited by 247
Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation
Kim, G., & Kandler, K. (2003) · Nature Neuroscience · doi:10.1038/nn1015 · Cited by 233
Two Heteromeric Kv1 Potassium Channels Differentially Regulate Action Potential Firing
Dodson, P. D., Barker, M., & Forsythe, I. D. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-06953.2002 · Cited by 230
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
Keller, A. F., Coull, J. A. M., Chéry, N., Poisbeau, P., & Koninck, Y. D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-07871.2001 · Cited by 227
GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil
Roberts, R. C., & Ribak, C. E. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902580207 · Cited by 227
Inhibitory Transmission Mediated by Asynchronous Transmitter Release
Lu, T., & Trussell, L. O. (2000) · Neuron · doi:10.1016/s0896-6273(00)81204-0 · Cited by 223
Tia, S., Wang, J. F., Kotchabhakdi, N., & Vicini, S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-11-03630.1996 · Cited by 214
Iwasaki, S., & Takahashi, T. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.419bn.x · Cited by 207
Balakrishnan, V., Becker, M., Löhrke, S., Nothwang, H. G., Güresir, E., & Friauf, E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-04134.2003 · Cited by 206
Perrais, D., & Ropert, N. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-02-00578.1999 · Cited by 188
Distinct Roles of Kv1 and Kv3 Potassium Channels at the Calyx of Held Presynaptic Terminal
Ishikawa, T., Nakamura, Y., Saitoh, N., Li, W., Iwasaki, S., & Takahashi, T. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10445.2003 · Cited by 181
Ehrlich, I., Löhrke, S., & Friauf, E. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00121.x · Cited by 180
Hollrigel, G. S., & Soltész, I. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05119.1997 · Cited by 169
Otsu, Y., Shahrezaei, V., Li, B., Raymond, L. A., Delaney, K. R., & Murphy, T. H. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4452-03.2004 · Cited by 169
Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem
Iwasaki, S., & Takahashi, T. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00861.x · Cited by 169
Delayed release of transmitter at the frog neuromuscular junction
Rahamimoff, R., & Yaari, Y. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010084 · Cited by 165
Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive
Adams, J. C., & Mugnaini, E. (1990) · Hearing Research · doi:10.1016/0378-5955(90)90109-3 · Cited by 157
Dehay, C., Giroud, P., Berland, M., Killackey, H. P., & Kennedy, H. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960325)367:1 · Cited by 157
Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture
Obata, K., Oide, M., & Tanaka, H. (1978) · Brain Research · doi:10.1016/0006-8993(78)90447-x · Cited by 150
Heterogeneity of Glycine Receptors and Their Messenger RNAs in Rat Brain and Spinal Cord
Akagi, H., & Miledi, R. (1988) · Science · doi:10.1126/science.2845580 · Cited by 130
Neonatal development of the rat visual cortex: synaptic function of GABAa receptor α subunits
Bosman, L. W. J., Rosahl, T. W., & Brussaard, A. B. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.026534 · Cited by 126
Development of glycine- and GABA-gated currents in rat spinal motoneurons
Gao, B.-X., & Ziskind‐Conhaim, L. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.1.113 · Cited by 113
Monsivais, P., Yang, L., & Rubel, E. W. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02954.2000 · Cited by 110
Reciprocal developmental regulation of presynaptic ionotropic receptors
Tureček, R., & Trussell, L. O. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.212419699 · Cited by 106
Draguhn, A., & Heinemann, U. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.6.3983 · Cited by 97
Joshi, I., Shokralla, S., Titis, P., & Wang, L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1074-03.2004 · Cited by 91
Akagi, H., Hirai, K., & Hishinuma, F. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)80383-e · Cited by 88
Mixed excitatory and inhibitory GABA‐mediated transmission in chick cochlear nucleus
Lu, T., & Trussell, L. O. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-1-00125.x · Cited by 87
Inhibitory Control at a Synaptic Relay
Awatramani, G. B., Tureček, R., & Trussell, L. O. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5144-03.2004 · Cited by 82
Distribution patterns of mRNAs encoding glycine receptor channels in the developing rat spinal cord
Watanabe, E., & Akagi, H. (1995) · Neuroscience Research · doi:10.1016/0168-0102(95)00972-v · Cited by 75
Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse
Sahara, Y., & Takahashi, T. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00189.x · Cited by 70
Piechotta, K., Weth, F., Harvey, R. J., & Friauf, E. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1319 · Cited by 65
Leão, R. M., & von Gersdorff, H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.87.5.2297 · Cited by 63
Elezgarai, I., Díez, J., Puente, N., Azkue, J. J., Benı́tez, R., Bilbao, A., Knöpfel, T., Doñate-Oliver, F., & Grandes, P. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00068-x · Cited by 61
Development of spontaneous synaptic transmission in the rat spinal cord.
Gao, B.-X., Cheng, G., & Ziskind-Conhaim, L. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.5.2277 · Cited by 59
Ml, C., de Cabo, C., Wisden, W., Juiz, J. M., & Merlo, D. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00525-x · Cited by 57
Lowry, C. A., Richardson, C., Zoeller, T. R., Miller, L. J., Muske, L. E., & Moore, F. L. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970818)385:1 · Cited by 56
Mu�oz, A., Liu, X.-B., & Jones, E. G. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990712)409:4 · Cited by 50
Jüttner, R., Meier, J. C., & Grantyn, R. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01587.x · Cited by 44
Chuhma, N., Koyano, K., & Ohmori, H. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0093m.x · Cited by 42
Physiology and pharmacology of native glycine receptors in developing rat auditory brainstem neurons
Kungel, M., & Friauf, E. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00087-4 · Cited by 40
Lim, R., Oleskevich, S., Few, A. P., Leão, R. N., & Walmsley, B. D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.035071 · Cited by 40
Sato, K., Kuriyama, H., & Altschuler, R. A. (1995) · Hearing Research · doi:10.1016/0378-5955(95)00156-5 · Cited by 28
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Metadata
- Authors
- Awatramani, G. B., Turecek, R., & Trussell, L. O.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2005-02
- Volume
- 93
- Issue
- 2
- Pages
- 819-828
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2025066952
- Cited by
- 138
- References
- 63
- Citations by year
- 2026: 2 · 2025: 5 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 2 · 2019: 10 · 2018: 7 · 2017: 6 · 2016: 6 · 2015: 6 · 2014: 14 · 2013: 11 · 2012: 3
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (DC04450, R01DC004450)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- medial nucleus of the trapezoid body, GABAergic neurotransmission, glycinergic transmission, inhibitory postsynaptic currents, miniature IPSCs, synapse maturation, GABAA receptor, glycine receptor, chloride gradient, postnatal development
- MeSH terms
- Age Factors, Animals, Brain Stem, gamma-Aminobutyric Acid, Glycine, Synaptic Transmission, Receptors, GABA-A, Rats, Wistar, Receptors, Glycine, Rats, GABA-A Receptor Agonists, In Vitro Techniques
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