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Retrograde Regulation of GABA Transmission by the Tonic Release of Oxytocin and Endocannabinoids Governs Postsynaptic Firing
Open accessAbstract
The probability of neurotransmitter release at the nerve terminal is an important determinant of synaptic efficacy. At some central synapses, the postsynaptic, or target, neuron determines neurotransmitter release probability (Pr) at the presynaptic terminal. The mechanisms responsible for this target-cell dependent control of Pr have not been elucidated. Using whole-cell patch-clamp recordings from magnocellular neurosecretory cells in the paraventricular and supraoptic nuclei of the hypothalamus, we demonstrate that inhibitory, GABA synapses specifically onto oxytocin (OT)-producing neurosecretory cells exhibit a low Pr that is relatively uniform at multiple synapses onto the same cell. This low Pr results from a two-step process that requires the tonic release of OT from the postsynaptic cell. The ambient extracellular levels of neuropeptide are sufficient to activate postsynaptic OT receptors and trigger the Ca 2+-dependent production of endocannabinoids, which act in a retrograde manner at presynaptic cannabinoid CB 1 receptors to decrease GABA release. The functional consequence of this tonic inhibition of GABA release is that all inhibitory inputs facilitate uniformly when activated at high rates of activity. This causes inhibition in the postsynaptic cell that is sufficiently powerful to disrupt firing. Blockade of CB 1 receptors increases Pr at these synapses, resulting in a rapid depression of IPSCs at high rates of activity, thereby eliminating the ability of afferent inputs to inhibit postsynaptic firing. By playing a deterministic role in GABA release at the afferent nerve terminal, the postsynaptic OT neuron effectively filters synaptic signals and thereby modulates its own activity patterns.
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“oxytocin signalling controls the probability of presynaptic GABA release through the postsynaptic release of endocannabinoids and the activation of presynaptic CB1 receptors50.”
From Neural circuitry for maternal oxytocin release induced by infant cries (2023) · cites this paper as [50]
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Cites
Short-Term Synaptic Plasticity
Zucker, R. S., & Regehr, W. G. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.092501.114547 · Cited by 5,068
Synaptic depression and cortical gain control
Abbott, L. F., Varela, J. A., Sen, K., & Nelson, S. B. (1997) · Science · doi:10.1126/science.275.5297.221 · Cited by 1,690
Abbott, L. F., & Regehr, W. G. (2004) · Nature · doi:10.1038/nature03010 · Cited by 1,684
Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses
Wilson, R. I., & Nicoll, R. A. (2001) · Nature · doi:10.1038/35069076 · Cited by 1,607
Tsodyks, M. V., & Markram, H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.2.719 · Cited by 1,607
Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex
Gupta, A., Wang, Y., & Markram, H. (2000) · Science · doi:10.1126/science.287.5451.273 · Cited by 1,036
Ohno‐Shosaku, T., Maejima, T., & Kano, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00247-1 · Cited by 874
Redistribution of synaptic efficacy between neocortical pyramidal neurons
Markram, H., & Tsodyks, M. V. (1996) · Nature · doi:10.1038/382807a0 · Cited by 857
Target-cell-specific facilitation and depression in neocortical circuits
Reyes, A., Lujan, R., Rozov, A., Burnashev, N., Somogyi, P., & Sakmann, B. (1998) · Nature Neuroscience · doi:10.1038/1092 · Cited by 716 · cited 2×
“Although targetcell-dependent modulation of GABA release probability has been reported previously (Reyes et al., 1998; Gupta et al., 2000; Rozov et al., 2001; Koester and Johnston, 2005), there have been few descriptions of the mechanisms used by individual postsynaptic neurons to regulate Pr.”
BackgroundHeterosynaptic LTD of Hippocampal GABAergic Synapses
Chevaleyre, V., & Castillo, P. E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00235-6 · Cited by 647
Varela, J. A., Sen, K., Gibson, J. R., Fost, J. W., Abbott, L. F., & Nelson, S. B. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-20-07926.1997 · Cited by 605
GABA: A dominant neurotransmitter in the hypothalamus
Decavel, C., & van den Pol, A. N. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903020423 · Cited by 575
Maejima, T., Hashimoto, K., Yoshida, T., Aiba, A., & Kano, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00375-0 · Cited by 575
The impact of receptor desensitization on fast synaptic transmission
Jones, M. V., & Westbrook, G. L. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80037-3 · Cited by 472
Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis
Pow, D. V., & Morris, J. F. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90091-2 · Cited by 446
Metabotropic Glutamate Receptors Drive the Endocannabinoid System in Hippocampus
Varma, N., Carlson, G. C., Ledent, C. A., & Alger, B. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-24-j0003.2001 · Cited by 414
Rozov, A., Burnashev, N., Sakmann, B., & Neher, E. (2001) · Journal of Physiology · doi:10.1111/j.1469-7793.2001.0807h.x · Cited by 392
Cerebellar Depolarization-Induced Suppression of Inhibition Is Mediated by Endogenous Cannabinoids
Kreitzer, A. C., & Regehr, W. G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-j0005.2001 · Cited by 353
Renaud, L. P., & Bourquet, C. W. (1991) · Progress in Neurobiology · doi:10.1016/0301-0082(91)90020-2 · Cited by 348
Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites
Ludwig, M., Sabatier, N., Bull, P. M., Landgraf, R., Dayanithi, G., & Leng, G. (2002) · Nature · doi:10.1038/nature00822 · Cited by 344
Roland, B. L., & Sawchenko, P. E. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903320109 · Cited by 334
Hashimotodani, Y., Ohno‐Shosaku, T., Tsubokawa, H., Ogata, H., Emoto, K., Maejima, T., Araishi, K., Shin, H., & Kano, M. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.004 · Cited by 317
Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids
Bacci, A., Huguenard, J., & Prince, D. (2004) · Nature · doi:10.1038/nature02913 · Cited by 295
Electrophysiological differentiation of oxytocin-and vasopressin-secreting neurones
Poulain, D. A., Wakerley, J. B., & Dyball, R. E. J. (1977) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1977.0046 · Cited by 243
Maejima, T., Oka, S., Hashimotodani, Y., Ohno‐Shosaku, T., Aiba, A., Wu, D., Waku, K., Sugiura, T., & Kano, M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0945-05.2005 · Cited by 237
Orser, B. A., Wang, L., Pennefather, P., & MacDonald, J. F. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07747.1994 · Cited by 237
Brown, S. P., Brenowitz, S. D., & Regehr, W. G. (2003) · Nature Neuroscience · doi:10.1038/nn1126 · Cited by 236
Neumann, I., Ludwig, M., Engelmann, M., Pittman, Q. J., & Landgraf, R. (2008) · Neuroendocrinology · doi:10.1159/000126604 · Cited by 236
The magnocellular and parvocellular paraventricular nucleus of rat: intrinsic organization
Van Den Pol, A. N. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902060402 · Cited by 228
Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses
Koester, H. J., & Johnston, D. (2005) · Science · doi:10.1126/science.1100815 · Cited by 222
Talking back: dendritic neurotransmitter release
Ludwig, M., & Pittman, Q. J. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00072-9 · Cited by 210
Lambert, R. C., Dayanithi, G., Moos, F., & Richard, P. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020249 · Cited by 202
Enhancement of Synaptic Efficacy by Presynaptic GABAB Receptors
Brenowitz, S. D., David, J., & Trussell, L. O. (1998) · Neuron · doi:10.1016/s0896-6273(00)80441-9 · Cited by 196
Kombian, S. B., Mouginot, D., & Pittman, Q. J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80971-x · Cited by 186
Theodosis, D. T., Paut-Pagano, L., & Tappaz, M. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90016-3 · Cited by 179
Slow Desensitization Regulates the Availability of Synaptic GABAAReceptors
Overstreet, L. S., Jones, M. V., & Westbrook, G. L. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-07914.2000 · Cited by 171
Belin, V., & Moos, F. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016192 · Cited by 163
Wong, A. Y. C., Graham, B. P., Billups, B., & Forsythe, I. D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-04868.2003 · Cited by 162
A Novel Presynaptic Inhibitory Mechanism Underlies Paired Pulse Depression at a Fast Central Synapse
Bellingham, M. C., & Walmsley, B. D. (1999) · Neuron · doi:10.1016/s0896-6273(00)80762-x · Cited by 157
Moos, F., & Richard, P. (1989) · The Journal of Physiology · doi:10.1113/jphysiol.1989.sp017442 · Cited by 156
Adaptation of Ca2+-Triggered Exocytosis in Presynaptic Terminals
Hsu, S., Augustine, G. J., & Jackson, M. B. (1996) · Neuron · doi:10.1016/s0896-6273(00)80182-8 · Cited by 153
Minimizing Synaptic Depression by Control of Release Probability
Brenowitz, S. D., & Trussell, L. O. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-01857.2001 · Cited by 144
Molecular heterogeneity of central synapses: afferent and target regulation
Craig, A. M., & Boudin, H. (2001) · Nature Neuroscience · doi:10.1038/88388 · Cited by 142
Hirasawa, M., Schwab, Y., Natah, S. S., Hillard, C. J., Mackie, K., Sharkey, K. A., & Pittman, Q. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.066159 · Cited by 141
Hentges, S. T., Low, M. J., & Williams, J. T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2769-05.2005 · Cited by 136
Lambert, R. C., Moos, F., & Richard, P. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90046-i · Cited by 132
Stern, J. E., & Armstrong, W. E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-03-00841.1998 · Cited by 130
Gies, U., & Theodosis, D. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02861.1994 · Cited by 125
Brussaard, A. B., Kits, K. S., & Vlieger, T. A. D. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021783 · Cited by 122
Jourdain, P., Israël, J.-M., Dupouy, B., Oliet, S. H. R., Michèle Allard, A., Vitiello, S., Theodosis, D. T., & Poulain, D. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-06641.1998 · Cited by 118
Self-citationCalcium Dependence of Retrograde Inhibition by Endocannabinoids at Synapses onto Purkinje Cells
Brenowitz, S. D., & Regehr, W. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-15-06373.2003 · Cited by 116
Somatodendritic Secretion in Oxytocin Neurons Is Upregulated during the Female Reproductive Cycle
de Kock, C. P. J., Wierda, K. D. B., Bosman, L. W. J., Min, R., Koksma, J.-J., Mansvelder, H. D., Verhage, M., & Brussaard, A. B. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02726.2003 · Cited by 103
Actions of gamma‐aminobutyric acid on rat supraoptic nucleus neurosecretory neurones in vitro.
Randle, J. C. R., & Renaud, L. P. (1987) · The Journal of Physiology · doi:10.1113/jphysiol.1987.sp016592 · Cited by 98
GABA‐induced facilitation of the periodic bursting activity of oxytocin neurones in suckled rats.
Moos, F. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020949 · Cited by 79
Kombian, S. B., Hirasawa, M., Mouginot, D., Chen, X., & Pittman, Q. J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2542 · Cited by 71
Stern, J. E., & Armstrong, W. E. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022036 · Cited by 71
Chevaleyre, V., Moos, F., & Desarménien, M. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00265.2002 · Cited by 56
Chapter 18 Modulation of synaptic transmission by oxytocin and vasopressin in the supraoptic nucleus
Kombian, S. B., Hirasawa, M., Mouginot, D., & Pittman, Q. J. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)39020-4 · Cited by 52
Ohno‐Shosaku, T., Hashimotodani, Y., Maejima, T., & Kano, M. (2005) · Cell Calcium · doi:10.1016/j.ceca.2005.06.014 · Cited by 50
NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats
De Kock, C. P. J., Burnashev, N., Lodder, J. C., Mansvelder, H. D., & Brussaard, A. B. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.069005 · Cited by 50
Kombian, Mouginot, Hirasawa, & Pittman, Q. J. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00462.x · Cited by 49
Dopamine Modulates Use-Dependent Plasticity of Inhibitory Synapses
Baimoukhametova, D. V., Hewitt, S. A., Sank, C. A., & Bains, J. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4979-03.2004 · Cited by 45
Self-citationTarget-Specific Regulation of Synaptic Amplitudes in the Neocortex
Watanabe, J., Rozov, A. V., & Wollmuth, L. P. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3951-04.2005 · Cited by 41
Possible Control by Oxytocin of Periodical and Synchronous Neurosecretory Bursts of Oxytocin Cells
Freund‐Mercier, M. J., Moos, F., Guerné, Y., & Richard, P. (1983) · Progress in brain research · doi:10.1016/s0079-6123(08)64387-3 · Cited by 6
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Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,595
Endocannabinoid Signaling and Synaptic Function
Castillo, P. E., Younts, T. J., Chávez, A. E., & Hashimotodani, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.020 · Cited by 1,191
“Tonic signaling can be observed as an increase in basal synaptic transmission after pharmacological blockade of CB 1 Rs (Auclair et al., 2000; Hentges et al., 2005; Losonczy et al., 2004; Neu et al., 2007; Oliet et al., 2007; Slanina and Schweitzer, 2005; Zhu and Lovinger, 2010).”
BackgroundMultiple Functions of Endocannabinoid Signaling in the Brain
Katona, I., & Freund, T. F. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150420 · Cited by 630
“…receptors OX1 and OX2 (Haj-Dahmane and Shen, 2005), endothelin-1 and its ETA receptor (Zampronio et al., 2010), oxytocin and its OT receptor (Oliet et al., 2007) or ghrelin and its receptor (Kola et al., 2008), and then regulate feed-back hormonal responses via the modification of synaptic…”
BackgroundCB1 Receptor Signaling in the Brain: Extracting Specificity from Ubiquity
Busquets-García, A., Bains, J. S., & Marsicano, G. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.206 · Cited by 365
“This has been demonstrated in hypothalamus where blockade of CB1 receptors increases Pr at GABA synapses, but weakens inhibition to the postsynaptic neuron when GABA inputs are recruited at a high frequency (Oliet et al, 2007).”
BackgroundSelf-citationFerguson, A. V., Latchford, K. J., & Samson, W. K. (2008) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.12.6.717 · Cited by 316
“Although they will not be discussed in-depth here it should also be emphasized that recent studies have also highlighted important roles for both dendritic release of peptides produced in the PVN neurons [11,12] , and glial cell release of amino acid signaling molecules [13] in shaping the integrated outputs of the PV…”
Background
Metadata
- Authors
- Oliet, S. H. R., Baimoukhametova, D. V., Piet, R., & Bains, J. S.
- Affiliations
- Inserm (FR)
- University of Calgary (CA)
- Université Bordeaux Segalen (FR)
- Corresponding author
- Bains, Jaideep S.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-02-07
- Volume
- 27
- Issue
- 6
- Pages
- 1325-1333
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673587
- OpenAlex
- W2091992063
- Cited by
- 107
- References
- 64
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 4 · 2021: 5 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 6 · 2016: 3 · 2015: 7 · 2014: 9 · 2013: 7 · 2012: 8
- FWCI
- 4.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fondation pour la Recherche Médicale
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Keywords
- retrograde regulation, oxytocin, endocannabinoids, CB1 receptor, postsynaptic inhibition, presynaptic inhibition, magnocellular neurosecretory cells, paraventricular nucleus, supraoptic nucleus, hypothalamus, inhibitory synapses
- MeSH terms
- Animals, Calcium, Egtazic Acid, Female, gamma-Aminobutyric Acid, Hypothalamus, Anterior, Male, Morpholines, Naphthalenes, Oxytocin, Paraventricular Hypothalamic Nucleus, Piperidines, Pyrazoles, Rats, Sprague-Dawley, Rats, Wistar, Presynaptic Terminals, Patch-Clamp Techniques, 6-Cyano-7-nitroquinoxaline-2,3-dione, Receptor, Cannabinoid, CB1, Extracellular Fluid, Benzoxazines, Rats, Cannabinoid Receptor Modulators, Endocannabinoids
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