Cited by 184Neuroscience and Neuropharmacology ResearchCircadian rhythm and melatoninHypothalamic control of reproductive hormones

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GABA and glutamate mediate rapid neurotransmission from suprachiasmatic nucleus to hypothalamic paraventricular nucleus in rat

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Hermes, M L, Coderre, E M, Buijs, R M, Renaud, L P·1996·The Journal of Physiology

DOI 10.1113/jphysiol.1996.sp021724PMC PMC1160861

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Abstract

1. Intracellular sharp electrode and whole-cell patch-clamp recording from characterized paraventricular nucleus (PVN) neurones in rat hypothalamic slices were used to study the synaptic mechanism and associated neurotransmitters that mediate their response to suprachiasmatic nucleus (SCN) stimulation. 2. Electrical stimulation restricted to SCN evoked short-latency inhibitory postsynaptic potentials (IPSPs) or combinations of IPSPs and excitatory postsynaptic potentials (EPSPs) in all (n = 59) PVN neurones tested. Type I neurones (n = 18) were magnocellular and a majority (13/18) demonstrated monosynaptic IPSPs that reversed polarity at the chloride equilibrium potential and were sensitive to bicuculline. 3. Type II (n = 10) and III parvocellular (n = 13), and unclassifiable neurones (n = 18) displayed combinations of IPSPs and EPSPs following similar stimuli applied to SCN. IPSP blockade with bicuculline uncovered SCN-evoked monosynaptic dual-component EPSPs that were sensitive to N-methyl-D-aspartate (NMDA) and non-NMDA receptor antagonists. In addition, chemical microstimulation within SCN was associated with transient increases in spontaneous EPSPs recorded from these PVN neurones. 4. These data imply that the amino acids GABA and glutamate are important mediators of fast monosynaptic transmission from SCN to defined neurones in PVN, and are candidates for conveying circadian rhythmicity to PVN regulation of neuroendocrine and autonomic processes.

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BackgroundInfluential
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Cui, L.-N., Coderre, E., & Renaud, L. P. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.4.r1283 · Cited by 99
“An alternative possibility arising from our current and earlier electrophysiological studies (16) is the existence of a glutamatergic projection from SCN, most easily demonstrable in slice preparations after pharmacological blockade of GABAA receptors.”
BackgroundInfluential
Paraventricular nucleus of the human hypothalamus in primary hypertension: Activation of corticotropin-releasing hormone neurons
Goncharuk, V. D., Van Heerikhuize, J., Swaab, D. F., & Buijs, R. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10124 · Cited by 97
“…in the PVN are affected by strongly inhibitory inputs from adjacent hypothalamic structures—with the SCN playing a pivotal role (Buijs et al., 1993; Hermes et al., 1996; Kalsbeek et al., 1996)—such a reduction of SCN activity could underlie or reinforce the activation of the CRH system in the PVN…”
Background
Melatonin and anesthesia: a clinical perspective
Naguib, M., Gottumukkala, V. N. R., & Goldstein, P. A. (2006) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2006.00384.x · Cited by 97
Physical and Inflammatory Stressors Elevate Circadian Clock Gene mPer1 mRNA Levels in the Paraventricular Nucleus of the Mouse.
Takahashi, S., Yokota, S.-I., Hara, R., Kobayashi, T., Akiyama, M., Moriya, T., & Shibata, S. (2001) · Endocrinology · doi:10.1210/endo.142.11.8487 · Cited by 18
Daily regulation of hormone profiles.
Kalsbeek, A., & Fliers, E. (2013) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-25950-0_8 · Cited by 91
Glutamatergic clock output stimulates melatonin synthesis at night
Perreau‐Lenz, S., Kalsbeek, A., Pévet, P., & Buijs, R. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2003.03132.x · Cited by 99
Function and Pharmacology of Spinally-Projecting Sympathetic Pre-Autonomic Neurones in the Paraventricular Nucleus of the Hypothalamus
Barrett‐Jolley, R., Nunn, N., Womack, M. D., & Dart, C. (2011) · Current Neuropharmacology · doi:10.2174/157015911795596531 · Cited by 90
“There are strong excitatory and inhibitory pathways from the SCN to the PVN of rats [99, 192], and, specifically, to spinally-projecting SPANs [31].”
Background
Vasopressin Increases GABAergic Inhibition of Rat Hypothalamic Paraventricular Nucleus Neurons In Vitro
Hermes, M. L. H. J., Ruijter, J. M., Klop, A., Buijs, R. M., & Renaud, L. P. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.2.705 · Cited by 87
Per and neuropeptide expression in the rat suprachiasmatic nuclei: compartmentalization and differential cellular induction by light
Dardente, H., Poirel, V., Klosen, P., Pévet, P., & Masson‐Pévet, M. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03563-1 · Cited by 91
Orexin depolarizes rat hypothalamic paraventricular nucleus neurons
Shirasaka, T., Miyahara, S., Kunitake, T., Jin, Q.-H., Kato, K., Takasaki, M., & Kannan, H. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.4.r1114 · Cited by 85
“Excitatory inputs to parvocellular as well as magnocellular neurons of the PVN are mediated mainly by an intrahypothalamic glutamatergic pathway (5, 11).”
Background
VR1 Receptor Activation Induces Glutamate Release and Postsynaptic Firing in the Paraventricular Nucleus
Li, D., Chen, S.-R., & Pan, H. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00171.2004 · Cited by 85
Attenuation of the hypothalamic–pituitary–adrenal axis responsivity to the Trier Social Stress Test by the benzodiazepine alprazolam
Fries, E., Hellhammer, D. H., & Hellhammer, D. H. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.09.009 · Cited by 83
“, 2004) and its close proximity (Boudaba et al., 1996; Hermes et al., 1996; Herman et al., 2002, 2003) a dense network of GABAergic neurons as well as a high density of subunits of the GABAA-benzodiazepine receptor complex exists (Cullinan, 2000), mediating the inhibitory effects of GABA on the secretion of corticotro…”
Background
Cardiovascular effects of leptin and orexins
Shirasaka, T., Takasaki, M., & Kannan, H. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00359.2002 · Cited by 84
“For example, the PVN of the hypothalamus, which is enriched with a vast number of neuroendocrine modulators (19, 36), has been implicated in the stress response, control of pituitary function, body fluid homeostasis, analgesia, and cardiovascular and gastrointestinal functions (4, 90, 91).”
Background
Daily Rhythms of Fos Expression in Hypothalamic Targets of the Suprachiasmatic Nucleus in Diurnal and Nocturnal Rodents
Núñez, A. A., Bult, A., McElhinny, T. L., & Smale, L. (1999) · Journal of Biological Rhythms · doi:10.1177/074873099129000713 · Cited by 72
“To determine whether targets of the SCN (Stephan et al., 1981; Watts, 1991; Hermes et al., 1996; Cui et al., 1997) function differently in diurnal and nocturnal mammals, we evaluated the rhythmic expression of Fos in hypothalamic targets of SCN efferent projections in the diurnal rodent Arvicanthis niloticus (unstripe…”
Background
Electrophysiological analysis of suprachiasmatic nucleus projections to the ventrolateral preoptic area in the rat
Sun, X., Whitefield, S., Rusak, B., & Semba, K. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.0001755.x · Cited by 72
Adiponectin selectively inhibits oxytocin neurons of the paraventricular nucleus of the hypothalamus
Hoyda, T. D., Fry, M., Ahima, R. S., & Ferguson, A. V. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.144519 · Cited by 68
“) treatment (Hermes et al. 1999; Follwell & Ferguson, 2002; Latchford & Ferguson, 2003; Ferri et al. 2005).”
Result
The Rhythmic GABAergic System
Cardinali, D. P., & Golombek, D. A. (1998) · Neurochemical Research · doi:10.1023/a:1022426519297 · Cited by 65
Pituitary Adenylate Cyclase-Activating Polypeptide and Melatonin in the Suprachiasmatic Nucleus: Effects on the Calcium Signal Transduction Cascade
Kopp, M. D. A., Schomerus, C., Dehghani, F., Korf, H., & Meissl, H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00206.1999 · Cited by 65
Minireview: Circadian Control of Metabolism by the Suprachiasmatic Nuclei
Kalsbeek, A., Kreier, F., Fliers, E., Sauerwein, H. P., Romijn, J. A., & Buijs, R. M. (2007) · Endocrinology · doi:10.1210/en.2007-0776 · Cited by 58
“cleus, and medial preoptic area, and preautonomic neurons in the PVN were described as well (11, 12).”
TNF-.ALPHA. in Hypothalamic Paraventricular Nucleus Contributes to Sympathoexcitation in Heart Failure by Modulating AT1 Receptor and Neurotransmitters
Kang, Y., Wang, Y., Yang, L., Elks, C. M., Cardinale, J. P., Yu, X., Zhao, X.-F., Zhang, J., Zhang, L.-H., Yang, Z., et al. (2010) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.222.251 · Cited by 58
“Functional glutamate receptors expressed in the PVN (Hermes et al. 1996; Tasker et al. 1998) are involved in cardiovascular reflex control (Antonaccio et al. 1978; Brennan et al. 1983).”
Background
Central neural control of sympathetic nerve activity in heart failure following exercise training
Patel, K. P., & Zheng, H. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00676.2011 · Cited by 59
“A large body of evidence suggests that GABA plays an important role in central cardiovascular control (4, 24).”
Background
Glutamatergic innervation of corticotropin-releasing hormone- and thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat
Wittmann, G., Lechan, R. M., Liposits, Z., & Fekete, C. (2005) · Brain Research · doi:10.1016/j.brainres.2005.01.090 · Cited by 56
“First, both VGLUT1 and VGLUT2 specifically transport glutamate into synaptic vesicles [3,6,22,25,26,53,54,57].”
Dissection of glucocorticoid receptor-mediated inhibition of the hypothalamic–pituitary–adrenal axis by gene targeting in mice
Laryea, G. N., Muglia, L. M., Arnett, M. G., & Muglia, L. J. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.09.002 · Cited by 57
“Physiological data has also demonstrated that the SCN evokes both inhibitory and excitatory postsynaptic potentials in PVN neurons and in this way directly targets PVN CRH neurons (Hermes et al., 1996).”
Mechanisms of circadian clock interactions with aryl hydrocarbon receptor signalling
Tischkau, S. A. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14361 · Cited by 56
“Glutamate and gamma amino- butyric acid (GABA; Buijs, Wortel, & Hou, 1995; Hermes et al., 1996) are primary neurotransmitters associated with SCN output, although a number of other molecules, including arginine vasopressin (Kalsbeek et al., 2006), cardiotrophin- like cytokine (Kraves & Weitz,…”
Background
Rapid neuromodulation by cortisol in the rat paraventricular nucleus: an in vitro study
Zaki, A., & Barrett‐Jolley, R. (2002) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704832 · Cited by 53
“3; neuromodulation; paraventricular nucleus; patch clamp; potassium channel; sympathetic Abbreviations: ACSF, arti®cial cerebrospinal ¯uid; ECl7, equilibrium potential for chloride ions; GABA, g-aminobutyric acid; GC, glucocorticoid; GR, glucocorticoid intracellular receptor; hKv, human voltage-gated potassium channel…”
BackgroundInfluential
Seasonal changes in day length induce multisynaptic neurotransmitter switching to regulate hypothalamic network activity and behavior
Porcu, A., Nilsson, A., Booreddy, S., Barnes, S. A., Welsh, D. K., & Dulcis, D. (2022) · Science Advances · doi:10.1126/sciadv.abn9867 · Cited by 49
“SCN neurons send major output signals to the PVN region via diffusible factors (including neuropeptides) ( 58 ) and neuronal projections ( 59 ).”
Background
Mechanism of bilateral communication in the suprachiasmatic nucleus
Michel, S. H., Marek, R., vanderLeest, H. T., Vansteensel, M. J., Schwartz, W. J., Colwell, C. S., & Meijer, J. H. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12109 · Cited by 49
“Other physiological studies have accumulated evidence for a role of glutamate in the output of SCN neurons (Hermes et al., 1996; Cui et al., 2001; Perreau-Lenz et al., 2004).”
Background
Ultradian calcium rhythms in the paraventricular nucleus and subparaventricular zone in the hypothalamus
Wu, Y.-E., Enoki, R., Oda, Y., Huang, Z., Honma, K., & Honma, S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1804300115 · Cited by 49
“SCN neurons send the major output signals to the SPZ and further to the paraventricular nucleus (PVN) region in the hypothalamus (14, 15) via diffusible factors, such as arginine vasopressin (AVP) (16) and neuronal projections (17, 18).”
Background
Serotonin increases the excitability of the hypothalamic paraventricular nucleus magnocellular neurons
Ho, S. S. N., Chow, B., & Yung, W. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05547.x · Cited by 47
“…the origin of GABAergic axonal terminals impinging onto the PVN magnocellular neurons, possible sources are from the suprachiasmatic nucleus (Hermes et al., 1996; Cui et al., 2000), the arcuate nucleus (Bouret et al., 2004) and from other hypothalamic nuclei in a local network (Roland &…”
Background
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
“In addition to a direct inhibitory projection from the SCN (Buijs et al., 1994; Hermes et al., 1996; Cui et al., 2000), MNCs in PVN also receive inhibitory input from GABAergic interneurons positioned just outside the nucleus, ventral to the fornix (Boudaba et al.”
BackgroundMethod
Regulation of Synaptic Inputs to Paraventricular-Spinal Output Neurons by α2 Adrenergic Receptors
Li, D.-P., Atnip, L. M., Chen, S.-R., & Pan, H. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00564.2004 · Cited by 45
“Regulation of Synaptic Inputs to Paraventricular-Spinal Output Neurons by 2 Adrenergic Receptors”
Background
Cortical connections of striate and extrastriate visual areas in tree shrews
Lyon, D. C., Jain, N., & Kaas, J. H. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19981109)401:1 · Cited by 78
Interaction Between AT1 Receptor and NF-κB in Hypothalamic Paraventricular Nucleus Contributes to Oxidative Stress and Sympathoexcitation by Modulating Neurotransmitters in Heart Failure
Yu, X., Suo, Y., Qi, J., Yang, Q., Li, H., Zhang, D., Yi, Q.-Y., Zhang, J., Zhu, G., Zhu, Z., et al. (2013) · Cardiovascular Toxicology · doi:10.1007/s12012-013-9219-x · Cited by 41
Deletion of Metabotropic Glutamate Receptors 2 and 3 (mGlu2 & mGlu3) in Mice Disrupts Sleep and Wheel-Running Activity, and Increases the Sensitivity of the Circadian System to Light
Pritchett, D., Jagannath, A., Brown, L. A., Tam, S. K. E., Hasan, S., Gatti, S., Harrison, P. J., Bannerman, D. M., Foster, F., & Peirson, S. N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125523 · Cited by 42
Swim stress triggers the release of vasopressin within the suprachiasmatic nucleus of male rats
Engelmann, M., Ebner, K., Landgraf, R., & Wotjak, C. T. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00243-1 · Cited by 39
Distribution of choline acetyltransferase (ChAT) immunoreactivity in the brain of the adult trout and tract-tracing observations on the connections of the nuclei of the isthmus
Pérez, S. E., Y��ez, J., Marín, Ó., Anad�n, R., Gonz�lez, A., & Rodríguez‐Moldes, I. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001218)428:3 · Cited by 96
Pre- and postsynaptic gabab receptors modulate rapid neurotransmission from suprachiasmatic nucleus to parvocellular hypothalamic paraventricular nucleus neurons
Wang, D., Cui, L.-N., & Renaud, L. P. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00906-5 · Cited by 38
Electrophysiology and pharmacology of projections from the suprachiasmatic nucleus to the ventromedial preoptic area in rat
Sun, X., Rusak, B., & Semba, K. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00170-6 · Cited by 38
Relationship between sedation and pupillary function: comparison of diazepam and diphenhydramine
Hou, R. H., Scaife, J. C., Freeman, C., Langley, R. W., Szabadi, E., & Bradshaw, C. M. (2006) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2006.02632.x · Cited by 38
Suprachiasmatic nucleus communicates with anterior thalamic paraventricular nucleus neurons via rapid glutamatergic and gabaergic neurotransmission: State-dependent response patterns observed in vitro
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Vasopressin induces depolarization and state-dependent firing patterns in rat thalamic paraventricular nucleus neurons in vitro
Zhang, L., Doroshenko, P. A., Cao, X.-H., Irfan, N. U. A., Coderre, E., Kolaj, M., & Renaud, L. P. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00770.2005 · Cited by 37
Competing clocks: Metabolic status moderates signals from the master circadian pacemaker
Blum, I. D., Lamont, E. W., & Abizaid, A. B. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.06.003 · Cited by 38
The hypothalamic clock and its control of glucose homeostasis
Kalsbeek, A., Ruiter, M., la Fleur, S. E., Cailotto, C., Kreier, F., & Buijs, R. M. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)53017-1 · Cited by 33

Authors: Hermes, M. L., Coderre, E. M., Buijs, R. M., & Renaud, L. P.
Affiliations: University of Ottawa (CA)
ORCID: Hermes, M L
Buijs, R M
Renaud, L P
Venue: The Journal of Physiology
Publisher: Wiley
Published: 1996-11
Volume: 496
Issue: 3
Pages: 749-757
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.1996.sp021724
PMC: PMC1160861
OpenAlex: W2023286290
Cited by: 184
References: 33
Citations by year: 2026: 1 · 2024: 1 · 2023: 1 · 2022: 3 · 2021: 3 · 2020: 2 · 2019: 6 · 2018: 5 · 2017: 2 · 2016: 4 · 2015: 4 · 2014: 7 · 2013: 7 · 2012: 6
FWCI: 2.16
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: Heart and Stroke Foundation of Canada
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords: suprachiasmatic nucleus, paraventricular nucleus, GABA, glutamate, monosynaptic transmission, inhibitory postsynaptic potentials, excitatory postsynaptic potentials, circadian rhythm, hypothalamus, magnocellular neurons, parvocellular neurons, NMDA receptor, non-NMDA receptors, bicuculline, chloride equilibrium potential, neuroendocrine regulation
MeSH terms: Animals, Bicuculline, Electric Stimulation, Evoked Potentials, gamma-Aminobutyric Acid, Male, Synaptic Transmission, Neurons, Paraventricular Hypothalamic Nucleus, Suprachiasmatic Nucleus, Time Factors, Patch-Clamp Techniques, Glutamic Acid, Rats, In Vitro Techniques

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GABA and glutamate mediate rapid neurotransmission from suprachiasmatic nucleus to hypothalamic paraventricular nucleus in rat

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