Literature DB >> 21727221

Short-term plasticity impacts information transfer at glutamate synapses onto parvocellular neuroendocrine cells in the paraventricular nucleus of the hypothalamus.

Vincent Marty1, J Brent Kuzmiski, Dinara V Baimoukhametova, Jaideep S Bains.   

Abstract

Glutamatergic synaptic inputs onto parvocellular neurosecretory cells (PNCs) in the paraventricular nucleus of the hypothalamus (PVN) regulate the hypothalamic-pituitary-adrenal (HPA) axis responses to stress and undergo stress-dependent changes in their capacity to transmit information. In spite of their pivotal role in regulating PNCs, relatively little is known about the fundamental rules that govern transmission at these synapses. Furthermore, since salient information in the nervous system is often transmitted in bursts, it is also important to understand the short-term dynamics of glutamate transmission under basal conditions. To characterize these properties, we obtained whole-cell patch clamp recordings from PNCs in brain slices from postnatal day 21-35 male Sprague-Dawley rats and examined EPSCs. EPSCs were elicited by electrically stimulating glutamatergic afferents along the periventricular aspect. In response to a paired-pulse stimulation protocol, EPSCs generally displayed a robust short-term depression that recovered within 5 s. Similarly, trains of synaptic stimuli (5-50 Hz) resulted in a frequency-dependent depression until a near steady state was achieved. Application of inhibitors of AMPA receptor (AMPAR) desensitization or the low-affinity, competitive AMPAR antagonist failed to affect the depression due to paired-pulse and trains of synaptic stimulation indicating that this use-dependent short-term synaptic depression has a presynaptic locus of expression. We used cumulative amplitude profiles during trains of stimulation and variance-mean analysis to estimate synaptic parameters. Finally, we report that these properties contribute to hamper the efficiency with which high frequency synaptic inputs generate spikes in PNCs, indicating that these synapses operate as effective low-pass filters in basal conditions.

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Year:  2011        PMID: 21727221      PMCID: PMC3180582          DOI: 10.1113/jphysiol.2011.208082

Source DB:  PubMed          Journal:  J Physiol        ISSN: 0022-3751            Impact factor:   5.182


  53 in total

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Authors:  Volker Scheuss; Ralf Schneggenburger; Erwin Neher
Journal:  J Neurosci       Date:  2002-02-01       Impact factor: 6.167

2.  Neurosecretory and non-neurosecretory parvocellular neurones of the hypothalamic paraventricular nucleus express distinct electrophysiological properties.

Authors:  J A Luther; S S Daftary; C Boudaba; G C Gould; K Cs Halmos; J G Tasker
Journal:  J Neuroendocrinol       Date:  2002-12       Impact factor: 3.627

3.  Variance-mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation.

Authors:  John D Clements
Journal:  J Neurosci Methods       Date:  2003-12-15       Impact factor: 2.390

4.  Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses.

Authors:  Matthew A Xu-Friedman; Wade G Regehr
Journal:  J Neurosci       Date:  2003-03-15       Impact factor: 6.167

5.  Priming of excitatory synapses by alpha1 adrenoceptor-mediated inhibition of group III metabotropic glutamate receptors.

Authors:  Grant R J Gordon; Jaideep S Bains
Journal:  J Neurosci       Date:  2003-07-16       Impact factor: 6.167

6.  Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse.

Authors:  Kelly A Foster; Wade G Regehr
Journal:  Neuron       Date:  2004-07-08       Impact factor: 17.173

7.  Glutamate receptor desensitization and its role in synaptic transmission.

Authors:  L O Trussell; G D Fischbach
Journal:  Neuron       Date:  1989-08       Impact factor: 17.173

8.  Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains.

Authors:  Adrian Y C Wong; Bruce P Graham; Brian Billups; Ian D Forsythe
Journal:  J Neurosci       Date:  2003-06-15       Impact factor: 6.167

9.  Neuropeptide W has cell phenotype-specific effects on the excitability of different subpopulations of paraventricular nucleus neurones.

Authors:  C J Price; W K Samson; A V Ferguson
Journal:  J Neuroendocrinol       Date:  2009-07-21       Impact factor: 3.627

10.  Glutamate, the dominant excitatory transmitter in neuroendocrine regulation.

Authors:  A N van den Pol; J P Wuarin; F E Dudek
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  8 in total

Review 1.  Stress-related synaptic plasticity in the hypothalamus.

Authors:  Jaideep S Bains; Jaclyn I Wamsteeker Cusulin; Wataru Inoue
Journal:  Nat Rev Neurosci       Date:  2015-07       Impact factor: 34.870

Review 2.  Identifying links in the chain: the dynamic coupling of catecholamines, peptide synthesis, and peptide release in hypothalamic neuroendocrine neurons.

Authors:  Alan G Watts; Arshad M Khan
Journal:  Adv Pharmacol       Date:  2013

3.  Chronic alcohol disrupts hypothalamic responses to stress by modifying CRF and NMDA receptor function.

Authors:  Vincent N Marty; Yatendra Mulpuri; Joseph J Munier; Igor Spigelman
Journal:  Neuropharmacology       Date:  2020-02-12       Impact factor: 5.250

4.  Glial glutamate transporter and glutamine synthetase regulate GABAergic synaptic strength in the spinal dorsal horn.

Authors:  Enshe Jiang; Xisheng Yan; Han-Rong Weng
Journal:  J Neurochem       Date:  2012-03-21       Impact factor: 5.372

5.  Spontaneous Synaptic Activation of Muscarinic Receptors by Striatal Cholinergic Neuron Firing.

Authors:  Aphroditi A Mamaligas; Christopher P Ford
Journal:  Neuron       Date:  2016-06-30       Impact factor: 17.173

Review 6.  AMPA Receptor Function in Hypothalamic Synapses.

Authors:  Maria Royo; Beatriz Aznar Escolano; M Pilar Madrigal; Sandra Jurado
Journal:  Front Synaptic Neurosci       Date:  2022-01-31

7.  Characterization of corticotropin-releasing hormone neurons in the paraventricular nucleus of the hypothalamus of Crh-IRES-Cre mutant mice.

Authors:  Jaclyn I Wamsteeker Cusulin; Tamás Füzesi; Alan G Watts; Jaideep S Bains
Journal:  PLoS One       Date:  2013-05-28       Impact factor: 3.240

8.  Nitric Oxide Synthase Inhibitor Attenuates the Effects of Repeated Restraint Stress on Synaptic Transmission in the Paraventricular Nucleus of the Rat Hypothalamus.

Authors:  Magdalena Kusek; Anna Tokarska; Marcin Siwiec; Anna Gadek-Michalska; Bernadeta Szewczyk; Grzegorz Hess; Krzysztof Tokarski
Journal:  Front Cell Neurosci       Date:  2017-05-03       Impact factor: 5.505

  8 in total

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