Literature DB >> 19778589

Bi-directional modulation of bed nucleus of stria terminalis neurons by 5-HT: molecular expression and functional properties of excitatory 5-HT receptor subtypes.

J-D Guo1, S E Hammack, R Hazra, L Levita, D G Rainnie.   

Abstract

Activation of neurons in the anterolateral bed nucleus of the stria terminalis (BNST(ALG)) plays an important role in mediating the behavioral response to stressful and anxiogenic stimuli. Application of 5-HT elicits complex postsynaptic responses in BNST(ALG) neurons, which includes (1) membrane hyperpolarization (5-HT(Hyp)), (2) hyperpolarization followed by depolarization (5-HT(Hyp-Dep)), (3) depolarization (5-HT(Dep)) or (4) no response (5-HT(NR)). We have shown that the inhibitory response is mediated by activation of postsynaptic 5-HT(1A) receptors. Here, we used a combination of in vitro whole-cell patch-clamp recording and single cell reverse transcriptase polymerase chain reaction (RT-PCR) to determine the pharmacological properties and molecular profile of 5-HT receptor subtypes mediating the excitatory response to 5-HT in BNST(ALG) neurons. We show that the depolarizing component of both the 5-HT(Hyp/Dep) and the 5-HT(Dep) response was mediated by activation of 5-HT(2A), 5-HT(2C) and/or 5-HT(7) receptors. Single cell RT-PCR data revealed that 5-HT(7) receptors (46%) and 5-HT(1A) receptors (41%) are the most prevalent receptor subtypes expressed in BNST(ALG) neurons. Moreover, 5-HT receptor subtypes are differentially expressed in type I-III BNST(ALG) neurons. Hence, 5-HT(2C) receptors are almost exclusively expressed by type III neurons, whereas 5-HT(7) receptors are expressed by type I and II neurons, but not type III neurons. Conversely, 5-HT(2A) receptors are found predominantly in type II neurons. Finally, bi-directional modulation of individual neurons occurs only in type I and II neurons. Significantly the distribution of 5-HT receptor subtypes in BNST(ALG) neurons predicted the observed expression pattern of 5-HT responses determined pharmacologically. Together, these results suggest that 5-HT can differentially modulate the excitability of type I-III neurons, and further suggest that bi-directional modulation of BNST(ALG) neurons occurs primarily through an interplay between 5-HT(1A) and 5-HT(7) receptors. Hence, modulation of 5-HT(7) receptor activity in the BNST(ALG) may offer a novel avenue for the design of anxiolytic medications.

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Year:  2009        PMID： 19778589      PMCID： PMC2783788          DOI： 10.1016/j.neuroscience.2009.09.028

Source DB:  PubMed          Journal:  Neuroscience        ISSN： 0306-4522            Impact factor:   3.590


  129 in total

1.  c-Fos proteins, induced by the serotonin receptor agonist DOI, are not expressed in 5-HT2A positive cortical neurons.

Authors:  M Maćkowiak; A Chocyk; K Fijał; A Czyrak; K Wedzony
Journal:  Brain Res Mol Brain Res       Date:  1999-08-25

2.  Neurons of the bed nucleus of the stria terminalis (BNST). Electrophysiological properties and their response to serotonin.

Authors:  D G Rainnie
Journal:  Ann N Y Acad Sci       Date:  1999-06-29       Impact factor: 5.691

3.  Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex.

Authors:  F M Zhou; J J Hablitz
Journal:  J Neurophysiol       Date:  1999-12       Impact factor: 2.714

4.  Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex.

Authors:  Maria Toledo-Rodriguez; Barak Blumenfeld; Caizhi Wu; Junyi Luo; Bernard Attali; Philip Goodman; Henry Markram
Journal:  Cereb Cortex       Date:  2004-06-10       Impact factor: 5.357

5.  5-HT1A autoreceptor desensitization by chronic ultramild stress in mice.

Authors:  L Lanfumey; M C Pardon; N Laaris; C Joubert; N Hanoun; M Hamon; C Cohen-Salmon
Journal:  Neuroreport       Date:  1999-11-08       Impact factor: 1.837

Review 6.  Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus.

Authors:  Christopher A Lowry; Matthew W Hale; Andrew K Evans; Jasper Heerkens; Daniel R Staub; Paul J Gasser; Anantha Shekhar
Journal:  Ann N Y Acad Sci       Date:  2008-12       Impact factor: 5.691

7.  5-Hydroxytryptamine action in the rat olfactory bulb: in vitro electrophysiological patch-clamp recordings of juxtaglomerular and mitral cells.

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8.  5-HT3A receptor subunits in the rat medial nucleus of the solitary tract: subcellular distribution and relation to the serotonin transporter.

Authors:  Jie Huang; Avron D Spier; Virginia M Pickel
Journal:  Brain Res       Date:  2004-12-03       Impact factor: 3.252

9.  5-HT2A receptors stimulate ACTH, corticosterone, oxytocin, renin, and prolactin release and activate hypothalamic CRF and oxytocin-expressing cells.

Authors:  L D Van de Kar; A Javed; Y Zhang; F Serres; D K Raap; T S Gray
Journal:  J Neurosci       Date:  2001-05-15       Impact factor: 6.167

Review 10.  The response of neurons in the bed nucleus of the stria terminalis to serotonin: implications for anxiety.

Authors:  Sayamwong E Hammack; Ji-Dong Guo; Rimi Hazra; Joanna Dabrowska; Karyn M Myers; Donald G Rainnie
Journal:  Prog Neuropsychopharmacol Biol Psychiatry       Date:  2009-05-23       Impact factor: 5.067
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  30 in total

Review 1.  Serotonin 5-HT7 receptor agents: Structure-activity relationships and potential therapeutic applications in central nervous system disorders.

Authors:  Marcello Leopoldo; Enza Lacivita; Francesco Berardi; Roberto Perrone; Peter B Hedlund
Journal:  Pharmacol Ther       Date:  2010-10-20       Impact factor: 12.310

2.  Presynaptic muscarinic M(2) receptors modulate glutamatergic transmission in the bed nucleus of the stria terminalis.

Authors:  Ji-Dong Guo; Rimi Hazra; Joanna Dabrowska; E Chris Muly; Jürgen Wess; Donald G Rainnie
Journal:  Neuropharmacology       Date:  2011-12-08       Impact factor: 5.250

3.  Contrasting distribution of physiological cell types in different regions of the bed nucleus of the stria terminalis.

Authors:  Olga E Rodríguez-Sierra; Hjalmar K Turesson; Denis Pare
Journal:  J Neurophysiol       Date:  2013-08-07       Impact factor: 2.714

4.  Double-dissociation of the catecholaminergic modulation of synaptic transmission in the oval bed nucleus of the stria terminalis.

Authors:  Michal Krawczyk; François Georges; Robyn Sharma; Xenos Mason; Amandine Berthet; Erwan Bézard; Eric C Dumont
Journal:  J Neurophysiol       Date:  2010-11-03       Impact factor: 2.714

Review 5.  Stress Modulation of Opposing Circuits in the Bed Nucleus of the Stria Terminalis.

Authors:  Sarah E Daniel; Donald G Rainnie
Journal:  Neuropsychopharmacology       Date:  2015-06-22       Impact factor: 7.853

Review 6.  The role of biogenic amine signaling in the bed nucleus of the stria terminals in alcohol abuse.

Authors:  Thomas Louis Kash
Journal:  Alcohol       Date:  2012-03-25       Impact factor: 2.405

7.  Intrinsic connections in the anterior part of the bed nucleus of the stria terminalis.

Authors:  Hjalmar K Turesson; Olga E Rodríguez-Sierra; Denis Pare
Journal:  J Neurophysiol       Date:  2013-02-27       Impact factor: 2.714

Review 8.  The Deakin/Graeff hypothesis: focus on serotonergic inhibition of panic.

Authors:  Evan D Paul; Philip L Johnson; Anantha Shekhar; Christopher A Lowry
Journal:  Neurosci Biobehav Rev       Date:  2014-03-21       Impact factor: 8.989

9.  Attenuation of the anxiogenic effects of cocaine by 5-HT1B autoreceptor stimulation in the bed nucleus of the stria terminalis of rats.

Authors:  Adam K Klein; Michael A Brito; Sayeh Akhavan; Dylan R Flanagan; Nikki Le; Tatum Ohana; Anand S Patil; Erin M Purvis; Carl Provenzano; Alex Wei; Lucy Zhou; Aaron Ettenberg
Journal:  Psychopharmacology (Berl)       Date:  2016-11-25       Impact factor: 4.530

10.  Presynaptic 5-HT(1B) receptor-mediated serotonergic inhibition of glutamate transmission in the bed nucleus of the stria terminalis.

Authors:  J-D Guo; D G Rainnie
Journal:  Neuroscience       Date:  2009-12-03       Impact factor: 3.590
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