Multiple anxiogenic drugs recruit a parvalbumin-containing subpopulation of GABAergic interneurons in the basolateral amygdala

Matthew W. Hale, Philip Johnson, Alex M. Westerman, Jolane K. Abrams, Anantha Shekhar, Christopher A. Lowry

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

The basolateral amygdala is a nodal structure within a distributed and interconnected network that regulates anxiety states and anxiety-related behavior. Administration of multiple anxiogenic drugs increases cellular responses (i.e., increases c-Fos expression) in a subregion of the basolateral amygdala, but the neurochemical phenotypes of these cells are not known. The basolateral amygdala contains glutamatergic projection neurons and several populations of γ-aminobutyric acid-synthesizing (GABAergic) interneurons, including a population of parvalbumin (PV)-expressing GABAergic interneurons that co-express the excitatory 5-HT2A receptor. The role for these PV-expressing GABAergic interneurons in anxiety-states is unclear. In this experiment we examined the effects of multiple anxiogenic drugs including the 5-HT2C/2A receptor agonist m-chlorophenyl piperazine (mCPP), the adenosine receptor antagonist caffeine, the α2-adrenoreceptor antagonist yohimbine and the partial inverse agonist at the benzodiazepine allosteric site on the GABAA receptor, N-methyl-beta-carboline-3-carboxamide (FG-7142), on c-Fos expression in PV-immunoreactive (PV-ir) interneurons in subdivisions of the basolateral amygdala. All drugs with the exception of mCPP increased c-Fos expression in PV-ir neurons in the basolateral amygdaloid nucleus, anterior part (BLA). The numbers of c-Fos-immunoreactive (c-Fos-ir)/PV-ir GABAergic interneurons in the BLA were positively correlated with the numbers of c-Fos-ir serotonergic neurons in the mid-rostrocaudal dorsal raphe nucleus (DR) and with a measure of anxiety-related behavior. All four drugs increased c-Fos expression in non-PV-ir cells in most of the subdivisions of the basolateral amygdala that were sampled, compared with vehicle-injected controls. Together, these data suggest that the PV/5-HT2A receptor expressing GABAergic interneurons in the basolateral amygdala are part of a DR-basolateral amygdala neuronal circuit modulating anxiety-states and anxiety-related behavior.

Original languageEnglish
Pages (from-to)1285-1293
Number of pages9
JournalProgress in Neuro-Psychopharmacology and Biological Psychiatry
Volume34
Issue number7
DOIs
StatePublished - Oct 2010

Fingerprint

Parvalbumins
Interneurons
Anxiety
Pharmaceutical Preparations
Receptor, Serotonin, 5-HT2A
Amygdala
Receptor, Serotonin, 5-HT2C
Allosteric Site
Purinergic P1 Receptor Antagonists
Aminobutyrates
Serotonergic Neurons
Neurons
Yohimbine
GABA-A Receptors
Basolateral Nuclear Complex
Caffeine
Benzodiazepines
Population
Phenotype

Keywords

  • Anxiety
  • Basolateral amygdala
  • C-Fos
  • Dorsal raphe nucleus
  • Serotonin

ASJC Scopus subject areas

  • Biological Psychiatry
  • Pharmacology

Cite this

Multiple anxiogenic drugs recruit a parvalbumin-containing subpopulation of GABAergic interneurons in the basolateral amygdala. / Hale, Matthew W.; Johnson, Philip; Westerman, Alex M.; Abrams, Jolane K.; Shekhar, Anantha; Lowry, Christopher A.

In: Progress in Neuro-Psychopharmacology and Biological Psychiatry, Vol. 34, No. 7, 10.2010, p. 1285-1293.

Research output: Contribution to journalArticle

@article{d0a73126eaa14295872f8c85f203f3be,
title = "Multiple anxiogenic drugs recruit a parvalbumin-containing subpopulation of GABAergic interneurons in the basolateral amygdala",
abstract = "The basolateral amygdala is a nodal structure within a distributed and interconnected network that regulates anxiety states and anxiety-related behavior. Administration of multiple anxiogenic drugs increases cellular responses (i.e., increases c-Fos expression) in a subregion of the basolateral amygdala, but the neurochemical phenotypes of these cells are not known. The basolateral amygdala contains glutamatergic projection neurons and several populations of γ-aminobutyric acid-synthesizing (GABAergic) interneurons, including a population of parvalbumin (PV)-expressing GABAergic interneurons that co-express the excitatory 5-HT2A receptor. The role for these PV-expressing GABAergic interneurons in anxiety-states is unclear. In this experiment we examined the effects of multiple anxiogenic drugs including the 5-HT2C/2A receptor agonist m-chlorophenyl piperazine (mCPP), the adenosine receptor antagonist caffeine, the α2-adrenoreceptor antagonist yohimbine and the partial inverse agonist at the benzodiazepine allosteric site on the GABAA receptor, N-methyl-beta-carboline-3-carboxamide (FG-7142), on c-Fos expression in PV-immunoreactive (PV-ir) interneurons in subdivisions of the basolateral amygdala. All drugs with the exception of mCPP increased c-Fos expression in PV-ir neurons in the basolateral amygdaloid nucleus, anterior part (BLA). The numbers of c-Fos-immunoreactive (c-Fos-ir)/PV-ir GABAergic interneurons in the BLA were positively correlated with the numbers of c-Fos-ir serotonergic neurons in the mid-rostrocaudal dorsal raphe nucleus (DR) and with a measure of anxiety-related behavior. All four drugs increased c-Fos expression in non-PV-ir cells in most of the subdivisions of the basolateral amygdala that were sampled, compared with vehicle-injected controls. Together, these data suggest that the PV/5-HT2A receptor expressing GABAergic interneurons in the basolateral amygdala are part of a DR-basolateral amygdala neuronal circuit modulating anxiety-states and anxiety-related behavior.",
keywords = "Anxiety, Basolateral amygdala, C-Fos, Dorsal raphe nucleus, Serotonin",
author = "Hale, {Matthew W.} and Philip Johnson and Westerman, {Alex M.} and Abrams, {Jolane K.} and Anantha Shekhar and Lowry, {Christopher A.}",
year = "2010",
month = "10",
doi = "10.1016/j.pnpbp.2010.07.012",
language = "English",
volume = "34",
pages = "1285--1293",
journal = "Progress in Neuro-Psychopharmacology and Biological Psychiatry",
issn = "0278-5846",
publisher = "Elsevier Inc.",
number = "7",

}

TY - JOUR

T1 - Multiple anxiogenic drugs recruit a parvalbumin-containing subpopulation of GABAergic interneurons in the basolateral amygdala

AU - Hale, Matthew W.

AU - Johnson, Philip

AU - Westerman, Alex M.

AU - Abrams, Jolane K.

AU - Shekhar, Anantha

AU - Lowry, Christopher A.

PY - 2010/10

Y1 - 2010/10

N2 - The basolateral amygdala is a nodal structure within a distributed and interconnected network that regulates anxiety states and anxiety-related behavior. Administration of multiple anxiogenic drugs increases cellular responses (i.e., increases c-Fos expression) in a subregion of the basolateral amygdala, but the neurochemical phenotypes of these cells are not known. The basolateral amygdala contains glutamatergic projection neurons and several populations of γ-aminobutyric acid-synthesizing (GABAergic) interneurons, including a population of parvalbumin (PV)-expressing GABAergic interneurons that co-express the excitatory 5-HT2A receptor. The role for these PV-expressing GABAergic interneurons in anxiety-states is unclear. In this experiment we examined the effects of multiple anxiogenic drugs including the 5-HT2C/2A receptor agonist m-chlorophenyl piperazine (mCPP), the adenosine receptor antagonist caffeine, the α2-adrenoreceptor antagonist yohimbine and the partial inverse agonist at the benzodiazepine allosteric site on the GABAA receptor, N-methyl-beta-carboline-3-carboxamide (FG-7142), on c-Fos expression in PV-immunoreactive (PV-ir) interneurons in subdivisions of the basolateral amygdala. All drugs with the exception of mCPP increased c-Fos expression in PV-ir neurons in the basolateral amygdaloid nucleus, anterior part (BLA). The numbers of c-Fos-immunoreactive (c-Fos-ir)/PV-ir GABAergic interneurons in the BLA were positively correlated with the numbers of c-Fos-ir serotonergic neurons in the mid-rostrocaudal dorsal raphe nucleus (DR) and with a measure of anxiety-related behavior. All four drugs increased c-Fos expression in non-PV-ir cells in most of the subdivisions of the basolateral amygdala that were sampled, compared with vehicle-injected controls. Together, these data suggest that the PV/5-HT2A receptor expressing GABAergic interneurons in the basolateral amygdala are part of a DR-basolateral amygdala neuronal circuit modulating anxiety-states and anxiety-related behavior.

AB - The basolateral amygdala is a nodal structure within a distributed and interconnected network that regulates anxiety states and anxiety-related behavior. Administration of multiple anxiogenic drugs increases cellular responses (i.e., increases c-Fos expression) in a subregion of the basolateral amygdala, but the neurochemical phenotypes of these cells are not known. The basolateral amygdala contains glutamatergic projection neurons and several populations of γ-aminobutyric acid-synthesizing (GABAergic) interneurons, including a population of parvalbumin (PV)-expressing GABAergic interneurons that co-express the excitatory 5-HT2A receptor. The role for these PV-expressing GABAergic interneurons in anxiety-states is unclear. In this experiment we examined the effects of multiple anxiogenic drugs including the 5-HT2C/2A receptor agonist m-chlorophenyl piperazine (mCPP), the adenosine receptor antagonist caffeine, the α2-adrenoreceptor antagonist yohimbine and the partial inverse agonist at the benzodiazepine allosteric site on the GABAA receptor, N-methyl-beta-carboline-3-carboxamide (FG-7142), on c-Fos expression in PV-immunoreactive (PV-ir) interneurons in subdivisions of the basolateral amygdala. All drugs with the exception of mCPP increased c-Fos expression in PV-ir neurons in the basolateral amygdaloid nucleus, anterior part (BLA). The numbers of c-Fos-immunoreactive (c-Fos-ir)/PV-ir GABAergic interneurons in the BLA were positively correlated with the numbers of c-Fos-ir serotonergic neurons in the mid-rostrocaudal dorsal raphe nucleus (DR) and with a measure of anxiety-related behavior. All four drugs increased c-Fos expression in non-PV-ir cells in most of the subdivisions of the basolateral amygdala that were sampled, compared with vehicle-injected controls. Together, these data suggest that the PV/5-HT2A receptor expressing GABAergic interneurons in the basolateral amygdala are part of a DR-basolateral amygdala neuronal circuit modulating anxiety-states and anxiety-related behavior.

KW - Anxiety

KW - Basolateral amygdala

KW - C-Fos

KW - Dorsal raphe nucleus

KW - Serotonin

UR - http://www.scopus.com/inward/record.url?scp=77956439558&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77956439558&partnerID=8YFLogxK

U2 - 10.1016/j.pnpbp.2010.07.012

DO - 10.1016/j.pnpbp.2010.07.012

M3 - Article

VL - 34

SP - 1285

EP - 1293

JO - Progress in Neuro-Psychopharmacology and Biological Psychiatry

JF - Progress in Neuro-Psychopharmacology and Biological Psychiatry

SN - 0278-5846

IS - 7

ER -