Expression of neurotrophins in hippocampal interneurons immunoreactive for the neuropeptides somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholecystokinin

M. Pascual, L. Acsády, N. Rocamora, T. Freund, E. Soriano

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22 Citations (Scopus)

Abstract

Using a double detection method, which combines in situ hybridization for the detection of neurotrophin messenger RNA with immunocytochemistry against the neuropeptides somatostatin, neuropeptide Y, vasoactive intestinal polypeptide and cholecystokinin, we have analysed the expression of the neurotrophins, nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in distinct populations of neuropeptide-immunoreactive hippocampal interneurons. Nerve growth factor messenger RNA expression was found in subsets of the four subpopulations of neuropeptide-immunoreactive interneurons. The highest degree of co-localization was observed in the neuropeptide-Y-positive cells (up to 70%) and in somatostatin-immunoreactive cells (48%). Only small subsets of cholecystokinin- and vasoactive intestinal polypeptide-positive neurons (21% and 10%, respectively) displayed nerve growth factor hybridization signals. In contrast, expression of neurotrophin- 3 messenger RNA was exclusively observed in 26% of neuropeptide-Y- immunoreactive cells. Brain-derived neurotrophic factor hybridization signals were never detected in the neuropeptide-positive hippocampal interneurons. Morphological analysis of neuropeptide-immunoreactive interneurons that express or lack nerve growth factor messenger RNA revealed that most perisomatic inhibitory neurons, such as large vasoactive intestinal polypeptide/cholecystokinin-immunoreactive cells, showed positive nerve growth factor hybridization signals. In addition, some somatostatin/neuropeptide-Y-immunoreactive interneurons, which are responsible for dendritic inhibition of principal hippocampal neurons, expressed nerve growth factor messenger RNA. In contrast, interneurons specialized to innervate other GABAergic cells, such as small vasoactive intestinal polypeptide-positive cells, lacked nerve growth factor expression. All these data indicate that expression of neurotrophins is differentially regulated in functionally distinct classes of hippocampal interneurons immunoreactive for neuropeptides. We also analysed whether neuropeptide- immunoreactive interneurons expressing neurotrophins were targets of the GABAergic septohippocampal pathway. We used a triple detection method, combining anterograde tracing of this connection, with in situ hybridization for the detection of neurotrophin mRNA, and immunocytochemistry against neuropeptides. Our data showed that the four populations of hippocampal interneurons studied (somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholescystokinin) received GABAergic afferents from the septum. However, no preference for neuropeptide-immunoreactive cells expressing neurotrophins was observed, compared to neuropeptide-positive neurons lacking neurotrophin expression.

Original languageEnglish
Pages (from-to)1089-1101
Number of pages13
JournalNeuroscience
Volume89
Issue number4
DOIs
Publication statusPublished - 1999

Fingerprint

Neuropeptide Y
Vasoactive Intestinal Peptide
Cholecystokinin
Nerve Growth Factors
Interneurons
Somatostatin
Neuropeptides
Nerve Growth Factor
Messenger RNA
Neurotrophin 3
Neurons
Brain-Derived Neurotrophic Factor
In Situ Hybridization
Immunohistochemistry
Somatostatin-Secreting Cells
Population

Keywords

  • GABAergic interneurons
  • Hippocampus
  • Neuropeptides
  • Neurotrophin expression
  • Septohippocampal afferents

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

@article{1fe16150c32442d8b1f6e264ae48145a,
title = "Expression of neurotrophins in hippocampal interneurons immunoreactive for the neuropeptides somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholecystokinin",
abstract = "Using a double detection method, which combines in situ hybridization for the detection of neurotrophin messenger RNA with immunocytochemistry against the neuropeptides somatostatin, neuropeptide Y, vasoactive intestinal polypeptide and cholecystokinin, we have analysed the expression of the neurotrophins, nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in distinct populations of neuropeptide-immunoreactive hippocampal interneurons. Nerve growth factor messenger RNA expression was found in subsets of the four subpopulations of neuropeptide-immunoreactive interneurons. The highest degree of co-localization was observed in the neuropeptide-Y-positive cells (up to 70{\%}) and in somatostatin-immunoreactive cells (48{\%}). Only small subsets of cholecystokinin- and vasoactive intestinal polypeptide-positive neurons (21{\%} and 10{\%}, respectively) displayed nerve growth factor hybridization signals. In contrast, expression of neurotrophin- 3 messenger RNA was exclusively observed in 26{\%} of neuropeptide-Y- immunoreactive cells. Brain-derived neurotrophic factor hybridization signals were never detected in the neuropeptide-positive hippocampal interneurons. Morphological analysis of neuropeptide-immunoreactive interneurons that express or lack nerve growth factor messenger RNA revealed that most perisomatic inhibitory neurons, such as large vasoactive intestinal polypeptide/cholecystokinin-immunoreactive cells, showed positive nerve growth factor hybridization signals. In addition, some somatostatin/neuropeptide-Y-immunoreactive interneurons, which are responsible for dendritic inhibition of principal hippocampal neurons, expressed nerve growth factor messenger RNA. In contrast, interneurons specialized to innervate other GABAergic cells, such as small vasoactive intestinal polypeptide-positive cells, lacked nerve growth factor expression. All these data indicate that expression of neurotrophins is differentially regulated in functionally distinct classes of hippocampal interneurons immunoreactive for neuropeptides. We also analysed whether neuropeptide- immunoreactive interneurons expressing neurotrophins were targets of the GABAergic septohippocampal pathway. We used a triple detection method, combining anterograde tracing of this connection, with in situ hybridization for the detection of neurotrophin mRNA, and immunocytochemistry against neuropeptides. Our data showed that the four populations of hippocampal interneurons studied (somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholescystokinin) received GABAergic afferents from the septum. However, no preference for neuropeptide-immunoreactive cells expressing neurotrophins was observed, compared to neuropeptide-positive neurons lacking neurotrophin expression.",
keywords = "GABAergic interneurons, Hippocampus, Neuropeptides, Neurotrophin expression, Septohippocampal afferents",
author = "M. Pascual and L. Acs{\'a}dy and N. Rocamora and T. Freund and E. Soriano",
year = "1999",
doi = "10.1016/S0306-4522(98)00391-1",
language = "English",
volume = "89",
pages = "1089--1101",
journal = "Neuroscience",
issn = "0306-4522",
publisher = "Elsevier Limited",
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TY - JOUR

T1 - Expression of neurotrophins in hippocampal interneurons immunoreactive for the neuropeptides somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholecystokinin

AU - Pascual, M.

AU - Acsády, L.

AU - Rocamora, N.

AU - Freund, T.

AU - Soriano, E.

PY - 1999

Y1 - 1999

N2 - Using a double detection method, which combines in situ hybridization for the detection of neurotrophin messenger RNA with immunocytochemistry against the neuropeptides somatostatin, neuropeptide Y, vasoactive intestinal polypeptide and cholecystokinin, we have analysed the expression of the neurotrophins, nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in distinct populations of neuropeptide-immunoreactive hippocampal interneurons. Nerve growth factor messenger RNA expression was found in subsets of the four subpopulations of neuropeptide-immunoreactive interneurons. The highest degree of co-localization was observed in the neuropeptide-Y-positive cells (up to 70%) and in somatostatin-immunoreactive cells (48%). Only small subsets of cholecystokinin- and vasoactive intestinal polypeptide-positive neurons (21% and 10%, respectively) displayed nerve growth factor hybridization signals. In contrast, expression of neurotrophin- 3 messenger RNA was exclusively observed in 26% of neuropeptide-Y- immunoreactive cells. Brain-derived neurotrophic factor hybridization signals were never detected in the neuropeptide-positive hippocampal interneurons. Morphological analysis of neuropeptide-immunoreactive interneurons that express or lack nerve growth factor messenger RNA revealed that most perisomatic inhibitory neurons, such as large vasoactive intestinal polypeptide/cholecystokinin-immunoreactive cells, showed positive nerve growth factor hybridization signals. In addition, some somatostatin/neuropeptide-Y-immunoreactive interneurons, which are responsible for dendritic inhibition of principal hippocampal neurons, expressed nerve growth factor messenger RNA. In contrast, interneurons specialized to innervate other GABAergic cells, such as small vasoactive intestinal polypeptide-positive cells, lacked nerve growth factor expression. All these data indicate that expression of neurotrophins is differentially regulated in functionally distinct classes of hippocampal interneurons immunoreactive for neuropeptides. We also analysed whether neuropeptide- immunoreactive interneurons expressing neurotrophins were targets of the GABAergic septohippocampal pathway. We used a triple detection method, combining anterograde tracing of this connection, with in situ hybridization for the detection of neurotrophin mRNA, and immunocytochemistry against neuropeptides. Our data showed that the four populations of hippocampal interneurons studied (somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholescystokinin) received GABAergic afferents from the septum. However, no preference for neuropeptide-immunoreactive cells expressing neurotrophins was observed, compared to neuropeptide-positive neurons lacking neurotrophin expression.

AB - Using a double detection method, which combines in situ hybridization for the detection of neurotrophin messenger RNA with immunocytochemistry against the neuropeptides somatostatin, neuropeptide Y, vasoactive intestinal polypeptide and cholecystokinin, we have analysed the expression of the neurotrophins, nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in distinct populations of neuropeptide-immunoreactive hippocampal interneurons. Nerve growth factor messenger RNA expression was found in subsets of the four subpopulations of neuropeptide-immunoreactive interneurons. The highest degree of co-localization was observed in the neuropeptide-Y-positive cells (up to 70%) and in somatostatin-immunoreactive cells (48%). Only small subsets of cholecystokinin- and vasoactive intestinal polypeptide-positive neurons (21% and 10%, respectively) displayed nerve growth factor hybridization signals. In contrast, expression of neurotrophin- 3 messenger RNA was exclusively observed in 26% of neuropeptide-Y- immunoreactive cells. Brain-derived neurotrophic factor hybridization signals were never detected in the neuropeptide-positive hippocampal interneurons. Morphological analysis of neuropeptide-immunoreactive interneurons that express or lack nerve growth factor messenger RNA revealed that most perisomatic inhibitory neurons, such as large vasoactive intestinal polypeptide/cholecystokinin-immunoreactive cells, showed positive nerve growth factor hybridization signals. In addition, some somatostatin/neuropeptide-Y-immunoreactive interneurons, which are responsible for dendritic inhibition of principal hippocampal neurons, expressed nerve growth factor messenger RNA. In contrast, interneurons specialized to innervate other GABAergic cells, such as small vasoactive intestinal polypeptide-positive cells, lacked nerve growth factor expression. All these data indicate that expression of neurotrophins is differentially regulated in functionally distinct classes of hippocampal interneurons immunoreactive for neuropeptides. We also analysed whether neuropeptide- immunoreactive interneurons expressing neurotrophins were targets of the GABAergic septohippocampal pathway. We used a triple detection method, combining anterograde tracing of this connection, with in situ hybridization for the detection of neurotrophin mRNA, and immunocytochemistry against neuropeptides. Our data showed that the four populations of hippocampal interneurons studied (somatostatin, neuropeptide-Y, vasoactive intestinal polypeptide and cholescystokinin) received GABAergic afferents from the septum. However, no preference for neuropeptide-immunoreactive cells expressing neurotrophins was observed, compared to neuropeptide-positive neurons lacking neurotrophin expression.

KW - GABAergic interneurons

KW - Hippocampus

KW - Neuropeptides

KW - Neurotrophin expression

KW - Septohippocampal afferents

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U2 - 10.1016/S0306-4522(98)00391-1

DO - 10.1016/S0306-4522(98)00391-1

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JO - Neuroscience

JF - Neuroscience

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ER -