Extensive co-existence of neuropeptides in the rat visual cortex

doi:10.1016/0006-8993(87)90243-5

Brain Research

Volume 420, Issue 1, 8 September 1987, Pages 95-99

https://doi.org/10.1016/0006-8993(87)90243-5 Get rights and content

Abstract

The peroxidase-antiperoxidase immunohistochemical technique has been used to examine the co-existence of peptides within individual neurons of the rat visual cortex. Pairs of consecutive paraffin sections were stained alternately for 2 of the 4 peptides: somatostatin (SRIF), vasoactive intestinal polypeptide (VIP), cholecystokinin (CCK) and neuropeptide Y (NPY). Analysis revealed the co-existence of SRIF with VIP, CCK and NPY and between VIP and CCK. These results show that the localization of neuropeptides in cortical neurons is more widespread than previously demonstrated.

References (36)

BrashearH.R. et al.
Distribution of GABAergic and cholinergic neurons in the rat diagonal band
Neuroscience
(1986)
ChronwallB.M. et al.
Coexistence of neuropeptide Y and somatostatin in rat and human cortical and rat hypothalamic neurons
Neurosci. Lett.
(1984)
ConnorJ.R. et al.
Vasoactive intestinal polypeptide-immunoreactive neurons in rat visual cortex
Neuroscience
(1984)
JonesE.G. et al.
Co-localization of GABA and neuropeptides in neocortical neurons
TINS
(1986)
ParnavelasJ.G.
Morphology and distribution of peptide-containing neurons in the cerebral cortex
PennyG.R. et al.
Substance P-immunoreactive neurons in the neocortex of the rat: a subset of the glutamic acid decarboxylase-immunoreactive neurons
Neurosci. Lett.
(1986)
PetersA. et al.
Cholecystotokinin-like immunoreactive neurons in rat cerebral cortex
Neuroscience
(1983)
SugimotoT. et al.
Coexistence of neuropeptides in projection neurons of the thalamus i the ca
Brain Research
(1985)
VincentS.R. et al.
Coexistence of somatostatin- and avian pancreatic polypeptide (app)-like imins some forebrain beurons
Neuroscience
(1982)
BurnstockG.
Neuropeptides as trophic factors

EckensteinF. et al.

Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide

Nature (London)

(1984)

EmsonP.C. et al.

Peptide-containing neurons of the cerebral cortex

HendryS.H.C. et al.

Neuropeptide-containing neurons in the cerebral cortex are also GABAergic

HouserC.R. et al.

GABA neurons in the cerebral cortex

HouserC.R. et al.

Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses

J. Comp. Neurol.

(1985)

IversenL.L.

Amino-acids and peptides: fast and slow chemical signals in the nervous system

KellyJ.S.

Electrophysiology of peptides in the central nervous system

Br. Med. Bull.

(1982)

KosakaT. et al.

GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus

J. Comp. Neurol.

(1985)

Cited by (58)

Apoptosis in the visual system of normal and dark-reared rats
1999, Brain Research
Apoptotic cell death, known to play a role in the developing brain, was immunocytochemically mapped in cortical and subcortical visual centers of Wistar rats developing under normal lighting conditions or in complete darkness. Apoptosis was relatively pronounced and exhibited the same developmental pattern in all visual centers examined. Visual deprivation was found to have negligible effects on apoptosis in subcortical areas, or to amplify it temporarily in the cerebral cortex.
Ultrastructural evidence for combined action of noradrenaline and vasoactive intestinal polypeptide upon neurons, astrocytes, and blood vessels of the rat cerebral cortex
1998, Brain Research Bulletin
The intracortical organization of the noradrenaline (NA) and vasoactive intestinal polypeptide (VIP) systems provides ample opportunity for functional convergence, and accumulated evidence indicates that NA and VIP share certain cellular actions upon both neuronal and nonneuronal cortical elements. In the present study, a double immunolabeling method was combined with a silver–gold intensification procedure to examine the ultrastructural relationships of the NA coeruleocortical afferents and the intrinsic VIP neurons with three main constituents of the cortex: neurons, astrocytes, and blood vessels. Electron microscopy of singly or doubly labeled material indicated that NA and VIP boutons are engaged in a variety of anatomical relationships with both neuronal and nonneuronal elements. Dendritic shafts and perikarya of nonpyramidal neurons, some of which are VIP positive, receive combined NA and VIP synapses. A significant number of cortical microvessels are in intimate contact with NA or VIP profiles. NA axons often form perivascular loops, and VIP dendritic shafts of large diameter are frequently observed to bend around the vessel circumference. Serial section examination demonstrates that some NA boutons are directly apposed to the capillary wall at sites of glial end-feet discontinuities, whereas VIP boutons contact astrocytic sleeves of capillaries but never cross the perivascular astroglial barrier. Some VIP dendrites containing coated vesicles make intimate contact with the capillary basal lamina. Astrocytic perikarya, mainly in the supragranular layers, are also directly apposed to NA and/or VIP elements. These complex anatomical relationships provide a structural basis for the known interactions between NA and VIP in the control of cortical metabolism and function.
Postnatal development of somatostatin- and neuropeptide Y-immunoreactive neurons in rat cerebral cortex: A double-labeling immunohistochemical study
1998, International Journal of Developmental Neuroscience
The postnatal development of somatostatin (SOM)- and neuropeptide Y(NPY)-immunoreactive (ir) neurons was examined in rat cerebral cortex, while considering theircoexistence in cortical neurons. Using double immunohistochemical staining for SOM and NPYwith diaminobenzidine and benzidine dihydrochloride as chromogens, we subdividedimmunoreactive cells into double-labeled SOM/NPY-, SOM only-, and NPY only-ir neurons.SOM/NPY- and SOM only-ir neurons were detectable even at the day of birth, in contrast toNPY only-ir cells which first appeared in most cortices from week two. The morphologicalfeatures of double-labeled SOM/NPY neurons differed with those of SOM only- and NPYonly-ir neurons. No apparent changes in the shape and size of single-labeled neurons occurredwith age ; throughout their postnatal life they were round and ovoid, had a thin rim ofperinuclear cytoplasm, and short processes. However, the features of SOM/NPY-ir neurons werenot consistent according to postnatal age ; by day P7, these neurons showed immature featuresand they began to show more advanced neuronal characteristics by week P2, when they had alarger and more intensely-stained cytoplasm. In addition, their processes were longer, thicker andmore complex than at earlier ages. At this age, SOM/NPY-ir somata were close to their nearmaximum size. From week P4, they became smaller and were lightly labeled. SOM/NPY-irsomata were larger than SOM only- and NPY only-ir somata at and after two weeks of age. Thepresent results, showing different postnatal maturation patterns such as time of appearance andmorphological features, raise the possibilities that double-labeled SOM/NPY and single-labeledimmunoreactive neurons may be different populations regulated by different mechanisms in theirdevelopment, and with different functional properties during development.
Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons
1997, Brain Research
Examination of cholecystokinin-immunoreactive cells in the rat frontal cortex revealed the presence in layers I–VI of a non-uniform population ranging in size from small to large. All were also immunoreactive for GABA. The most commonly observed dendritic form of the small cells were bipolar or bitufted although some were multipolar and demonstrated vasoactive intestinal polypeptide and a few case calretinin immunoreactivity. The large cells were multipolar or bitufted and lacked expression of vasoactive intestinal polypeptide and calretinin immunoreactivity but occasionally showed calbindin D28k immunoreactivity. Therefore, the cholecystokinin-immunoreactive cells could be divided into two distinct subpopulations depending on their chemistry andn morphology. Our previous studis showed that GABAergic cells in teh neocortex could be classified into at least three chemically different subgroups: (1) par valbumin-containing cells: (2) somatostatin-containing cells (most of them also contain calbindin D28k): and (3) vasoactive intestinal polypeptide- and/or calretinin-containing cells. The present results indicated that the small cholecystokinin-immunoreactive non-pyramidal cells constitute a subset of the vsoactive intestinal polypeptide- and/or calretinin-containing cortical GABAergic cells. The large cells remain to be categorized. kwInterneuron; VIP; Calretinin; Calbindin D28k; Co-localization
Distinct choline acetyltransferase (ChAT) and vasoactive intestinal polypeptide (VIP) bipolar neurons project to local blood vessels in the rat cerebral cortex
1994, Brain Research
Innervation of rat intracortical cerebral blood vessels by acetylcholine (ACh) and vasoactive intestinal polypeptide (VIP) remains largely unexplored and it is known if the cells of origin are intra- or extracortical nor perivascular fibers colocalize ACh and VIP. Cortical cholinergic innervation arises primarily from the basal forebrain and to a small extent from intrinsic bipolar ACh neurons thought to be the sole source of cortical VIP. In order evaluate if intracortical perivascular ACh terminals could be distinguished from those of the basal forebrain by their colocalization with VIP, we performed a double immunofluorescence study and determined the percentage of colocalization of choline acetyltransferase (ChAT) and VIP in cortical neurons, as well as in terminal fields associated with intracortical blood vessels. From a total of 2103 cells examined in all cortical areas, VIP neurons accounted for the largest population (58.3%) followed by ChAT-positive cells (28.2%) with only 13.5% of cells being double-labelled for VIP and ChAT. Of the cortical ChAT-immunostained cells (n = 878), 32.3% colocalized VIP whereas only 18.8% of VIP neurons (n = 1509) also contained ChAT. In various cortical areas, ChAT cell bodies were seen to be contacted by VIP terminals which surrounded closely their cell soma and proximal dendrites. Perivascular fibers studied by double immunofluorescence and confocal microscopy were of three categories including cholinergic, VIPergic with a smaller population of fibers which costained for both ChAT and VIP. These results show hat cortical VIP neurons are much more numerous than those containing ChAT, and that a majority of VIP neurons do not colocalize with ChAT. This observation indicates that ACh and VIP are primarily located in distinct neuronal populations and that VIP cannot be used as a marker of intracortical ACh neurons and terminals. Our results further suggest that intracortical blood vessels are primarily under the influence of distinct ChAT and VIP perivascular fibers. Also, the presence of a subset of VIP and ChAT/VIP fibers in association with intracortical blood vessels strongly suggests a role for cortical bipolar neurons in local cerebrovascular regulation. The origin of the perivascular ChAT fibers which do not colocalize VIP, however, remains unknown.
Morphological and chemical characteristics of substance P receptor-immunoreactive neurons in the rat neocortex
1994, Neuroscience
Substance P receptor-expressing neurons in the rat cerebral neocortex were examined by single- and double-immunolabeling methods with an affinity-purified specific antibody to substance P receptor. Substance P receptor immunoreactivity was observed exclusively in non-pyramidal neurons. About a quarter of these substance P receptor-positive neocortical neurons showed intense immunoreactivity, and the other three quarters displayed weak substance P receptor immunoreactivity. The neurons showing intense substance P receptor immunoreactivity were large multipolar cells with a few long aspiny or sparsely-spiny dendrites, and were scattered throughout the neocortical layers except for layer I, and also in the underlying white matter. The weakly immunoreactive neurons were medium-sized multipolar cells with oval to round somata and aspiny varicose dendrites, and were distributed in all cortical layers with a bias to layers II–III and the superficial part of layer V.
The double-immunofluorescence study revealed that almost all substance P receptor-positive neurons were immunoreactive for GABA, but negative for glutaminase. Substance P receptor immunoreactivity in GABAergic neocortical neurons were further examined by the double-immunofluorescence method with antibodies to markers for subgroups of GABAergic neurons. Somatostatin immunoreactivity was found in 89% of neurons with intense substance P receptor immunoreactivity, and in 1.5% of neurons with weak substance P receptor immunoreactivity. Neuropeptide Y immunoreactivity was also observed in 92% of neurons with intense immunoreactivity for substance P receptor, and in 1.6% of neurons with weak immunoreactivity for substance P receptor. In contrast, parvalbumin immunoreactivity was seen in 1.3% of neurons with intense substance P receptor immunoreactivity, and in 59% of weak substance P receptor immunoreactivity. Calbindin D_28k immunoreactivity was found in 12 and 19% of neurons, respectively, with weak and intense immunoreactivities for substance P receptor. Virtually no cells showing substance P receptor immunoreactivity displayed immunoreactivity for vasoactive intestinal polypeptide or choline acetyltransferase.
These results indicate that the neocortical neurons expressing substance P receptor constitute a subpopulation of GABAergic non-pyramidal cells, and are segregated into neurons with intense immunoreactivity and those with weak immunoreactivity for substance P receptor; the vast majority of neurons with intense substance P receptor immunoreactivity contain somatostatin and neuropeptide Y, and the majority of neurons with weak substance P receptor immunoreactivity have parvalbumin.

View all citing articles on Scopus

View full text

Extensive co-existence of neuropeptides in the rat visual cortex

Abstract

Neuroscience

Neurosci. Lett.

Neuroscience

TINS

Neurosci. Lett.

Neuroscience

Brain Research

Neuroscience

Neuropeptides as trophic factors

Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide

Nature (London)

Peptide-containing neurons of the cerebral cortex

Neuropeptide-containing neurons in the cerebral cortex are also GABAergic

GABA neurons in the cerebral cortex

Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses

J. Comp. Neurol.

Amino-acids and peptides: fast and slow chemical signals in the nervous system

Electrophysiology of peptides in the central nervous system

Br. Med. Bull.

GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus

J. Comp. Neurol.