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Nitric oxide synthase-containing neurons in the amygdaloid nuclear complex of the rat

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Abstract

The nitric oxide-producing neurons in the rat amygdala (Am) were studied, using reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPHd) histochemistry. Almost all nuclei of the Am contained NADPHd-positive neurons and fibers, but the somatodendritic morphology and the intensity of staining of different subpopulations varied. The strongly stained neurons displayed labeling of the perikaryon and the dendritic tree with Golgi impregnation-like quality, whilst the dendrites of the lightly stained neurons were less successfully followed. Many strongly positive neurons were located in the external capsule and within the intraamygdaloid fiber bundles. A large number of small, strongly stained cells was present in the amygdalostriatal transition area. In the Am proper, a condensation of deeply stained cells occurred in the lateral amygdaloid nucleus. In the basolateral nucleus, the strongly NADPHd-positive neurons were few, and were located mainly along the lateral border of the nucleus. These cells clearly differed from the large, pyramidal, and efferent cells. The basomedial nucleus contained numerous positive cells but most of them were only lightly labeled. A moderate number of strongly stained neurons appeared in the medial division of the central nucleus, and a larger accumulation of strongly positive cells was present in the lateral and the capsular divisions. The medial amygdaloid nucleus contained numerous moderately stained neurons and displayed the strongest diffuse neuropil staining in Am. In the nucleus of the lateral olfactory tract, the first layer contained only NADPHd-stained axons, in the second layer, there were numerous moderately stained cells, and in the third layer, a few but deeply stained neurons. From the cortical nuclei, the most appreciable number of stained neurons was seen in the anterior cortical nucleus. The anterior amygdaloid area contained numerous NADPHd-positive neurons; in its dorsal part the majority of cells were only moderately stained, whereas in the ventral part the neurons were very strongly stained. The intercalated amygdaloid nucleus lacked NADPHd-positive neurons but an appreciable plexus of fine, tortuous axons was present. In the intra-amygdaloid part of the bed nucleus of the stria terminalis (st) some lightly stained cells were seen but along the entire course of st strongly stained neurons were observed. Some Am nuclei, and especially the central lateral nucleus and the intercalated nucleus, display considerable species differences when compared with the primate Am. The age-related changes of the nitrergic Am neurons, as well as their involvement in neurodegenerative diseases is discussed.

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Abbreviations

AA:

Anterior amygdaloid area

AAD:

Anterior amygdaloid area, dorsal part

AAV:

Anterior amygdaloid area, ventral part

ACo:

Anterior cortical amygdaloid nucleus

Am:

Amygdala, amygdaloid nuclear complex

AStr:

Amygdalostriatal transition area

BL:

Basolateral amygdaloid nucleus

BM:

Basomedial amygdaloid nucleus

BST:

Bed nucleus of the stria terminalis

BSTIA:

Bed nucleus of the stria terminalis, intraamygdaloid division

Ce:

Central amygdaloid nucleus

CeC:

Central amygdaloid nucleus, capsular division

CeL:

Central amygdaloid nucleus, lateral division

CeM:

Central amygdaloid nucleus, medial division

Co:

Cortical amygdaloid nuclei

DEn:

Dorsal endopiriform nucleus

IM:

Intercalated amygdaloid nucleus

iNOS:

Inducible nitric oxide synthase

La:

Lateral amygdaloid nucleus

LOT:

Nucleus of the lateral olfactory tract

LOT 1:

Nucleus of the lateral olfactory tract, first layer

LOT 2:

Nucleus of the lateral olfactory tract, second layer

LOT 3:

Nucleus of the lateral olfactory tract, third layer

Me:

Medial amygdaloid nucleus

MeAV:

Medial amygdaloid nucleus, anteroventral part

NADPHd:

Nicotinamide adenine dinucleotide phosphate diaphorase

nNOS:

Neuronal nitric oxide synthase

NO:

Nitric oxide

NOS:

Nitric oxide synthase

OT:

Optic tract

PB:

Phosphate buffer

PBS:

Phosphate buffered saline

Pir:

Piriform cortex

PLCo:

Posterolateral cortical amygdaloid nucleus

PRh:

Perirhinal cortex

st:

Stria terminalis

VEn:

Ventral endopiriform nucleus

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Acknowledgments

The expert technical assistance of Mrs. Barbara Kuhnke (Rostock), Mrs. Ekaterina A. Zlatanova, Mrs. Snejina S. Ilieva, and Mrs. Elena I. Ivanova (Sofia) is gratefully acknowledged. Grant sponsors: This work was supported by grants of the Federal Ministry of Education and Research (BMBF, 01 ZZ 0108) and of the Ministry of Education, Science and Culture of Mecklenburg-Vorpommern, by a research grant of Pfizer, Karlsruhe/Germany, and National Science Fund of Bulgaria (No L1012/2001).

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  1. Faculty of Medicine, Department of Anatomy and Histology, Medical University, Sofia, 1431, Bulgaria

    K. G. Usunoff

  2. Institute of Physiology, Bulgarian Academy of Sciences, Sofia, 1113, Bulgaria

    K. G. Usunoff & D. E. Itzev

  3. Faculty of Medicine, Institute of Anatomy, University of Rostock, P. O. Box 10 08 88, 18055, Rostock, Germany

    K. G. Usunoff, O. Schmitt & A. Wree

  4. Faculty of Medicine, Department of Neurology, University of Rostock, P. O. Box 10 08 88, 18055, Rostock, Germany

    A. Rolfs

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Usunoff, K.G., Itzev, D.E., Rolfs, A. et al. Nitric oxide synthase-containing neurons in the amygdaloid nuclear complex of the rat. Anat Embryol 211, 721–737 (2006). https://doi.org/10.1007/s00429-006-0134-9

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