Principles of rat subcortical forebrain organization: a study using histological techniques and multiple fluorescence labeling

• Published in: Journal of chemical neuroanatomy Vol. 23; no. 2; pp. 75 - 104
• Main Authors: Riedel, A, Härtig, W, Seeger, G, Gärtner, U, Brauer, K, Arendt, Th
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01-02-2002
• Subjects: Amygdala - cytology; Animals; Antibodies; Calbindin 2; Calbindins; Calcitonin Gene-Related Peptide - analysis; Calcitonin Gene-Related Peptide - immunology; Calcium-binding proteins; Extended amygdala; Fluorescent Antibody Technique - methods; Glutamate Decarboxylase - analysis; Glutamate Decarboxylase - immunology; Islands of Calleja; Islands of Calleja - cytology; Lectins; Limbic System - cytology; Male; Myelin Basic Protein - analysis; Myelin Basic Protein - immunology; Neostriatum - cytology; Neural Pathways; Neurons - chemistry; Neurons - enzymology; Neuropeptide Y - analysis; Neuropeptide Y - immunology; Neuropeptides; Nitric Oxide Synthase - analysis; Nitric Oxide Synthase - immunology; Nitric Oxide Synthase Type I; Olfactory Pathways - cytology; Parvalbumins - analysis; Parvalbumins - immunology; Plant Lectins; Rats; Rats, Wistar; Receptors, GABA-A - analysis; Receptors, GABA-A - immunology; Receptors, N-Acetylglucosamine; S100 Calcium Binding Protein G - analysis; S100 Calcium Binding Protein G - immunology; Septal Nuclei - cytology; Septum; Sincalide - analysis; Sincalide - immunology; Striatopallidum; Substance P - analysis; Substance P - immunology; Transmitters; Tyrosine 3-Monooxygenase - analysis; Tyrosine 3-Monooxygenase - immunology; Vasoactive Intestinal Peptide - analysis; Vasoactive Intestinal Peptide - immunology; GAD 65+67, glutamic acid decarboxylase (antibody labeling 65 and 67 kDa isoforms); ir, immunoreactive, immunoreactivity; TBS-NGS-T, TBS containing 0.3% Triton X-100 and 5% normal goat serum; ACC, nucleus accumbens; Cy3, carbocyanine 3, red fluorescence; VS, ventral striatum; DAG, donkey-anti goat IgG; LOT, lateral olfactory tract; nNOS, constitutive neuronal nitric oxide synthase I; SP, substance P; Neuropeptides; Pu, putamen; GAD 67, glutamic acid decarboxylase (antibody labeling 67 kDa isoform); CaBPs, calcium binding proteins; ICJc, core-region of island of Calleja; Transmitters; TH, tyrosine hydroxylase; GP, globus pallidus; PB, phosphate buffer (0.1 M, pH 7.4); PARV, parvalbumin; VPr, reticulate ventral pallidum; Calcium-binding proteins; EA, extended amygdala; GAGP, goat-anti guinea pig IgG; VPm, subcommissural- (rostral) medial part of the ventral pallidum; BF, basal forebrain; VPn, non-reticulate ventral pallidum; ICJ, island(s) of Calleja; TBS-NDS-T, TBS containing 0.3% Triton X-100 and 5% normal donkey serum; VPl, subcommissural- (rostral) lateral part of the ventral pallidum; IPAC, interstitial nucleus of the posterior limb of the anterior commissure; WFA, Wisteria floribunda agglutinin; CCK-8, cholecystokinin; MBP, myelin basic protein; TBS, Tris-buffered saline (0.1 M, pH 7.4); VIP, vasoactive intestinal polypeptide; GAR, goat-anti rabbit IgG; OT, olfactory tubercle; Extended amygdala; SF, septofimbrial nucleus; BST, bed nucleus of stria terminalis; PL, polymorph layer of olfactory tubercle; ACsh, shell of nucleus accumbens; CALB, calbindin-D 28k; ICJsh, shell-region of island of Calleja; CP, caudate–putamen-complex; EAON, external anterior olfactory nucleus; DL, dense layer of olfactory tubercle; LS, lateral septum; MN, nucleus basalis Meynert; NPY, neuropeptide Y; VPc, caudal part of the ventral pallidum; CB(s), striatal cell bridge(s); AMCA, 7-amino-4-methylcoumarin-3-acetate; DAR, donkey-anti rabbit IgG; PIR, piriform cortex; ACc, core of nucleus accumbens; DAM, donkey-anti mouse IgG; BSA, bovine serum albumin; MFB, medial forebrain bundle; Septum; ICM, insula Calleja magna; TT, taenia tecta; Striatopallidum; ChAT, choline acetyltransferase; CALR, calretinin; Cy2, carbocyanine 2, green fluorescence; p, patch; MS, medial septum; ma, matrix; PNs, perineuronal nets; C, caudate nucleus; VP, ventral pallidum; Islands of Calleja; GABA AR-α1, GABA A receptor-α1subunit; DB, diagonal band of Broca; GAM, goat-anti mouse IgG; CGRP, calcitonin gene-related peptide
• ISSN: 0891-0618; 1873-6300
• DOI: 10.1016/S0891-0618(01)00142-9

In the present study, we introduce new views on neuro- and chemoarchitectonics of the rat forebrain subcortex deduced from traditional and current concepts of anatomical organization and from our own results. It is based on double and triple immunofluorescence of markers for transmitter-related enzymes, calcium-binding proteins, receptor proteins, myelin basic protein (MBP) and neuropeptides, and on histological cell/myelin stains. The main findings can be summarized as follows: (i) the dorsal striatum of rat and other myomorph rodents reveals a small caudate equivalent homotopic to the caudate nucleus (C) of other mammals, and a large putamen (Pu). (ii) Shell and core can be distinguished also in the ‘rostral pole’ of nucleus accumbens (ACC) with the calretinin/calbindin and neuropeptide Y (NPY) immunostaining. The shell reveals characteristics of a genuine striatal but not of an extended amygdala (EA) subunit. (iii) EA and lateral septum show striking similarities in structure and fiber connections and may therefore represent a separate parastriatal complex. (iv) The meandering dense layer (DL) of olfactory tubercle (OT) forms longitudinal gyrus- and sulcus-like structures converging in its rostral pole. (v) The core regions of the islands of Calleja that border the ventral pallidum (VP) sharing some of its features are invaded by myelinated fibers of the medial forebrain bundle (MFB). The island of Calleja magna is also apposed to an inconspicuous, slender dorsal appendage of VP. (vi) The VP is composed of a large dorsal reticulated part traversed by the myelinated GABAergic parvalbumin-immunoreactive axons of the MFB and a slender ventral non-reticulate part close to the islands of Calleja. (vii) Considering their close association to the limbic system, ventral striatum (VS) and VP may represent the oldest part of basal ganglia, whereas dorsal striatopallidal subunits were progressively developed in parallel to the growing neocortical influence on motor behavior.