Development of β1 and β2 adrenergic receptors in baboon brain: An autoradiographic study using [125I]iodocyanopindolol

Slesinger, Paul A.; Löwenstein, Pedro R.; Singer, Harvey S.; Walker, Lary C.; Price, Donald L.; Coyle, Joseph T.

doi:10.1002/cne.902730304

Cited by 23 publications

(12 citation statements)

References 48 publications

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“…A few available studies of the striatum in baboons show prenatal and/or postnatal changes in adrenergic, cholinergic, and dopaminergic ligand binding sites by autoradiography (Slesinger et al, 1988; Lowenstein et al, 1989) as well as sodium-dependent high affinity choline uptake binding sites (Lowenstein et al, 1987). However the normal spatiotemporal development of connectively, cell adhesion molecules, synapses, neurotransmitters, receptor proteins, and signal transduction molecules in the striatum of non-human primates is mostly unknown.…”

Section: Discussionmentioning

confidence: 99%

The non-human primate striatum undergoes marked prolonged remodeling during postnatal development

Martin

Cork

2014

Front. Cell. Neurosci.

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We examined the postnatal ontogeny of the striatum in rhesus monkeys (Macaca mulatta) to identify temporal and spatial patterns of histological and chemical maturation. Our goal was to determine whether this forebrain structure is developmentally static or dynamic in postnatal life. Brains from monkeys at 1 day, 1, 4, 6, 9, and 12 months of age (N = 12) and adult monkeys (N = 4) were analyzed. Nissl staining was used to assess striatal volume, cytoarchitecture, and apoptosis. Immunohistochemistry was used to localize and measure substance P (SP), leucine-enkephalin (LENK), tyrosine hydroxylase (TH), and calbindin D28 (CAL) immunoreactivities. Mature brain to body weight ratio was achieved at 4 months of age, and striatal volume increased from ∼1.2 to ∼1.4 cm3 during the first postnatal year. Nissl staining identified, prominently in the caudate nucleus, developmentally persistent discrete cell islands with neuronal densities greater than the surrounding striatal parenchyma (matrix). Losses in neuronal density were observed in island and matrix regions during maturation, and differential developmental programmed cell death was observed in islands and matrix regions. Immunohistochemistry revealed striking changes occurring postnatally in striatal chemical neuroanatomy. At birth, the immature dopaminergic nigrostriatal innervation was characterized by islands enriched in TH-immunoreactive puncta (putative terminals) in the neuropil; TH-enriched islands aligned completely with areas enriched in SP immunoreactivity but low in LENK immunoreactivity. These areas enriched in SP immunoreactivity but low in LENK immunoreactivity were identified as striosome and matrix areas, respectively, because CAL immunoreactivity clearly delineated these territories. SP, LENK, and CAL immunoreactivities appeared as positive neuronal cell bodies, processes, and puncta. The matrix compartment at birth contained relatively low TH-immunoreactive processes and few SP-positive neurons but was densely populated with LENK-immunoreactive neurons. The nucleus accumbens part of the ventral striatum also showed prominent differences in SP, LENK, and CAL immunoreactivities in shell and core territories. During 12 months of postnatal maturation salient changes occurred in neurotransmitter marker localization: TH-positive afferents densely innervated the matrix to exceed levels of immunoreactivity in the striosomes; SP immunoreactivity levels increased in the matrix; and LENK-immunoreactivity levels decreased in the matrix and increased in the striosomes. At 12 months of age, striatal chemoarchitecture was similar qualitatively to adult patterns, but quantitatively different in LENK and SP in caudate, putamen, and nucleus accumbens. This study shows for the first time that the rhesus monkey striatum requires more than 12 months after birth to develop an adult-like pattern of chemical neuroanatomy and that principal neurons within striosomes and matrix have different developmental programs for neuropeptide expression. We conclude that postnatal matura...

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Section: Discussionmentioning

confidence: 99%

The non-human primate striatum undergoes marked prolonged remodeling during postnatal development

Martin

Cork

2014

Front. Cell. Neurosci.

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“…These results are in agreement with previous studies in the avian brain, where ICYP binding attributable to b 2 -ARs is higher in the chick and pigeon mesopallium and hippocampus as compared to b 1 -AR binding (FernandezLopez et al, 1997). However, in mammalian species (baboon, rat, guinea-pig), b 1 -AR binding was higher in all brain regions, apart from the hippocampus, where b 2 -AR binding was higher in baboons (Slesinger et al, 1988) but similar levels in rat and guinea-pig hippocampus (Booze et al, 1989). Another study in rat hippocampus showed higher b 1 -AR populations as compared to b 2 -ARs (Rainbow et al, 1984).…”

Section: Role Of Hippocampal B 1 -Ars In Memory Formationmentioning

confidence: 95%

Memory Processing in the Avian Hippocampus Involves Interactions between β-Adrenoceptors, Glutamate Receptors, and Metabolism

Gibbs

Bowser

Hutchinson

et al. 2008

Neuropsychopharmacol

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Noradrenaline is known to modulate memory formation in the mammalian hippocampus. We have examined how noradrenaline and selective beta-adrenoceptor (AR) agonists affect memory consolidation and how antagonists inhibit memory consolidation in the avian hippocampus. Injection of selective beta-AR agonists and antagonists at specific times within 30 min of a weakly or strongly reinforced, single-trial, bead discrimination learning test in 1-day-old chicks allowed us to determine the pattern of beta-AR involvement in hippocampal memory processing. Different beta-AR subtypes were recruited in temporal sequence after learning in the order beta(1), beta(3), and beta(2.) We provide evidence that the effect of manipulation of beta(1)-ARs by selective agonists and antagonists within 2.5 min of training parallels the action of NMDA receptor agonists and antagonists. Activation of beta(3)- and beta(2)-ARs facilitated memory but utilized different mechanisms: beta(3)-ARs by stimulating glucose uptake and metabolism, and beta(2)-ARs by increasing the breakdown of glycogen--with both metabolic events occurring in astrocytes and affecting intermediate memory. The different receptors are activated at different times within the lifetime of labile memory and within 30 min of learning. We have defined separate roles for the three beta-ARs in memory and demonstrated that the avian hippocampus is involved in learning and memory in much the same way as the hippocampus in the mammalian brain.

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“…Thus, the hypothesis that disturbances in the expression of p1 receptors predominantly contribute to neuropsychiatric illness is largely based on studies of beta-receptor regulation in the rat. It is known that the distribution of P-receptors varies significantly between the rat and other species, such as the guinea pig, baboon, and human (Booze et al, 1989;De Paermentier et al, 1989;Pazos et al, 1985;Reznikoff et al, 1986;Shimohama et al, 1987;Slesinger et al, 1988). Thus, it is possible that the regulation of P-receptors may also vary between species.…”

Section: Introductionmentioning

confidence: 99%

Distribution of beta‐adrenergic receptor subtypes in human post‐mortem brain: Alterations in limbic regions of schizophrenics

Joyce

Lexow

Kim

et al. 1992

Synapse

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The distribution of the beta 1 (beta 1) and beta 2 (beta 2) subtypes of the beta-adrenergic receptor was examined in rat and nondiseased control human tissue. The distribution of the beta 1 and beta 2 receptors was also examined in schizophrenic cases, with additional studies in schizophrenic suicide and nonschizophrenic suicide cases. Scatchard analysis of the binding of [125I]iodopindolol (IPIN) to cortical membranes showed a similar Kd in human (177 pM) and rat (161 pM), but a lower maximum binding site (Bmax) in the human tissue (18.7 fmol/mg protein and 55.6 fmol/mg protein). For the autoradiographic studies [125I]IPIN was used to visualize both subtypes (total) or was displaced with the selective beta 1-receptor antagonist ICI-89,406 to visualize beta 2 sites, or with the selective beta 2-receptor antagonist ICI-118,551 to visualize beta 1 sites. Important differences in the regional distribution of the two subtypes of the beta-adrenergic receptors were noted between rat and human. In the nucleus accumbens and ventral putamen (ventral striatum), a patchy distribution of beta 1 receptors was observed that was not evident in the rat. These patches were aligned with markers of the matrix compartment of the striatum. The schizophrenic cases showed significant increases in the labeling of the beta 1-receptor patches with [125I]IPIN. In contrast to the frontal cortex of the nondisease controls, the parietal and temporal cortex showed a high ratio of beta 1 to beta 2 receptors and a highly laminar organization of the subtypes. [125I]IPIN binding to beta 1 receptors was highest in the external laminae with the reverse gradient for the beta 2 subtype. The medial temporal cortex displayed an alteration in the ratio of the 2 subtypes of the beta-adrenergic receptor, with the parahippocampus and hippocampus of the human, in contrast to the rat brain, predominantly expressing the beta 2 receptor. Moreover, there were consistently higher densities of beta 2 receptors in the hippocampus of the right hemisphere than the left hemisphere of the nondisease controls. There was not a left and right hemispheric asymmetry of beta 2 receptors in the hippocampus of elderly schizophrenics or in young schizophrenics who committed suicide. The asymmetry was evident in nonschizophrenic suicides, suggesting that the lack of asymmetry in the hippocampus of schizophrenics is evident early in the disease process. Thus limbic structures show alterations in the patterning of beta 1 and beta 2 receptors in the schizophrenic cases.

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Development of β₁ and β₂ adrenergic receptors in baboon brain: An autoradiographic study using [¹²⁵I]iodocyanopindolol

Cited by 23 publications

References 48 publications

The non-human primate striatum undergoes marked prolonged remodeling during postnatal development

The non-human primate striatum undergoes marked prolonged remodeling during postnatal development

Memory Processing in the Avian Hippocampus Involves Interactions between β-Adrenoceptors, Glutamate Receptors, and Metabolism

Distribution of beta‐adrenergic receptor subtypes in human post‐mortem brain: Alterations in limbic regions of schizophrenics

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