Ontogeny of M1 and M2 muscarinic binding sites in the striatum of the cat: Relationships to one another and to striatal compartmentalization

Nastuk, Mary A.; Graybiel, Ann M.

doi:10.1016/0306-4522(89)90316-3

Cited by 16 publications

(4 citation statements)

References 67 publications

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“…The striosomal-matrix compartmentalization of m1 receptor expression delineated in this study is in accord with findings of muscarinic binding patterns in young rats, cats, and ferrets and in adult cats (Nastuk and Graybiel, 1985) and is also in register with m1 and m2 receptor binding in adult cats, monkeys, and humans (Nastuk and Graybiel, 1988) and in developing cats (Nastuk and Graybiel, 1989). In juvenile monkeys, m1 was more intense in matrix zones compared with striosomes.…”

Section: Segregated Distribution Of Muscarinic M1 and M2 Receptorssupporting

confidence: 89%

Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto‐striatal pathways

Alcantara

Mrzljak

Jakab

et al. 2001

J of Comparative Neurology

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The cellular and subcellular localization of muscarinic receptor proteins m1 and m2 was examined in the neostriatum of macaque monkeys by using light and electron microscopic immunocytochemical techniques. Double-labeling immunocytochemistry revealed m1 receptors in calbindin-D28k--positive medium spiny projection neurons. Muscarinic m1 labeling was dramatically more intense in the striatal matrix compartment in juvenile monkeys but more intense in striosomes in the adult caudate, suggesting that m1 expression undergoes a developmental age-dependent change. Ultrastructurally, m1 receptors were predominantly localized in asymmetric synapse-forming spines, indicating that these spines receive extrastriatal excitatory afferents. The association of m1-positive spines with lesion-induced degenerating prefronto-striatal axon terminals demonstrated that these afferents originate in part from the prefrontal cortex. The synaptic localization of m1 in these spines indicates a role of m1 in the modulation of excitatory neurotransmission. To a lesser extent, m1 was present in symmetric synapses, where it may also modulate inhibitory neurotransmission originating from local striatal neurons or the substantia nigra. Conversely, m2/choline acetyltransferase (ChAT) double labeling revealed that m2-positive neurons corresponded to large aspiny cholinergic interneurons and ultrastructurally, that the majority of m2 labeled axons formed symmetric synapses. The remarkable segregation of the m1 and m2 receptor proteins to projection and local circuit neurons suggests a functional segregation of m1 and m2 mediated cholinergic actions in the striatum: m1 receptors modulate extrinsic glutamatergic and monoaminergic afferents and intrinsic GABAergic afferents onto projection neurons, whereas m2 receptors regulate acetylcholine release from axons of cholinergic interneurons.

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Section: Segregated Distribution Of Muscarinic M1 and M2 Receptorssupporting

confidence: 89%

Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto‐striatal pathways

Alcantara

Mrzljak

Jakab

et al. 2001

J of Comparative Neurology

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“…At later postnatal ages (P16 and P32), this pattern was no longer apparent, as the network of ACh axons was extremely dense throughout, even if a slight lateromedial gradient of density was still visible. A transient patchy distribution has been reported for other cholinergic markers in the developing neostriatum of several mammalian species, including rat (Graybiel, 1984;Nastuk and Graybiel, 1989). It could be related to other aspects of the cytoarchitectural compartmentation in immature neostriatum, and particularly to the early presence of dopamine and opiate receptor rich islands (Graybiel et al, 1981;Moon Edley and Herkenham, 1984;Nastuk and Graybiel, 1985).…”

Section: Discussionmentioning

confidence: 78%

Fine structural features of the acetylcholine innervation in the developing neostriatum of rat

Aznavour

Mechawar

Watkins

et al. 2003

J of Comparative Neurology

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The acetylcholine (ACh) innervation in the developing neostriatum of rat was examined by means of light and electron microscopic immunocytochemistry with a highly sensitive antibody against choline acetyltransferase (ChAT). ChAT-immunoreactive cell bodies and their emerging processes, located at birth in the lateral part of neostriatum, progressively pervaded the whole region, to give rise to an extremely dense axonal network. As visualized and measured in single thin sections, at postnatal (P) ages P8, P16, and P32, the intrinsic and relational features of ChAT-immunostained profiles of axon varicosities in the lateral and medial parts of neostriatum were similar to those previously described in the adult. At the three postnatal ages, the immunoreactive profiles were comparable in shape, size, and vesicular content, and displayed one or more mitochondria with increasing frequency (from 10% at P8 to 29% at P32). The proportion which showed a synaptic junction was low at the three ages (8-16%), indicating an average synaptic incidence of 22% for whole varicosities after stereological extrapolation. The observed junctions were relatively small, mostly symmetrical, and made with dendritic spines or branches. The frequency of synapses on spines versus branches increased with age, from 20% at P8 to almost 60% at P32. Thus, the relational features of the neostriatal ACh innervation were similar to adult as soon as it appeared, as previously observed to be the case in the developing cerebral cortex. The diffuse mode of transmission may therefore be characteristic of both ACh interneurons (neostriatum) and projection neurons (cerebral cortex) in the CNS, and could be determining their functional properties during development as well as at maturity.

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“…Striatal neurotransmitters and their receptors undergo remodeling during early postnatal periods to establish their final adult patterns. Ontogenetic changes in patch/matrix compartments are observed with monoamines, SP, enkephalin, and receptors for these transmitters as well as other neuropeptides and ACh (Liozou, 1972;Olson et al,, 1972;Tennyson et al, 1972;Graybiel et al, 1981;Quit-ion and Dam, 1986;Lowenstein et al, 1989;Nastuk and Graybiel, 1989;Tribollet et al, 1989). In addition, pre-and postnatal changes in glycoconjugated molecules, neu-distribution of opiate receptors in newborn monkeys (Bacheropeptides, glutamate, and dopamine suggest that these sub-valier et al, 1986).…”

Section: Possible Mechanisms Accounting For Chemoarchitectonic Changementioning

confidence: 99%

“…These structures are complex, chemically heterogeneous regions with integral compartments that differ in neurotransmitter composition and connections Ragsdale, 1978, 1983;Beckstead et al, 1979;Haber and Elde, 1982;Beach and McGeer, 1984;Crutcher and DeLong, 1984;Gerfen, 1984;Gerfen et al, 1985;Haber, 1986;Berendse et al, 1988;DeLong et al, 1988;Ragsdale and Graybiel, 1988;Hadfield et al, 1989;Langer and Graybiel, 1989). Moreover, the striatum and amygdala undergo changes in neurotransmitters and neurotransmitter receptors postnatally to achieve the adult pattern of organization (Liozou, 1972;Olson et al, 1972;Tennyson et al, 1972;Graybiel et al, 198 1;Bachevalier et al, 1986;Nastuk and Graybiel, 1989;Sirinathsinghji and Dunnett, 1989). We used immunocytochemistry to test the hypothesis that the formation of chemoarchitectonic patterns within the forebrain of adult nonhuman primates was influenced by early social deprivation.…”

mentioning

confidence: 99%

Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions

et al. 1991

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Rhesus monkeys (Macaca mulatta) reared during the first year of life without social contact develop persistent stereotyped movements, self-directed behaviors, and psychosocial abnormalities, but neurobiological mechanisms underlying the behaviors of socially deprived (SD) monkeys are unknown. Monkeys were reared in total social deprivation for the first 9 months of life; control monkeys were reared socially (SR) with mothers and peers. Subjects were killed at 19-24 yr of age. Because the behaviors of SD monkeys are reminiscent of changes in striatal or amygdalar function, we used immunocytochemistry for substance P (SP), leucine-enkephalin (LENK), somatostatin, calbindin, and tyrosine hydroxylase (TH) to evaluate qualitatively and quantitatively patterns of neurotransmitter marker immunoreactivity within subcortical regions. In SD monkeys, the chemoarchitecture of the striatum was altered. Neuronal cell bodies and processes immunoreactive for SP and LENK were depleted markedly in patch (striosome) and matrix regions of the caudate nucleus and putamen; the average density of SP-immunoreactive neurons was reduced 58% relative to SR monkeys. Calbindin and TH immunoreactivities were diminished in the matrix of caudate and putamen of SD monkeys. TH-immunoreactive neurons, but not cresyl violet-stained neurons, in the substantia nigra pars compacta were decreased (43%) in SD monkeys. Peptide-immunoreactive terminals were reduced in the globus pallidus and substantia nigra in SD monkeys. The nucleus accumbens was the least affected of striatal regions. Striatal somatostatin immunoreactivity wa qualitatively and quantitatively similar in SD and SR monkeys. Several regions, for example, bed nucleus of the stria terminalis, amygdala, and basal forebrain magnocellular complex, that were in the same sections and are enriched in these markers did not appear altered in SD monkeys, suggesting a regional specificity for vulnerability. The altered chemoarchitecture of some basal ganglia regions in adult monkeys that experienced social deprivation as infants suggests that the postnatal maturation of neurotransmitter phenotypes in some structures is influenced by social environment. Abnormal motor and psychosocial behaviors resulting from this form of social/sensory deprivation may result from alterations in peptidergic and dopaminergic systems within the basal ganglia.

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Ontogeny of M1 and M2 muscarinic binding sites in the striatum of the cat: Relationships to one another and to striatal compartmentalization

Cited by 16 publications

References 67 publications

Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto‐striatal pathways

Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto‐striatal pathways

Fine structural features of the acetylcholine innervation in the developing neostriatum of rat

Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions

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