A Golgi study of neuronal types in the neostriatum of monkeys

DiFiglia, Marian; Pasik, Pedro; Pasik, Tauba

doi:10.1016/0006-8993(76)90669-7

Cited by 334 publications

(131 citation statements)

References 5 publications

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“…For 80 years the status of the giant interneurons was disputed, most famously by Ramon y Cajal (1911), who incorrectly identified the striatal spiny neuron as an interneuron and the giant cell as a projection neuron. The current view emerged from a combination of very careful examination of axons using the Golgi method (Leontovich, 1954;DiFiglia et al, 1976) and retrograde labeling (Grofová, 1979). Golgi staining and intracellular labeling with immunocytochemistry for choline acetyltransferase established that the giant interneurons of Kölliker are the cholinergic cells (Bolam et al, 1984;Kawaguchi, 1993).…”

Section: Cholinergic Interneurons In the Striatummentioning

confidence: 99%

Cholinergic interneuron characteristics and nicotinic properties in the striatum

2002

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ABSTRACT:The neostriatum (dorsal striatum) is composed of the caudate and putamen. The ventral striatum is the ventral conjunction of the caudate and putamen that merges into and includes the nucleus accumbens and striatal portions of the olfactory tubercle. About 2% of the striatal neurons are cholinergic. Most cholinergic neurons in the central nervous system make diffuse projections that sparsely innervate relatively broad areas. In the striatum, however, the cholinergic neurons are interneurons that provide very dense local innervation. The cholinergic interneurons provide an ongoing acetylcholine (ACh) signal by firing action potentials tonically at about 5 Hz. A high concentration of acetylcholinesterase in the striatum rapidly terminates the ACh signal, and thereby minimizes desensitization of nicotinic acetylcholine receptors. Among the many muscarinic and nicotinic striatal mechanisms, the ongoing nicotinic activity potently enhances dopamine release. This process is among those in the striatum that link the two extensive and dense local arbors of the cholinergic interneurons and dopaminergic afferent fibers. During a conditioned motor task, cholinergic interneurons respond with a pause in their tonic firing. It is reasonable to hypothesize that this pause in the cholinergic activity alters action potential dependent dopamine release. The correlated response of these two broad and dense neurotransmitter systems helps to coordinate the output of the striatum, and is likely to be an important process in sensorimotor planning and learning.

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Section: Cholinergic Interneurons In the Striatummentioning

confidence: 99%

Cholinergic interneuron characteristics and nicotinic properties in the striatum

2002

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“…Occasional autapses on neurons have been reported in anatomical studies from various brain regions (Held, 1897;Chan-Palay, 1971;Scheibel and Scheibel, 1971;Shkol'nik-Yarros, 1971; Van der Loos and Glaser, 1972;DiFiglia et al, 1976;Karabelas and Purpura, 1980;Peters and Proskauer, 1980;Preston et al, 1980;Kuffler et al, 1987;Shi and Rayport, 1994;Lübke et al, 1996), but in view of our difficulty predicting the existence of autapses on the basis of light microscopy, some of the previous predictions will require reexamination, including EM or physiology. To our knowledge, electron microscopic studies have so far verified one autapse on a smooth dendritic stellate cell (Peters and Proskauer, 1980), six autapses on layer V pyramidal cells (Lübke et al, 1996), one autaptic junction on a fast-spiking interneuron (Thomson et al, 1996), and five autapses on a hippocampal basket cell (Cobb et al, 1997).…”

Section: Autapses In the Cnsmentioning

confidence: 99%

“…In addition to their original Golgi study in rabbit neocortex predicting the existence of autapses, possible autaptic contacts have been described in dog (Shkol'nik-Yarros, 1971) and rat (Peters and Proskauer, 1980;Preston et al, 1980) cerebral cortex, monkey neostriatum (DiFiglia et al, 1976), and cat spinal cord (Scheibel and Scheibel, 1971). Using intracellular markers, several groups also detected apparent self-innervating connections from various brain regions, such as substantia nigra (Karabelas and Purpura, 1980) and striatum (Park et al, 1980;Preston et al, 1980), but the above studies were based on light microscopic observations.…”

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confidence: 99%

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

1997

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Autapses are transmitter release sites made by the axon of a neuron on its own dendrites. We determined the numbers and precise subcellular position of autapses on different spiny and smooth dendritic cell types using intracellular biocytin filling in slices of adult neocortex.Potential self-innervation was light microscopically assessed on 10 pyramidal cells, 7 spiny stellate cells, and 41 smooth dendritic neurons from cortical layers II-V. Putative autapses occurred on each smooth dendritic neuron and on seven pyramids, but not on spiny stellate cells. However, electron microscopic examination of all light microscopically predicted sites on pyramids (n ϭ 28) showed only one case of self-innervation with two autapses on dendritic spines. Interneurons were classified by postsynaptic target distribution (Tamá s et al., 1997) and all putative autapses of seven basket, three dendrite-targeting, and three double bouquet cells were scrutinized. All basket and dendrite-targeting cells established self-innervation, the number of autapses being 12 Ϯ 7 and 22 Ϯ 12 (mean Ϯ SD), respectively; only one of the double bouquet cells formed autapses (n ϭ 3). Basket cell autapses (n ϭ 74) were closer to the soma (12.2 Ϯ 22.3 m) than autapses established by dendrite-targeting cells (51.8 Ϯ 49.9 m; n ϭ 66).The degree of self-innervation is cell type-specific. Unlike on spiny cells, autapses are abundant on GABAergic basket and dendrite-targeting interneurons, with subcellular location similar to that of synapses formed by the parent cell on other neurons. The extensive self-innervation may modulate integrative properties and/or the firing rhythm of the neuron in a manner temporally correlated with its own activity.

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“…It is the target of inputs from the entire cortex and certain thalamic nuclei (parafascicular and centromedian nucleus) and provides output to other nuclei of the basal ganglia. The striatum is composed primarily of spiny projection neurons (DiFiglia et al, 1976;Bishop et al, 1982;Gerfen and Wilson, 1996), which constitute ϳ95% of the striatal neuronal population (Kemp and Powell, 1971). These projection neurons are also the major target of afferents to the striatum.…”

Section: Abstract: Striatum; Dopaminergic Cells; Parkinson's Diseasementioning

confidence: 99%

Dopaminergic Neurons Intrinsic to the Primate Striatum

Betarbet¹,

Turner²,

Chockkan³

et al. 1997

J. Neurosci.

241

198

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Intrinsic, striatal tyrosine hydroxylase-immunoreactive (TH-i) cells have received little consideration. In this study we have characterized these neurons and their regulatory response to nigrostriatal dopaminergic deafferentation. TH-i cells were observed in the striatum of both control and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated monkeys; TH-i cell counts, however, were 3.5-fold higher in the striatum of MPTPlesioned monkeys. To establish the dopaminergic nature of the TH-i cells, sections were double-labeled with antibodies to dopamine transporter (DAT). Immunofluorescence studies demonstrated that nearly all TH-i cells were double-labeled with DAT, suggesting that they contain the machinery to be functional dopaminergic neurons. Two types of TH-i cells were identified in the striatum: small, aspiny, bipolar cells with varicose dendrites and larger spiny, multipolar cells. The aspiny cells, which were more prevalent, corresponded morphologically to the GABAergic interneurons of the striatum. Doublelabel immunofluorescence studies using antibodies to TH and glutamate decarboxylase (GAD 67 ), the synthetic enzyme for GABA, showed that 99% of the TH-i cells were GAD 67 -positive. Very few (Ͻ1%) of the TH-i cells, however, were immunoreactive for the calcium-binding proteins calbindin and parvalbumin. In summary, these results demonstrate that the dopaminergic cell population of the striatum responds to dopamine denervation by increasing in number, apparently to compensate for loss of extrinsic dopaminergic innervation. Moreover, this population of cells corresponds largely with the intrinsic GABAergic cells of the striatum. This study also suggests that the adult primate striatum does retain some intrinsic capacity to compensate for dopaminergic cell loss.

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A Golgi study of neuronal types in the neostriatum of monkeys

Cited by 334 publications

References 5 publications

Cholinergic interneuron characteristics and nicotinic properties in the striatum

Cholinergic interneuron characteristics and nicotinic properties in the striatum

Massive Autaptic Self-Innervation of GABAergic Neurons in Cat Visual Cortex

Dopaminergic Neurons Intrinsic to the Primate Striatum

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