Ultrastructure of normal and degenerating glomerular terminals of dorsal root axons in the substantia gelatinosa of the rhesus monkey

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Abstract

The fine structure of primary sensory terminals within glomerular complexes of lamina II of Rexed (substantia gelatinosa Rolandi) in the spinal cord was investigated in normal adult rhesus monkeys and in monkeys subjected to thoracic or lumbosacral dorsal root transection. Three types of 'scalloped' primary sensory terminals were distinguished on the basis of their ultrastructural characteristics, size, and distribution of synaptic vesicle population: (1) dense sinusoid axon (DSA) terminals contain medium-sized (42-46 nm and 58-62 nm) and large (80 nm) clear synaptic vesicles; (2) large dense-core vesicles (LDCV) terminals are equipped with empty synaptic vesicles ranging from 30 to 106 nm, large, (80 nm) and very large, (100 nm) dense-core vesicles; and (3) regular synaptic vesicles (RSV) terminals contain a homogeneous population of 45-50 nm clear synaptic vesicles. Following transection of the dorsal roots, all three types or primary afferents degenerate and become engulfed and phagocytosed by glial cells. However, each type of terminal displays a different mode and tempo of degeneration as seen in monkeys sacrificed 36, 48, and 72 hours following rhizotomy. DSAs follow the osmiophilic degeneration pattern; LDCVs are characterized by a gradual increase in the number of 'electron-dense bodies' and, less frequently, by a progressive osmiophilic process; RSVs exhibit signs of a filamentous degeneration, accompanied by clusters of synaptic vesicles. The three types of terminals are distributed in an overlapping but distinct pattern within the posterior horn. Thus DSAs are present in highest numbers in lamina II where they constitute the most frequent terminal type. LDCVs also occur in lamina II in its outer half but are most concentrated in lamina I. RSVs predominate in the deeper layers of the dorsal horn (lamina III) but are also found in the internal half of lamina II. On the basis of these ultrastructural data and a comparison with afferent profiles impregnated according to the Golgi method, it appears that DSAs and LDCVs correspond respectively to superficial and marginal collaterals of small, thin dorsal root fibers whereas RSVs represent terminals of deep collaterals from large, thick dorsal root axons.

Original languageEnglish
Pages (from-to)357-375
Number of pages19
JournalJournal of Comparative Neurology
Volume210
Issue number4
Publication statusPublished - 1982

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Substantia Gelatinosa
Spinal Nerve Roots
Synaptic Vesicles
Macaca mulatta
Axons
Presynaptic Terminals
Secretory Vesicles
Haplorhini
Rhizotomy
Horns
Phagocytosis
Neuroglia
Population
Spinal Cord
Thorax
Electrons

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Ultrastructure of normal and degenerating glomerular terminals of dorsal root axons in the substantia gelatinosa of the rhesus monkey",
abstract = "The fine structure of primary sensory terminals within glomerular complexes of lamina II of Rexed (substantia gelatinosa Rolandi) in the spinal cord was investigated in normal adult rhesus monkeys and in monkeys subjected to thoracic or lumbosacral dorsal root transection. Three types of 'scalloped' primary sensory terminals were distinguished on the basis of their ultrastructural characteristics, size, and distribution of synaptic vesicle population: (1) dense sinusoid axon (DSA) terminals contain medium-sized (42-46 nm and 58-62 nm) and large (80 nm) clear synaptic vesicles; (2) large dense-core vesicles (LDCV) terminals are equipped with empty synaptic vesicles ranging from 30 to 106 nm, large, (80 nm) and very large, (100 nm) dense-core vesicles; and (3) regular synaptic vesicles (RSV) terminals contain a homogeneous population of 45-50 nm clear synaptic vesicles. Following transection of the dorsal roots, all three types or primary afferents degenerate and become engulfed and phagocytosed by glial cells. However, each type of terminal displays a different mode and tempo of degeneration as seen in monkeys sacrificed 36, 48, and 72 hours following rhizotomy. DSAs follow the osmiophilic degeneration pattern; LDCVs are characterized by a gradual increase in the number of 'electron-dense bodies' and, less frequently, by a progressive osmiophilic process; RSVs exhibit signs of a filamentous degeneration, accompanied by clusters of synaptic vesicles. The three types of terminals are distributed in an overlapping but distinct pattern within the posterior horn. Thus DSAs are present in highest numbers in lamina II where they constitute the most frequent terminal type. LDCVs also occur in lamina II in its outer half but are most concentrated in lamina I. RSVs predominate in the deeper layers of the dorsal horn (lamina III) but are also found in the internal half of lamina II. On the basis of these ultrastructural data and a comparison with afferent profiles impregnated according to the Golgi method, it appears that DSAs and LDCVs correspond respectively to superficial and marginal collaterals of small, thin dorsal root fibers whereas RSVs represent terminals of deep collaterals from large, thick dorsal root axons.",
author = "E. Knyih{\'a}r-Csillik and B. Csillik and P. Rakic",
year = "1982",
language = "English",
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pages = "357--375",
journal = "Journal of Comparative Neurology",
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T1 - Ultrastructure of normal and degenerating glomerular terminals of dorsal root axons in the substantia gelatinosa of the rhesus monkey

AU - Knyihár-Csillik, E.

AU - Csillik, B.

AU - Rakic, P.

PY - 1982

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N2 - The fine structure of primary sensory terminals within glomerular complexes of lamina II of Rexed (substantia gelatinosa Rolandi) in the spinal cord was investigated in normal adult rhesus monkeys and in monkeys subjected to thoracic or lumbosacral dorsal root transection. Three types of 'scalloped' primary sensory terminals were distinguished on the basis of their ultrastructural characteristics, size, and distribution of synaptic vesicle population: (1) dense sinusoid axon (DSA) terminals contain medium-sized (42-46 nm and 58-62 nm) and large (80 nm) clear synaptic vesicles; (2) large dense-core vesicles (LDCV) terminals are equipped with empty synaptic vesicles ranging from 30 to 106 nm, large, (80 nm) and very large, (100 nm) dense-core vesicles; and (3) regular synaptic vesicles (RSV) terminals contain a homogeneous population of 45-50 nm clear synaptic vesicles. Following transection of the dorsal roots, all three types or primary afferents degenerate and become engulfed and phagocytosed by glial cells. However, each type of terminal displays a different mode and tempo of degeneration as seen in monkeys sacrificed 36, 48, and 72 hours following rhizotomy. DSAs follow the osmiophilic degeneration pattern; LDCVs are characterized by a gradual increase in the number of 'electron-dense bodies' and, less frequently, by a progressive osmiophilic process; RSVs exhibit signs of a filamentous degeneration, accompanied by clusters of synaptic vesicles. The three types of terminals are distributed in an overlapping but distinct pattern within the posterior horn. Thus DSAs are present in highest numbers in lamina II where they constitute the most frequent terminal type. LDCVs also occur in lamina II in its outer half but are most concentrated in lamina I. RSVs predominate in the deeper layers of the dorsal horn (lamina III) but are also found in the internal half of lamina II. On the basis of these ultrastructural data and a comparison with afferent profiles impregnated according to the Golgi method, it appears that DSAs and LDCVs correspond respectively to superficial and marginal collaterals of small, thin dorsal root fibers whereas RSVs represent terminals of deep collaterals from large, thick dorsal root axons.

AB - The fine structure of primary sensory terminals within glomerular complexes of lamina II of Rexed (substantia gelatinosa Rolandi) in the spinal cord was investigated in normal adult rhesus monkeys and in monkeys subjected to thoracic or lumbosacral dorsal root transection. Three types of 'scalloped' primary sensory terminals were distinguished on the basis of their ultrastructural characteristics, size, and distribution of synaptic vesicle population: (1) dense sinusoid axon (DSA) terminals contain medium-sized (42-46 nm and 58-62 nm) and large (80 nm) clear synaptic vesicles; (2) large dense-core vesicles (LDCV) terminals are equipped with empty synaptic vesicles ranging from 30 to 106 nm, large, (80 nm) and very large, (100 nm) dense-core vesicles; and (3) regular synaptic vesicles (RSV) terminals contain a homogeneous population of 45-50 nm clear synaptic vesicles. Following transection of the dorsal roots, all three types or primary afferents degenerate and become engulfed and phagocytosed by glial cells. However, each type of terminal displays a different mode and tempo of degeneration as seen in monkeys sacrificed 36, 48, and 72 hours following rhizotomy. DSAs follow the osmiophilic degeneration pattern; LDCVs are characterized by a gradual increase in the number of 'electron-dense bodies' and, less frequently, by a progressive osmiophilic process; RSVs exhibit signs of a filamentous degeneration, accompanied by clusters of synaptic vesicles. The three types of terminals are distributed in an overlapping but distinct pattern within the posterior horn. Thus DSAs are present in highest numbers in lamina II where they constitute the most frequent terminal type. LDCVs also occur in lamina II in its outer half but are most concentrated in lamina I. RSVs predominate in the deeper layers of the dorsal horn (lamina III) but are also found in the internal half of lamina II. On the basis of these ultrastructural data and a comparison with afferent profiles impregnated according to the Golgi method, it appears that DSAs and LDCVs correspond respectively to superficial and marginal collaterals of small, thin dorsal root fibers whereas RSVs represent terminals of deep collaterals from large, thick dorsal root axons.

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