Evidence of Synaptic Contacts of Nociceptive Primary Afferent Central Terminals on GABAergic Interneurons in the Substantia Gelatinosa.

Hiura, Akio; Nasu, Fumio; Ishizuka, Hiroshi; Kuwahara, Michiyo; Ohta, Mika

doi:10.1679/aohc.59.55

Cited by 11 publications

(9 citation statements)

References 21 publications

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“…But the band widens from the medial to lateral side as if corresponding to the intensity of GABAimmunoreactivity, the broad band in the lateral superficial dorsal horn (Hiura et aL, 1996).…”

Section: Discussionmentioning

confidence: 98%

FRAP-positive and Capsaicin-Sensitive Terminals in the Substantia Gelatinosa of the Mouse Spinal Trigeminal Nucleus Caudalis

Hiura

Nasu

Ishizuka

1999

Okajimas Folia Anatomica Japonica

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Summary: FRAP (fluoride-resistant acid phosphatase) -reactivity in the substantia gelatinosa of the mouse spinal trigeminal nucleus caudalis (STNC) was examined by light and electron microscopy. Degenerated figures of terminals caused by capsaicin were compared with the FRAP-positive terminals. Scalloped (fan-like) or indented, sinuous, slender, and cap-like figures with closely packed agranular synaptic vesicles of various sizes were common to both FRAPpositive and capsaicin-sensitive terminals. These terminals had glomerular or nonglomerular endings. Sometimes FRAP-positive and capsaicin-sensitive glomerular terminals made presynapses with surrounding dendrites. Frequently, both nonglomerular terminals were in direct contact with the neuronal soma. The terminal features of FRAP-positive and capsaicin-sensitive ones in the mouse STNC are the same as those seen in the superficial dorsal horn of the spinal cord. These findings suggest that some of the FRAP-positive terminals are capsaicin-sensitive, thereby indicating their nociceptive primary afferent.FRAP (fluoride-resistant acid phosphatase), a nonlysozomal enzyme, is localized to small dorsal root ganglion (DRG) neurons. After dorsal root ligation (Knyihar, 1971), dorsal rhizotomy, blocking the axonal flow by microtubule polymerizing agents such as colchicin and vinblastine (Knyihar-Csillik and Csillik, 1981) and capsaicin treatment (Nagy et aL, 1981), FRAP reactivity disappeared in lamina II of the spinal dorsal horn and small DRG neurons. Accordingly, FRAP is believed to be synthesized in small primary afferent neurons and conveyed to the central (Knyihar, 1971) and peripheral (Devor and Claman, 1980) terminals by axonal flow. Thirty to 50% of the DRG cells projecting to the splanchnic or intercostal nerve are FRAPpositive (Dalsgaard et al., 1984). Moreover, numerous unmyelinated axons innervating the corneal epithelium exhibit acid phosphtase activity (Knyihar-Csillik and Csillik, 1981). Therefore, FRAP has been currently used for identification of the primary afferent neurons. The fine structures of FRAP-positive central endings of the primary afferent were extensively documented by KnyiharCsillik and Csillik (1981). The FRAP-positive terminals in the rat substantia gelatinosa of the spinal dorsal horn and caudal spinal trigeminal nucleus are dark sinusoid axons (DSA) or scalloped (fanlike) terminals with packed regular (clear) synaptic vesicles and few or numerous large dense core vesicles. Ribeiro-da-Silva et al. also examined FRAP-positive terminals in the substantia gelatinosa of the rat spinal dorsal horn (1986) and spinal trigeminal nucleus caudalis (1989). They showed that FRAP-positive terminals have electron-dense sinuous or scalloped contours with closely packed regular synaptic vesicles, few large dense core vesicles and mitochondria. Fine structures of the FRAP-positive terminals are the same as the central terminals (CI type), described by Ribeiro-daSilva and Coimbra in 1982, situated centrally forming synaptic glomeruli which are capsaicin...

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Section: Discussionmentioning

confidence: 98%

FRAP-positive and Capsaicin-Sensitive Terminals in the Substantia Gelatinosa of the Mouse Spinal Trigeminal Nucleus Caudalis

Hiura

Nasu

Ishizuka

1999

Okajimas Folia Anatomica Japonica

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“…The close topographical relationship observed between the small dorsal GABA-ir cells and the Retzius bipolar cells of amphioxus also suggests that GABA-ir cells may modulate (or be modulated by) the somatosensory system. GABA-ir neurons associated with the sensory tracts are numerous in mammals (McLaughlin et al, 1975;Barber et al, 1982;Magoul et al, 1987), and primary afferents contact GABA-ir interneurons of the dorsal horn (Hiura et al, 1996). The large multipolar GABA-ir cells of lampreys occupy more ventrolateral positions and appear related to the dorsolateral and ventrolateral neuropil.…”

Section: Spinal Cordmentioning

confidence: 99%

Distribution of GABA immunoreactivity in the central and peripheral nervous system of amphioxus (Branchiostoma lanceolatum pallas)

1998

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On the basis of labeling with an anti-gamma-aminobutyric acid (GABA) antibody, we report for the first time the presence and distribution of GABA-immunoreactive cells in the central and peripheral nervous system of amphioxus. In the nerve cord, there is a large dorsorostral group of cerebrospinal-fluid-contacting (CSFc) cells at the caudal end of the brain vesicle that gives rise to a large ventral commissure and neuropilar region. In the middle and caudal region of the brain, numerous commissural and CSFc neurons are situated below the region of large dorsal cells. In the spinal cord, several types of GABA-immunoreactive neurons of different size, appearance, and distribution were observed. In the dorsalmost region, very small commissural cells are scattered regularly along the cord. More ventrally in the cord, GABAergic neurons, both of commissural and CSFc cell types, form segmental groups, but scattered cells are observed throughout. These cells give rise to dense longitudinal fascicles of GABAergic fibers and to scattered commissural fibers. The caudal ampulla lacks GABAergic cells and fibers. Some of the fibers of the most rostral and caudal peripheral (sensory) nerves, as well as some sensory cells of the rostral and caudal epidermis, are GABA immunoreactive. The significance of these results for the understanding of the evolution of GABAergic systems of vertebrates is discussed.

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“…We also reported the presynaptic relationships of central endings of the nociceptive primary afferents to GABAergic dendrites (Hiura et aL, 1991;Hiura et al, 1996a) and interneuronal soma (Hiura and Ishizuka, 1995) in the mouse superficial dorsal horn. In contrast, Todd and Lochhead (1990) reported GABA-IR presynaptic dendrites to CI terminals in lamina II of the rat dorsal horn.…”

Section: Discussionmentioning

confidence: 98%

Relationship of Substance P-and CGRP-immunoreactive Central Endings of the Primary Afferent Neurons to GABAergic Interneurons in the Guinea Pig Substantia Gelatinosa

Hiura

Nasu

Ishizuka

1998

Okajimas Folia Anatomica Japonica

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Summary: The synaptic relationships between primary afferent central endings containing substance P (SP) and calcitonin gene-related peptide (CGRP) and GABAergic internenrons in the guinea pig substantia gelatinosa of the lumbar spinal dorsal horn were studied. The pre-embedding PAP method was used for detection of GABA and the post-embedding double immunogold labeling method for SP and CGRP detection. Immunogold particles specific for SP and CGRP were mainly localized separately or together in large synaptic vesicles devoid of dense cores. SP and CGRP immunoreactivity was separate or co-localized in small roundish, slender, sinuous or large scalloped (fan-like) terminals with closely packed round agranular synaptic vesides of various sizes and few large dense core vesides and mitochondria, which are thought to be capsaicin-sensitive primary afferent terminals. These SP-and CGRP-immunoreactive boutons make presynaptic or symmetric contacts with GABAergic dendrites and soma. These findings suggest that the central endings of nodceptive primary afferents transmit pain stimuli to intrinsic inhibitory internenrons, thereby modulating nodceptive information via a postsynaptic circuit.

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Evidence of Synaptic Contacts of Nociceptive Primary Afferent Central Terminals on GABAergic Interneurons in the Substantia Gelatinosa.

Cited by 11 publications

References 21 publications

FRAP-positive and Capsaicin-Sensitive Terminals in the Substantia Gelatinosa of the Mouse Spinal Trigeminal Nucleus Caudalis

FRAP-positive and Capsaicin-Sensitive Terminals in the Substantia Gelatinosa of the Mouse Spinal Trigeminal Nucleus Caudalis

Distribution of GABA immunoreactivity in the central and peripheral nervous system of amphioxus (Branchiostoma lanceolatum pallas)

Relationship of Substance P-and CGRP-immunoreactive Central Endings of the Primary Afferent Neurons to GABAergic Interneurons in the Guinea Pig Substantia Gelatinosa

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