Tatsumi Kusakabe

Kokushikan University, Japan

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Publications (88)201.89 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: Dopamine modulates the chemosensitivity of arterial chemoreceptors, and dopamine D2 receptor (D2R) is expected to localize in the glomus cells and/or sensory nerve endings of the carotid body. In the present study, the localization of D2R in the rat carotid body was examined using double immunofluorescence for D2R with various cell markers. D2R immunoreactivity was mainly localized in glomus cells immunoreactive to tyrosine hydroxylase or dopamine β-hydroxylase (DBH), but not in S100B-immunoreactive sustentacular cells. Furthermore, D2R immunoreactivity was observed in petrosal ganglion cells and nerve bundles in the carotid body, but not in the nerve endings with P2X2 immunoreactivity. In the carotid ganglion, a few punctate D2R-immunoreactive products were detected in DBH-immunoreactive nerve cell bodies. These results showed that D2R was mainly distributed in glomus cells, and suggested that D2R plays a role in the inhibitory modulation of chemosensory activity in a paracrine and/or autocrine manner. Copyright © 2015 Elsevier GmbH. All rights reserved.
    Acta histochemica 08/2015; DOI:10.1016/j.acthis.2015.07.007 · 1.71 Impact Factor
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    ABSTRACT: In the present study, we examined serotonin (5-HT)-induced intracellular Ca(2+) ([Ca(2+)]i) responses to hypoxia in glomus cells isolated from carotid body (CB) of the rat. 5-HT did not induce any [Ca(2+)]i responses in clustered glomus cells during normoxia (21% O2), whereas the perfusion of hypoxic solution (1% O2) induced repetitive increases in [Ca(2+)]i in the same specimens. The frequency and magnitude of hypoxia-induced [Ca(2+)]i changes observed in the glomus cells were enhanced in the presence of 5-HT, and this response was inhibited by the 5-HT2 receptor antagonist, ketanserin. Furthermore, RT-PCR analysis detected the expression of 5-HT1A, 5-HT1B, 5-HT1D, 5-HT1F, 5-HT2A, 5-HT2B, 5-HT3A, and 5-HT3B receptor mRNAs in extracts of the CB. These results suggest that 5-HT increases hypoxia-induced [Ca(2+)]i responses in glomus cells. 5-HT may elevate hypoxic responses in glomus cells in order to increase chemosensory activity of the CB. Copyright © 2015. Published by Elsevier Ireland Ltd.
    Neuroscience Letters 04/2015; 597. DOI:10.1016/j.neulet.2015.04.044 · 2.03 Impact Factor
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    ABSTRACT: Hypoxia-induced chemosensory activity in the carotid body (CB) may be enhanced by the sympathetic regulation of vascular tone in the CB. In the present study, we recorded cervical sympathetic nerve activity in rats exposed to hypoxia, and examined noradrenaline (NA)- and serotonin (5-HT)-induced intracellular Ca2+ ([Ca2+]i) responses in smooth muscle cells and pericytes in isolated blood vessels from the CB. Multifiber electrical activity recorded from the cervical sympathetic trunk was increased during the inhalation of hypoxic gas. NA induced [Ca2+]i increases in smooth muscle cells in arteriole specimens, whereas 5-HT did not cause any [Ca2+]i responses. However, NA did not induce [Ca2+]i increases in pericytes in capillaries, whereas 5-HT did and this response was inhibited by the 5-HT2 receptor antagonist, ketanserin. In conclusion, cervical sympathetic nerves enhanced by hypoxia may reduce blood flow in the CB in order to increase chemosensitivity. Thus, hypoxic chemosensitivity in the CB may involve a positive feedback mechanism via sympathetic nerves.
    Brain Research 11/2014; 1596. DOI:10.1016/j.brainres.2014.11.037 · 2.84 Impact Factor
  • Fumiya Takaki · Nobuaki Nakamuta · Tatsumi Kusakabe · Yoshio Yamamoto
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    ABSTRACT: The sympathetic ganglion contains small intensely fluorescent (SIF) cells derived from the neural crest. We morphologically characterize SIF cells and focus on their relationship with ganglionic cells, preganglionic nerve fibers and sensory nerve endings. SIF cells stained intensely for tyrosine hydroxylase (TH), with a few cells also being immunoreactive for dopamine β-hydroxylase (DBH). Vesicular acetylcholine transporter (VAChT)-immunoreactive puncta were distributed around some clusters of SIF cells, whereas some SIF cells closely abutted DBH-immunoreactive ganglionic cells. SIF cells contained bassoon-immunoreactive products beneath the cell membrane at the attachments and on opposite sites to the ganglionic cells. Ganglion neurons and SIF cells were immunoreactive to dopamine D2 receptors. Immunohistochemistry for P2X3 revealed ramified nerve endings with P2X3 immunoreactivity around SIF cells. Triple-labeling for P2X3, TH and VAChT allowed the classification of SIF cells into three types based on their innervation: (1) with only VAChT-immunoreactive puncta, (2) with only P2X3-immunoreactive nerve endings, (3) with both P2X3-immunoreactive nerve endings and VAChT-immunoreactive puncta. The results of retrograde tracing with fast blue dye indicated that most of these nerve endings originated from the petrosal ganglion. Thus, SIF cells in the superior cervical ganglion are innervated by preganglionic fibers and glossopharyngeal sensory nerve endings and can be classified into three types. SIF cells might modulate sympathetic activity in the superior cervical ganglion.
    Cell and Tissue Research 11/2014; 359(2). DOI:10.1007/s00441-014-2051-1 · 3.57 Impact Factor
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    ABSTRACT: The carotid body is a peripheral chemoreceptor that detects decreases in arterial pO2 and subsequently activates the carotid sinus nerve. The hypoxia-evoked activity of the carotid sinus nerve has been suggested to be modulated by glutamate. In the present study, we investigate the immunohistochemical localization of vesicular glutamate transporters in the carotid body of the rat. Vesicular glutamate transporter 2 (VGLUT2) labeling was closely associated with glomus cells immunoreactive to tyrosine hydroxylase but was not in the cytoplasm of these cells. The VGLUT2 immunoreactivity was observed within nerve endings that were immunoreactive to P2X3 and densely localized inside P2X3-immunoreactive axon terminals. These results suggest that VGLUT2 is localized in the afferent nerve terminals of the carotid body. Glutamate may be released from afferent nerve terminals to modulate the chemosensory activity of the carotid body.
    Cell and Tissue Research 06/2014; 358(1). DOI:10.1007/s00441-014-1921-x · 3.57 Impact Factor
  • Kouki Kato · Jun Wakai · Hideki Matsuda · Tatsumi Kusakabe · Yoshio Yamamoto
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    ABSTRACT: Under hypertension, it has been reported that the carotid body (CB) is enlarged and noradrenaline (NA) content in CB is increased. Therefore, it is hypothesized that morphological and neurochemical changes in CB are induced in hypertensive animal models. In the present study, we examined the morphological features and dopamine β-hydroxylase (DBH) immunoreactivity in CB of spontaneously hypertensive rats (SHR/Izm) and Wistar Kyoto rats (WKY/Izm). The CB of SHR/Izm was elongated in terms of the cross section of center and was enlarged in the reconstructed images compared with that of WKY/Izm, and the total volume of CB in SHR/Izm (0.048 ± 0.004 mm³) was significantly (p<0.05) increased compared with the value in WKY/Izm (0.032 ± 0.006 mm³). By immunohistochemistry, immunoreactivity for tyrosine hydroxylase in CB was mainly observed in glomus cells and the immunostaining properties were similar between WKY/Izm and SHR/Izm. On the other hand, DBH immunoreactivity was mainly observed in nerve fibers around blood vessels and observed in a few glomus cells in CB of WKY/Izm. The number of glomus cells with strong DBH immunoreactivity was increased in SHR/Izm compared with that in WKY/Izm. In conclusion, the present study exhibited the enlargement of CB as three-dimensional image and revealed the enhanced immunoreactivity for DBH of glomus cells in SHR/Izm. These results suggest that the morphology of CB is affected by the effect of sympathetic nerve and that the signal transduction from CB is regulated by NA in glomus cells under hypertensive conditions.
    Autonomic neuroscience: basic & clinical 04/2012; 169(1):49-55. DOI:10.1016/j.autneu.2012.03.005 · 1.56 Impact Factor
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    ABSTRACT: We examined morphological characteristics of the carotid body of spontaneously hypertensive rats (SHR), those of age-matched normotensive Wistar rats (NWR), and age-matched genetically comparable Wistar Kyoto rats (WKY). We examined the distribution and abundance of four different regulatory neuropeptides: substance P (SP), calcitonin gene-related peptide (CGRP), vasoactive intestinal polypeptide (VIP), and neuropeptide Y (NPY) in the carotid bodies of these three strains of rats. The carotid bodies of SHR were larger than those of NWR and WKY. The values of the long axis of the carotid bodies of SHR were significantly larger (1.3 times) than those of NWR and WKY. In the carotid bodies of SHR, the percentage of relatively large vessels was similar to that of the carotid bodies of WKY, although the carotid bodies themselves were significantly larger than in WKY. The density of VIP varicose fibers in the carotid bodies of SHR was lower than in the carotid bodies of WKY, although the density of SP, CGRP and NPY fibers was similar to that of the carotid bodies of NWR and WKY. These findings suggested that VIP was unrelated to enlargement of the carotid body of SHR, but it might modify the sensitivity of chemoreceptors in the carotid body.
    Histology and histopathology 03/2011; 26(3):369-75. · 2.10 Impact Factor
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    T Yoshida · H Matsuda · Y Yamamoto · Y Hayashida · M Tsukuda · T Kusakabe
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    ABSTRACT: The distribution and abundance of the calcium binding protein, calbindin D-28k (CB) immunoreactivity in the taste buds of the circumvallate papillae and larynx were compared between normoxic and chronically hypoxic rats (10% O2 for 8 weeks). In the normoxic rats, CB immunoreactivity was observed in some cells and fibers of the intragemmal region of the taste buds in the circumvallate papillae. In contrast, in the subgemmal region of the laryngeal taste buds, fibers but not cells were immunoreactive for CB. In chronically hypoxic rats, CB immunoreactive cells and fibers in the taste buds were decreased in the circumvallate papillae. In the laryngeal taste buds, the density of the subgemmal CB immunoreactive fibers in chronically hypoxic rats was greater than in normoxic rats. It is considered that function of the laryngeal taste buds is different from that of the lingual taste buds, so that laryngeal taste buds may be involved in chemosensation other than taste. The altered density of CB immunoreactive cells and fibers in the lingual and laryngeal taste buds is a predominant feature of hypoxic adaptation, and chronic hypoxic exposure might change the chemical sensitivity of the circumvallate papillae and larynx through the regulation of intracellular Ca2+.
    Histology and histopathology 01/2007; 21(12):1271-6. · 2.10 Impact Factor
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    ABSTRACT: The majority of research for the calcitonin gene-related peptide (CGRP) in the stomach has been devoted to the submucosal blood flow, and only slight attention has been paid to its involvement in the gastric epithelial function. In this study, we examined the age-related change in the CGRP-containing nerves and its effects on the mucus metabolism. We compared the immunoreactivity for CGRP in the gastric mucosa of 7-week-old rats (young) to that of 52-week-old animals (middle-aged). The effects of CGRP on the mucin biosynthesis were compared using the stomachs from both young and middle-aged rats. The nitric oxide synthase (NOS) activity was measured in the surface and deep mucosa of the gastric corpus. The density of the CGRP nerve fibers was reduced in both the lamina propria and submucosa of the middle-aged rats compared to the young rats. CGRP stimulated the mucin biosynthesis in the cultured corpus mucosa from the 7-week-old rats, but not from the 52-week-old rats. The total NOS activity of the surface layer in the corpus mucosa was markedly reduced in the middle-aged rats compared to the young rats. These findings demonstrate the age-dependent reduction in the CGRP-induced mucin biosynthesis, as well as in the density of the CGRP fibers in the rat stomach. The decreased NOS activity in the surface layer of the oxyntic mucosa in the aged rats may also be a principal cause for the lack of regulation of the mucin biosynthesis by CGRP.
    Biomedical Research 07/2006; 27(3):117-24. DOI:10.2220/biomedres.27.117 · 1.14 Impact Factor
  • Advances in Experimental Medicine and Biology 02/2006; 580:55-61; discussion 351-9. DOI:10.1007/0-387-31311-7_9 · 1.96 Impact Factor
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    ABSTRACT: The carotid bodies are enlarged in the rats exposed to long term hypoxia. In some studies the animals were exposed to hypoxia for relatively short periods, and in other studies for relatively long periods. However, most authors use the term “chronic hypoxia” in their publications. This terminology can cause much confusion. On the other hand, there are no morphological studies of the carotid bodies after the termination of chronic hypoxia except in a few instances (Heath et al., 1973). Recently high altitude training has been used to try to improve some physical conditions. High altitude exercise can help to make clear morphological changes in chemoreceptor organs during acclimatization to hypoxia and during deacclimatization after chronic hypoxia is terminated.
    Advances in Experimental Medicine and Biology 02/2006; 580:49-54; discussion 351-9. DOI:10.1007/0-387-31311-7_8 · 1.96 Impact Factor
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    ABSTRACT: Changes in brain vascularity in adult rats during adaptation to chronic normobaric hypoxia with or without elevated CO(2) were morphometrically investigated. Immunohistochemistry with anti-rat endothelial cell antigen (RECA-1) antibody was carried out for the vascular analysis. After the rats were subjected to hypoxia for 2 to 8 weeks (wks)(10 percent O(2) in N(2)), the total area of blood vessels was measured in 6 brain regions. After 2 wks of hypoxia, the blood vessel area was found to be significantly increased in the frontal cortex, striatum, hippocampus, thalamus, cerebellum, and medulla oblongata, by 44% , 96% , 65% , 50% , 102% and 97% , respectively. The ratio of large vessels with an area > 500 micro m(2) was also increased in all brain regions. Hypoxic adaptation in brain vascularity did not change during 8 wks of hypoxia, and the hypoxia-induced levels measured in the vasculature returned to control levels 2 wks after the termination of hypoxia in areas of the brain other than the cortex and thalamus. In addition, hypoxia-induced changes in terms of the total vascular area and vessel size distribution were significantly inhibited by the elevation in CO(2), whereas chronic hypercapnia without hypoxia had no effect on brain vascularity. These findings suggested that adaptations in brain vascularity in response to hypoxia are rapidly induced, and there are regional differences in the reversibility of such vascular changes. Carbon dioxide is a potent suppressor of hypoxia-induced vascular changes, and may play an important role in vascular remodeling during the process of adaptation to chronic hypoxia.
    Acta medica Okayama 09/2005; 59(4):135-43. · 0.70 Impact Factor
  • T Kusakabe · H Matsuda · Y Hayashida
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    ABSTRACT: Three types of hypoxia with different levels of carbon dioxide (hypocapnic, isocapnic, and hypercapnic hypoxia) have been called systemic hypoxia. The systemic hypoxic carotid bodies were enlarged several fold, but the degree of enlargement was different for each. The mean short and long axes of hypocapnic and isocapnic hypoxic carotid bodies were 1.6 (short axis) and 1.8-1.9 (long axis) times larger than normoxic control carotid bodies, respectively. Those of hypercapnic hypoxic carotid bodies were 1.2 (short axis) and 1.5 (long axis) times larger than controls, respectively. The rate of enlargement in hypercapnic hypoxic carotid bodies was lower than in hypocapnic and isocapnic hypoxic carotid bodies. The rate of vascular enlargement in hypercapnic hypoxic carotid bodies was also smaller than in hypocapnic and isocapnic hypoxic carotid bodies. Thus, the enlargement of hypoxic carotid bodies is mainly due to vascular dilation. Different levels of arterial CO2 tension change the peptidergic innervation during chronically hypoxic exposure. The characteristic vascular arrangement was under the control of altered peptidergic innervation. During the course of hypoxic adaptation, the enlargement of the carotid bodies with vascular expansion began soon after the start of hypoxic exposure. During the course of recovery, the shrinking of the carotid bodies with vascular contraction also started at a relatively early period after the termination of chronic hypoxia. These processes during the course of hypoxic adaptation and during the course of recovery were under the control of peptidergic innervation. These findings may provide a standard for further studies of hypoxic carotid bodies.
    Histology and histopathology 08/2005; 20(3):987-97. · 2.10 Impact Factor
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    ABSTRACT: The role of the autonomic nervous system, the central and peripheral chemoreceptors, and the arterial baroreceptors was examined in the cardiovascular response to hypercapnia in conscious rats chronically instrumented for the measurement of arterial blood pressure (ABP), heart rate (HR), and renal sympathetic nerve activity (RSNA). Rats were exposed to hypercapnia (6% CO2), and the cardiovascular and autonomic nervous responses in intact and carotid chemo- and/or aortic denervated rats were compared. In intact and carotid chemo-denervated rats, hypercapnia induced significant increases in mean ABP (MABP) and RSNA, and a significant decrease in HR. The HR decrease was reversed by atropine and eliminated by bilateral aortic denervation, which procedure, however, did not affect the MABP or RSNA response. Bilateral carotid chemo-denervation did not affect the baroreflex control of HR, although this control was attenuated by aortic denervation. Hypercapnia did not affect baroreflex sensitivity in intact rats. These results suggest that hypercapnia induces an increase in MABP due to an activation of sympathetic nervous system via central chemoreceptors and a decrease in HR due to a secondary reflex activation of the parasympathetic nervous system via arterial baroreceptors in response to the rise in ABP. In addition, carotid chemoreceptors do not play a major role in the overall cardiovascular response to hypercapnia in conscious rats. The mechanism responsible for the parasympatho-excitation may also involve CO2 induced aortic chemoreceptor simulation.
    Autonomic Neuroscience 03/2005; 117(2):105-14. DOI:10.1016/j.autneu.2004.11.009 · 1.56 Impact Factor
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    ABSTRACT: Morphological changes in the rat carotid bodies 1, 2, 4, and 8 weeks after the termination of chronically hypocapnic hypoxia (10% O2 for 8 weeks) were examined by means of morphometry and immunohistochemistry. The rat carotid bodies after 8 weeks of hypoxic exposure were enlarged several fold with vascular expansion. The carotid bodies 1 and 2 weeks after the termination of 8 weeks of hypoxic exposure were diminished in size, although their diameter remained larger than the normoxic controls. The expanded vasculature in chronically hypoxic carotid bodies returned to the normoxic control state. In the carotid bodies 1 week after the termination of chronic hypoxia, the density of NPY fibers was remarkably increased and that of VIP fibers was dramatically decreased in comparison with the density in chronically hypoxic carotid bodies. In the carotid bodies 2 and 4 weeks after the termination of hypoxia, the density of SP and CGRP fibers was gradually increased. In the carotid bodies 8 weeks after the termination of hypoxia, the appearance of the carotid body returned to a nearly normoxic state, and the density of SP, CGRP, VIP, and NPY fibers also recovered to that of normoxic controls. These results suggest that the morphological changes in the recovering carotid bodies start at a relatively early period after the termination of chronic hypoxia, and a part of these processes may be under the control of peptidergic innervation.
    Histology and histopathology 11/2004; 19(4):1133-40. · 2.10 Impact Factor
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    ABSTRACT: The distribution and abundance of neuropeptide-containing nerve fibers were examined in the carotid bodies of rats exposed to hypocapnic hypoxia (10% O2 in N2) for 2, 4, and 8 weeks. The carotid bodies after 2, 4, and 8 weeks of hypoxic exposure were enlarged by 1.2-1.5 times in the short axis, and 1.3-1.7 times in the long axis in comparison with the normoxic control ones. The enlarged carotid bodies contained a number of expanded blood vessels. Mean density per unit area (10(4) microm2) of substance P (SP) and calcitonin gene-related peptide (CGRP) immunoreactive fibers was transiently high in the carotid bodies after 4 weeks of hypoxic exposure, and decreased significantly to nearly or under 50% after 8 weeks of hypoxic exposure. Density of vasoactive intestinal polypeptide (VIP) immunoreactive fibers increased significantly in all periods of hypoxic exposure observed, and was especially high in the carotid bodies after 4 weeks of hypoxic exposure. Density of neuropeptide Y immunoreactive fibers was unchanged in the carotid bodies during hypoxic exposure. These characteristic changes in the density of SP, CGRP, and VIP fibers in the carotid bodies after 4 weeks of hypoxic exposure suggest that the role of these neuropeptide-containing fibers may be different in the carotid bodies after each of three periods of hypoxic exposure, and that the peptidergic innervation after 8 weeks of hypoxic exposure may show an acclimatizing state.
    Histology and histopathology 05/2003; 18(2):409-18. · 2.10 Impact Factor
  • Hideki Matsuda · Yoshiaki Hayashida · Tatsumi Kusakabe
    Advances in Experimental Medicine and Biology 02/2003; 536:353-8. · 1.96 Impact Factor
  • Advances in Experimental Medicine and Biology 02/2003; 536:473-9. · 1.96 Impact Factor
  • Tatsumi Kusakabe · Hideki Matsuda · Yoshiaki Hayashida
    Advances in Experimental Medicine and Biology 02/2003; 536:611-7. · 1.96 Impact Factor
  • Tatsumi Kusakabe
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    ABSTRACT: The amphibian carotid labyrinth is a characteristic maze-like vascular expansion at the bifurcation of the common carotid artery into the internal and external carotid arteries. The carotid labyrinths of anurans are spherical and those of urodeles are oblong. In the intervascular stroma of both anuran and urodelan carotid labyrinths, the glomus cells (type I cells, chief cells) are distributed singly or in clusters between connective tissue cells and smooth muscle cells. In fluorescence histochemistry, the glomus cells emit intense fluorescence for biogenic monoamines. In fine structure, the glomus cells are characterized by a number of dense-cored vesicles in their cytoplasm. The glomus cells have long, thin cytoplasmic processes, some of which are closely associated with smooth muscle cells, endothelial cells, and pericytes. Afferent, efferent, and reciprocal synapses are found on the glomus cells. The morphogenesis of the carotid labyrinth starts in the larvae at the point where the carotid arch descends to the internal gills. Through the early stages of larval development, the slightly expanded region of the external carotid artery becomes closely connected with the carotid arch. By the end of the foot stage, the expanded region becomes globular, and at the final stage of metamorphosis the carotid labyrinth is close to its adult form. In fine structure, the glomus cells appear as early as the initial stage of larval development. At the middle stages of development, the number of dense-cored vesicles increases remarkably. Distinct afferent synapses are found in juveniles, although efferent synapses can be seen during metamorphosis. The carotid labyrinth is innervated by nerve fibers containing several kinds of regulatory neuropeptides. Double-immunolabeling in combination with a multiple dye filter system demonstrates the coexistence of two different neuropeptides. The amphibian carotid labyrinth has been electrophysiologically confirmed to have arterial chemo- and baroreceptor functions analogous to those of the mammalian carotid body and carotid sinus. The ultrastructural characteristics of the glomus cells during and after metamorphosis suggest that the glomus cells contribute to the chemoreception after metamorphosis. The three-dimensional fine structure of vascular corrosion casts suggests that the amphibian carotid labyrinth has the appropriate architecture for controlling vascular tone and the findings throughout metamorphosis reveal that the vascular regulatory function begins at an early stage of metamorphosis. In addition, immunohistochemical studies suggest that the vascular regulation in the carotid labyrinth is under peptidergic innervation. Thus, the multiple functions of the carotid labyrinth underline the importance of this relatively small organ for maintenance of homeostasis and appropriate blood supply to the cephalic region.
    Microscopy Research and Technique 11/2002; 59(3):207-26. DOI:10.1002/jemt.10195 · 1.15 Impact Factor

Publication Stats

684 Citations
201.89 Total Impact Points


  • 2000–2015
    • Kokushikan University
  • 2006
    • International Buddhist University
      Ōsaka, Ōsaka, Japan
  • 1990–2000
    • Yokohama City University
      • Department of Medicine
      Yokohama, Kanagawa, Japan
  • 1998
    • Kitasato University
      • Department of Physiology
      Edo, Tōkyō, Japan
  • 1993
    • National University (California)
      San Diego, California, United States
  • 1991
    • Pierre and Marie Curie University - Paris 6
      Lutetia Parisorum, Île-de-France, France