Skip to main content
SpringerLink
Log in

Neuronal nitric oxide synthase immunopositive neurons in cat claustrum—a light and electron microscopic study

  • Original Paper
  • Published:
Journal of Molecular Histology Aims and scope Submit manuscript

Abstract

Nitric oxide is a unique neurotransmitter, which participates in many physiological and pathological processes in the organism. Nevertheless there are little data about the neuronal Nitric Oxide Synthase immunoreactive (nNOS-ir) neurons and fibers in the dorsal claustrum (DC) of a cat. In this respect the aims of this study were: (1) to demonstrate nNOS-ir in the neurons and fibers of the DC; (2) to describe their light microscopic morphology and distribution; (3) to investigate and analyze the ultrastructure of the nNOS-ir neurons, fibers and synaptic terminals; (4) to verify whether the nNOS-ir neurons consist a specific subpopulation of claustral neurons; (5) to verify whether the nNOS-ir neurons have a specific pattern of organization throughout the DC. For demonstration of the nNOS-ir the Avidin-Biotin-Peroxidase Complex method was applied. Immunopositive for nNOS neurons and fibers were present in all parts of DC. On the light microscope level nNOS-ir neurons were different in shape and size. According to the latter they were divided into three groups—small (with diameter under 15 μm), medium-sized (with diameter from 16 to 20 μm) and large (with diameter over 21 μm). Some of nNOS-ir neurons were lightly-stained while others were darkly-stained. On the electron microscope level the immunoproduct was observed in neurons, dendrites and terminal boutons. Different types of nNOS-ir neurons differ according to their ultrastructural features. Three types of nNOS-ir synaptic boutons were found. As a conclusion we hope that the present study will contribute to a better understanding of the functioning of the DC in cat and that some of the data presented could be extrapolated to other mammals, including human.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aoki C, Rhee J, Lubin M et al (1997) NMDA-R1 subunit of the cerebral cortex co-localizes with neuronal nitric oxide synthase at pre- and postsynaptic sites and in spines. Brain Res 750:25–40. doi:10.1016/S0006-8993(96)01147-X

    Article  PubMed  CAS  Google Scholar 

  • Ashwell KWS, Hardman C, Paxinos G (2004) The claustrum is not missing from all monotreme brains. Brain Behav Evol 64:223–241. doi:10.1159/000080243

    Article  PubMed  Google Scholar 

  • Berke JJ (1960) The claustrum, the external capsule and the extreme capsule of Macaca mulatta. Neurology 115:297–321

    Google Scholar 

  • Berlucchi C (1927) Richerche di fine anatomia sul claustrum e sull’ insula dell gate. Riv Sperim Freniatria 51:125–157 (Microscopic anatomy of the claustrum and insula of the cat)

    Google Scholar 

  • Bishop A, Anderson JE (2005) NO signaling in the CNS: from the physiological to the pathological. Toxicology 208:193–205. doi:10.1016/j.tox.2004.11.034

    Article  PubMed  CAS  Google Scholar 

  • Blumcke I, Hof PR, Morrison JH et al (1991) Parvalbumin in the monkey striate cortex: a quantitative immunoelectron microscopy study. Brain Res 554:237–243. doi:10.1016/0006-8993(91)90195-2

    Article  PubMed  CAS  Google Scholar 

  • Braak H, Braak E (1982) Neuronal types in the claustrum of man. Anat Embryol (Berl) 163:473–488. doi:10.1007/BF00305558

    Google Scholar 

  • Brand S (1981) A serial section Golgi analysis of the primate claustrum. Anat Embryol (Berl) 162:447–460. doi:10.1007/BF00301872

    Google Scholar 

  • Brockhaus H (1940) Cytoarchitectural and myeloarchitectural study of claustral cortex and claustrum in man. J Psychol Neurol 49:249–348

    Google Scholar 

  • Carey RG, Neal TL (1985) The rat claustrum; afferent and efferent connections with visual cortex. Brain Res 329:185–193. doi:10.1016/0006-8993(85)90524-4

    Article  PubMed  CAS  Google Scholar 

  • Carey RG, Bear MF, Diamond IT (1980) The laminar organization of the reciprocal projections between the claustrum and the striate cortex in the tree shrew, Tupaia glis. Brain Res 184:193–198. doi:10.1016/0006-8993(80)90597-1

    Article  PubMed  CAS  Google Scholar 

  • Czeiger D, White EL (1997) Comparison of the distribution of parvalbumin-immunoreactive and other synapses onto the somata of callosal projection neurons in mouse visual and somatosensory cortex. J Comp Neurol 379:198–210. doi :10.1002/(SICI)1096-9861(19970310)379:2<198::AID-CNE3>3.0.CO;2-Z

    Article  PubMed  CAS  Google Scholar 

  • Dahrmann G, Gossrau R (1996) Nitric oxide synthase (NOS) I immunoreactivity and NOS-associated-NADPH diaphorase (NOSaNADPHd) histochemistry in mouse skeletal muscles during postnatal developmnt. Ann Anat 178:229–230

    Google Scholar 

  • Dalkara T, Moskowitz MA (1994) The complex role of nitric oxide in the pathophysiology of focal cerebral ischemia. Brain Pathol 4:49–57

    PubMed  CAS  Google Scholar 

  • Dawson DA (1994) Nitric oxide and focal cerebral ischemia: multiplicity of actions and diverse outcome. Cerebrovasc Brain Metab Rev 6:299–324

    PubMed  CAS  Google Scholar 

  • Dawson VL, Dawson TM, London ED et al (1991a) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 15:6368–6371. doi:10.1073/pnas.88.14.6368

    Article  Google Scholar 

  • Dawson TM, Bredt DS, Fotuhi M et al (1991b) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissue. Proc Natl Acad Sci USA 88:7797–7801

    Article  PubMed  CAS  Google Scholar 

  • Dawson VL, Dawson TM, Bartley DA et al (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J Neurosci 13:2651–2661

    PubMed  CAS  Google Scholar 

  • De Vries E (1910) Bemerkungen zur ontogenie und vergleichenden anatomie des ckaustrums. Folia Neurobiol 4:481–513

    Google Scholar 

  • Dinopoulos A, Papadopoulos GC, Michaloudi H et al (1992) Claustrum in the hedgehog Erinaceus europaeus brain: cytoarchitecture and connections with cortical and subcortical structures. J Comp Neurol 316:187–205. doi:10.1002/cne.903160205

    Article  PubMed  CAS  Google Scholar 

  • Dohrn CS, Beitz AJ (1994) NMDA receptor mRNA expression in NOS-containing neurons in the spinal trigeminal nucleus of the rat. Neurosci Lett 175:28–32. doi:10.1016/0304-3940(94)91070-7

    Article  PubMed  CAS  Google Scholar 

  • Druga R (1966a) The claustrum of the cat (Felis domestica). Folia Morphol (Praha) 14:7–16

    CAS  Google Scholar 

  • Druga R (1966b) Cortico-claustral connections. I. Fronto-claustral connections. Folia Morphol (Praha) 14:391–399

    Google Scholar 

  • Druga R (1968) Cortico-claustral connections. II. Connections from the parietal, temporal and occipital cortex to the claustrum. Folia Morphol (Praha) 16:142–149

    CAS  Google Scholar 

  • Druga R (1971) Projection of prepyriform cortex into claustrum. Folia Morphol (Praha) 19:405–410

    CAS  Google Scholar 

  • Druga R (1974) The claustrum and the transitional neopaleocortical area of the hedgehog (Erinacea Europaeus). Anat Anz Jena 135:442–454

    CAS  Google Scholar 

  • Druga R (1975) Claustrum (Struktura, Ontogenese a Spoje). Doctoral dissertation. Charles University, Praha, 193 p

  • Druga R, Chen S, Bentivoglio M (1993) Parvalbumin and calbindin in the rat claustrum; an immunocytochemical study combined with retrograde tracing from frontoparietal cortex. J Chem Neuroanat 6:399–406. doi:10.1016/0891-0618(93)90014-U

    Article  PubMed  CAS  Google Scholar 

  • Edelstein LR, Denaro FJ (2004) The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol 50:675–702

    PubMed  CAS  Google Scholar 

  • Edelstein LR (1986) The anatomy of the claustrum: a light- and electron-microscopic analysis in rat and monkey incorporating the technique of HRP cytochemistry, Thesis, State University of New York at Stony Brook, New York, 279 pp. (incl. 66 figures)

  • Filimonoff IN (1966) The claustrum: its origin and development. J Hirnforsch 8:503–528

    PubMed  CAS  Google Scholar 

  • Gracy KN, Pickel VM (1997) Ultrastructural localization and comparative distinction of nitric oxide sybthase and N-methyl-D-aspartate receptors in the shell of the rat nucleus accumbens. Brain Res 747:259–272. doi:10.1016/S0006-8993(96)01249-8

    Article  PubMed  CAS  Google Scholar 

  • Guirado S, Real MA, Olmos JL, Davila JC et al (2003) Distinct types of nitric oxide-producing neurons in the developing and adult mouse claustrum. J Comp Neurol 465:431–444. doi:10.1002/cne.10835

    Article  PubMed  Google Scholar 

  • Hinova-Palova D (1981) Identification of degenerated boutons in claustrum dorsale after lesion of visual cortex. C R Acad bulg Sci 34:449–452

    Google Scholar 

  • Hinova-Palova D (1986) Light-microscopic and ultrastructural organization of the claustrum in the cat. Afferent and efferent connections. Thesis, Medical Academy, Sofia

  • Hinova-Palova DV, Paloff AM (1982) Corticoclaustral connections. An electron-microscopic study. Verh Anat Ges 76:503–504

    Google Scholar 

  • Hinova-Palova D, Paloff A (1984) Identification of degenerated synaptic boutons in the claustrum of cat after lesion of the parietal cortex. Contemp Probl Neuromorphol Sofia 13–14:154–160

    Google Scholar 

  • Hinova-Palova DV, Paloff AM, Usunoff KG (1980a) Identification of three types of degenerated boutons in claustrum dorsale of the cat after lesion of the temporal cortex. C R Acad Bulg Sci 33:125–128

    Google Scholar 

  • Hinova-Palova DV, Paloff AM, Usunoff KG (1980b) Identification of three types of degenerated boutons in claustrum dorsale of the cat after lesion of the frontal cortex. C R Acad Bulg Sci 33:129–132

    Google Scholar 

  • Hinova-Palova D, Paloff A, Usunoff K, Dimova R, Wossifov T, Ivanov D (1988) Reciprocal connections between the claustrum and the auditory cortical field in the cat. An experimental study using light and electron microscopic anterograde degeneration methods and the horseradish peroxidase retrograde axonal transport. J Hirnforsch 29:255–278

    PubMed  CAS  Google Scholar 

  • Hinova-Palova DV, Paloff AM, Christova T et al (1997) Topographical distribution of NADPH-diaphorase-positive neurons in the cat’s claustrum. Eur J Morphol 35:105–116. doi:10.1076/ejom.35.2.105.13068

    Article  PubMed  CAS  Google Scholar 

  • Hinova-Palova D, Papantchev V, Hristov S, Paloff A, Ovtscharoff W (2005) Light and electron microscopical demonstration of nNOS immunoreactivity in cat’s claustrum. On congress CD of XVII Congress of Anatomy with international participation, 10–12 June, Hissar, Bulgaria

  • Hinova-Palova D, Edelstein L, Paloff A et al (2007) Parvalbumin in the cat claustrum: ultrastructure, distribution and functional implications. Acta Histochem 109:61–77. doi:10.1016/j.acthis.2006.09.006

    Article  PubMed  CAS  Google Scholar 

  • Holstein GR, Friedrich VL, Martinelli GP (2001) Monoclonal L-citrulline immunostaining reveals nitric oxide-producing vestibular neurons. Ann N Y Acad Sci 942:65–78

    Article  PubMed  CAS  Google Scholar 

  • Hope BT, Michael GJ, Knigge KM et al (1991) Vincent SR. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814. doi:10.1073/pnas.88.7.2811

    Article  PubMed  CAS  Google Scholar 

  • Iadecola C (1997) Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci 20:132–139. doi:10.1016/S0166-2236(96)10074-6

    Article  PubMed  CAS  Google Scholar 

  • Kowianski P, Morys J, Karwacki Z (1998) The cortico-related zones of the rabbit claustrum - study of the claustrocortical connections based on the retrograde axonal transport of fluorescent tracers. Brain Res 784:199–209. doi:10.1016/S0006-8993(97)01326-7

    Article  PubMed  CAS  Google Scholar 

  • Kowianski P, Morys J, Wojcik S (2002) Postnatal development of NOS-ir neurons in the rat claustrum. Folia Morphol 61:11–17

    Google Scholar 

  • Kowianski P, Morys JM, Wojcik S et al (2003) Co-localization of NOS with calcium-binding proteins during the postnatal development of the rat claustrum. Folia Morphol (Warsz) 62:211–214

    Google Scholar 

  • Kowianski P, Morys JM, Wojcik S et al (2004) Neuropeptide-containing neurons in the endopiriform region of the rat: morphology and colocalization with calcium-binding proteins and nitric oxide synthase. Brain Res 996:97–110. doi:10.1016/j.brainres.2003.10.020

    Article  PubMed  CAS  Google Scholar 

  • Krushkov I, Markova T, Tsankov A (1996) The participation of nitric oxide in the functions of the central nervous system and the cardiovascular system. Mol Med (Sofia) 1:21–27

    CAS  Google Scholar 

  • Kullo IJ, Schwartz RS, Pompili VJ et al (1997) Expression and function of recombinant endothelial NO synthase in coronary artery smooth muscle cells. Arterioscler Thromb Vasc Biol 11:2405–2412

    Google Scholar 

  • Kunzle H (1975) Bilateral projection from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88:195–209. doi:10.1016/0006-8993(75)90384-4

    Article  PubMed  CAS  Google Scholar 

  • Kunzle H (1978) An autoradiographic analysis of the efferent connections from the premotor and adjacent prefrontal regions (area 6 and 9) in Macaca fascicularis. Brain Behav Evol 15:185–234

    Article  PubMed  CAS  Google Scholar 

  • Landau E (1923) Zur kenntnis der Beziehungen des claustrums zum nucleus amygdalae und zur area piriformis im speziellen zum tractus olfactorius. Schweiz Arch Neurol Psychiatr 13:391–400

    Google Scholar 

  • LeVay S, Sherk H (1981a) The visual claustrum of the cat. I. Structure and connections. J Neurosci 1:956–980

    PubMed  CAS  Google Scholar 

  • LeVay S, Sherk H (1981b) The visual claustrum of the cat. II. The visual field map. J Neurosci 1:981–992

    CAS  Google Scholar 

  • Lieberman AR (1973) Neurons with presynaptic perikarya and presynaptic dendrites in the rat lateral geniculate nucleus. Brain Res 59:35–59. doi:10.1016/0006-8993(73)90252-7

    Article  PubMed  CAS  Google Scholar 

  • Lin L-H, Talman T (2000) N-methyl-D-aspartate receptors on neurons that synthesize nitric oxide in rat nucleus tractus solitarii. Neuroscience 100:581–588. doi:10.1016/S0306-4522(00)00314-6

    Article  PubMed  CAS  Google Scholar 

  • Loo TT (1931) The forebrain of the opossum, Didelphis virginiana. J Comp Neurol 52:1–148. doi:10.1002/cne.900520102

    Article  Google Scholar 

  • Lysakowski A, Singer M (2000) Nitric oxide synthase localized in a subpopulation of vestibular efferents in NADPH diaphorase histochemistry and nitric oxide synthase immunohistochemistry. J Comp Neurol 427:508–521. doi :10.1002/1096-9861(20001127)427:4<508::AID-CNE2>3.0.CO;2-L

    Article  PubMed  CAS  Google Scholar 

  • Macchi G (1984) Morphology and structure of human claustrum. Cervello 24:1–26

    Google Scholar 

  • Macchi G, Bentivoglio M, Minciacchi D et al (1983) Claustroneocortical projections studied in the cat by means of multiple retrograde fluorescent tracing. J Comp Neurol 215:121–134. doi:10.1002/cne.902150202

    Article  PubMed  CAS  Google Scholar 

  • Maeda M, Inoue M, Takao S, Nakai M et al (1999) Central control mechanisms of circulation in the medulla oblongata by nitric oxide. Jpn J Physiol 49:467–478. doi:10.2170/jjphysiol.49.467

    Article  PubMed  CAS  Google Scholar 

  • Mamos L (1984) Morphology of claustral neurons in the rat. Folia Morphol (Warsz) 43:73–78

    CAS  Google Scholar 

  • Marino J, Cudeiro J (2003) Nitric oxide-mediated cortical activation: a diffuse wake-up system. J Neurosci 23:4299–4307

    PubMed  CAS  Google Scholar 

  • Martinelli G, Fridrich V, Holstein G (2002) l-citrulline immunostaining identifies nitric oxide production sites within neurons. Neuroscience 114:111–122. doi:10.1016/S0306-4522(02)00238-5

    Article  PubMed  CAS  Google Scholar 

  • Mizukawa K (1990) Reduced nicotinamide-adenine-dinucleotide-phosphat-diaphorase histochemistry: light and electron microscopic investigations. Methods Neurosci 3:457–472

    Google Scholar 

  • Mizukawa K, Vincent SR, McGeer PL et al (1989) Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphat-diaphorase-positive cells and fibers in the cat neurvous system. J Comp Neurol 279:281–311. doi:10.1002/cne.902790210

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Lopez B, Escudero M, Delgado-Garcia JM et al (1996) Nitric oxide production by brain stem neurons is required for normal performance of eye movements in alert animals. Neuron 17:739–745. doi:10.1016/S0896-6273(00)80205-6

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Lopez B, Estrada C, Escudero M (1998) Mechanisms of action and targets of nitric oxide in the oculomotor system. J Neurosci 18:10672–10679

    PubMed  CAS  Google Scholar 

  • Moreno-Lopez B, Escudero M, Estrada C (2001) Morphological identification of nitric oxide sources and targets in the cat oculomotor system. J Comp Neurol 435:311–324. doi:10.1002/cne.1032

    Article  PubMed  CAS  Google Scholar 

  • Morest DK (1971) Dendrodendritic synapses of the cells that have axons: the fine structure of the Golgi type II cells in the medial geniculate body of the cat. Z Anat Entwickl Gesch 133:216–246. doi:10.1007/BF00528025

    Article  CAS  Google Scholar 

  • Morys J, Berdel B, Maciejewska B et al (1996) Division of the human claustrum according to its architectonics, morphometric parameters and cortical connections. Folia Morphol (Warsz) 55:69–82

    CAS  Google Scholar 

  • Neal JW, Pearson RCA, Powell TPS (1986) The relationship between the auditory cortex and the claustrum in the cat. Brain Res 366:145–151. doi:10.1016/0006-8993(86)91289-8

    Article  PubMed  CAS  Google Scholar 

  • Norita M (1977) Demonstration of bilateral claustro-cortical connections in the cat with the method of retrograde axonal transport of horseradish peroxidase. Arch Histol Jpn 40:1–10

    PubMed  CAS  Google Scholar 

  • Olsen CR, Graybiel AM (1980) Sensory maps in the claustrum of the cat. Nature 288:479–481. doi:10.1038/288479a0

    Article  Google Scholar 

  • Otelin VA, Makarov FN (1972) Dokl Akad Nauk SSSR 202:723–725. Descending connections of the auditory cortex of the cat with contralateral neostriatal complex and claustrum, Ser Biol

    Google Scholar 

  • Paloff AM (1985) Somatodendritic synapses in the central nucleus of colliculus inferior (CI) in the cat. J Hirnforsch 26:353–358

    PubMed  CAS  Google Scholar 

  • Paloff AM, Hinova-Palova DV (1998) Topographical distribution of NADPH-diaphorase-positive neurons in the cat’s inferior colliculus. J Hirnforsch 39:231–243

    PubMed  CAS  Google Scholar 

  • Paloff AM, Usunoff KG (1992a) The fine structure of the inferior colliculus in the cat. II. Synaptic organization. J Hirnforsch 32:77–106

    Google Scholar 

  • Paloff AM, Usunoff KG (1992b) Projections to the inferior colliculus from the dorsal column nuclei. An experimental electron-microscopic study in the cat. J Hirnforsch 33:597–610

    PubMed  CAS  Google Scholar 

  • Paloff A, Bozhilova-Pastirova A, Hinova-Palova D, et al (1998) Co-existence of GABA and parvalbumin in the cat’s inferior colliculus. An electronmicroscopical study. Paper presented at the First congress of the Bulgarien Society for Neuroscience, Sofia, p 16

  • Paloff AM, Usunoff KG, Hinova-Palova D et al (1989) The fine structure of the inferior colliculus in the cat. I. Neuronal perikarya in the central nucleus. J Hirnforsch 30:69–90

    PubMed  CAS  Google Scholar 

  • Paloff A, Usunoff K, Yotovski P et al (2004) Parvalbumin-like immunostaining in the cat inferior colliculus. Light- and electron-microscopic investigation. Acta Histochem 106:219–234. doi:10.1016/j.acthis.2003.11.006

    Article  PubMed  Google Scholar 

  • Papantchev V, Christova T, Paloff A et al (2003) NADPH diaphorase positive capillaries in the brain stem of the cat. Praemedicus Since 1925 22:126–131

    Google Scholar 

  • Papantchev V, Paloff A, Christova T et al (2005) Light microscopical study of nitric oxide synthase I-positive neurons, including fibres in the vestibular nuclear complex of the cat. Acta Histochem 107:113–120. doi:10.1016/j.acthis.2005.01.004

    Article  PubMed  CAS  Google Scholar 

  • Papantchev V, Paloff A, Hinova-Palova D et al (2006) Neuronal nitric oxide synthase immunopositive neurons in cat vestibular complex: a light and electron microscopic study. J Mol Histol 37:343–352. doi:10.1007/s10735-006-9061-6

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1989) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Pearson RCA, Brodal P, Gatter KC et al (1982) The organization of the connections between the cortex and the claustrum in the monkey. Brain Res 234:435–441. doi:10.1016/0006-8993(82)90883-6

    Article  PubMed  CAS  Google Scholar 

  • Pilleri G (1961) The claustrum of Didelphis marsupialis Lin (Marsupialis, Didelphoidea). Acta Anat (Basel) 45:310–314. doi:10.1159/000141759

    Article  CAS  Google Scholar 

  • Pilleri G (1962) The claustrum of the Canadian beaver (Castor canadensis Kuhl): Structure and comparative anatomy. J Hirnforsch 5:59–81

    PubMed  CAS  Google Scholar 

  • Pro-Sistiaga P, Fuentes M, Alejo A et al (2002) Nitric oxide synthase expression in the rabbit claustrum (abstract) FENS forum, Paris

  • Rae ASL (1954) The connections of the claustrum. Confin Neurol Basel 14:211–219. doi:10.1159/000105714

    Article  CAS  Google Scholar 

  • Rahman F, Baizer J (2007) Neurochemically defined cell types in the claustrum of the cat. Brain Res 1159:94–111. doi:10.1016/j.brainres.2007.05.011

    Article  PubMed  CAS  Google Scholar 

  • Real MA, Davila JC, Guirado S (2003) Expression of calcium-binding proteins in the mouse claustrum. J Chem Neuroanat 25:151–160. doi:10.1016/S0891-0618(02)00104-7

    Article  PubMed  CAS  Google Scholar 

  • Reinozo-Suarez F (1961) Topographischer hirnatlas der katze fur experimental-physiologische untersuehungen. Darmstadt

  • Riche D, Lanoir J (1978) Some claustrocortical connections in the cat and baboon as studied by retrograde HRP transport. J Comp Neurol 177:435–444. doi:10.1002/cne.901770306

    Article  PubMed  CAS  Google Scholar 

  • Rodrigo J, Springall DR, Uttenthal O et al (1994) Localization of nitric oxide synthase in the adult rat brain. Philos Trans R Soc Lond B Biol Sci 345:175–221. doi:10.1098/rstb.1994.0096

    Article  PubMed  CAS  Google Scholar 

  • Romansky KV, Usunoff KG (1985) The fine structure of the subthalamic nucleus in the cat. I. Neuronal perikarya. J Hirnforsch 26:259–273

    PubMed  CAS  Google Scholar 

  • Rowniak M, Szteyn S, Robak A et al (1994) The types of neurons in the claustrum of Bison bonanus: Nissl and Golgi study. Folia Morphol 53:231–237

    CAS  Google Scholar 

  • Sadowski M, Morys J, Jakubowska-Sadowska K (1997) Rat’s claustrum shows two main cortico-related zones. Brain Res 756:147–152

    Article  PubMed  CAS  Google Scholar 

  • Samdani A, Dawson T, Dawson V (1997) Nitric oxide synthase in models of focal ischemia. Stroke 28:1283–1288

    PubMed  CAS  Google Scholar 

  • Sears CE, Ashley EA, Casadei B (2004) Nitric oxide control of cardiac function: is neuronal nitric oxide synthase a key component? Philos Trans R Soc Lond B Biol Sci 359:1021–1044. doi:10.1098/rstb.2004.1477

    Article  PubMed  CAS  Google Scholar 

  • Seidel B, Stanarius A, Wolf G (1997) Differential expression of neuronal and endothelial nitric oxide synthase in blood vessels of the rat brain. Neurosci Lett 239:109–112. doi:10.1016/S0304-3940(97)00912-9

    Article  PubMed  CAS  Google Scholar 

  • Seyidova D, Aliyev A, Rzayev N et al (2004) The role of nitric oxide in the pathogenesis of brain lesions during the development of Alzheimer’s disease. In vivo 18:325–333

    PubMed  CAS  Google Scholar 

  • Sherk H (1986) The claustrum and the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 5. Plenum Press, New York, pp 467–499

    Google Scholar 

  • Sloniewski P, Usunoff KG, Pilgrim C (1986) Diencephalic and mesencephalic afferents of the rat claustrum. Anat Embryol (Berl) 173:401–411. doi:10.1007/BF00318925

    Article  CAS  Google Scholar 

  • Soares JG, Mendez-Otero R, Gattass R (2003) Distribution of NADPH-diaphorase in the superior colliculus of Cebus monkeys, and co-localization with calcium-binding proteins. Neurosci Res 46:475–483. doi:10.1016/S0168-0102(03)00125-1

    Article  PubMed  CAS  Google Scholar 

  • Spahn B, Braak H (1985) Percentage of projection neurons and various types of interneurons in the human claustrum. Acta Anat (Basel) 122:245–248

    Article  CAS  Google Scholar 

  • Stelmasiak M (1955) Volume of the claustrum in man. Folia Morphol (Warsz) 6:137–144

    CAS  Google Scholar 

  • Sugiyama T, Fujita M, Koide N et al (2003) Differences in the mechanism of nitric oxide production between mouse vascular endothelial cells and macrophages. J Endotoxin Res 9:108–112

    PubMed  CAS  Google Scholar 

  • Tanne-Gariepy J, Boussaoud D, Rouiller EM (2002) Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey. J Comp Neurol 454:140–157. doi:10.1002/cne.10425

    Article  PubMed  Google Scholar 

  • Usunoff KG (1990) Cytoarchitectural, ultrastructural and histochemical characteristics of substantia nigra, Thesis. Medical Academy, Sofia, Bulgaria

  • Vater M, Braun K (1994) Parvalbumin, calbindin D-28 k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats. J Comp Neurol 341:534–558. doi:10.1002/cne.903410409

    Article  PubMed  CAS  Google Scholar 

  • Wada K, Chatzipanteli K, Kraydieh S et al (1998) The role of inducible nitric oxide synthase in the pathophysiology of traumatic brain injury in the rat. Neurosurgery 43:1427–1436. doi:10.1097/00006123-199812000-00096

    Article  PubMed  CAS  Google Scholar 

  • Witter MP, Room P, Groenewegen HJ et al (1988) Reciprocal connections of the insular and piriform claustrum with limbic cortex: an anatomical study in the cat. Neurosci 24:519–539. doi:10.1016/0306-4522(88)90347-8

    Article  CAS  Google Scholar 

  • Wojcik S, Dziewiatkowski J, Spodnik E et al (2004) Analysis of calcium-binding protein immunoreactivity in the claustrum and the endopiriform nucleus of the rabbit. Acta Neurobiol Exp (Warsz) 64:449–460

    Google Scholar 

  • Zilles K, Zilles B (1980) Schleicher A. A quantitative approach to cytoarchitectonics. VI. The areal pattern of the cortex of the albino rat. Anat Embryol (Berl) 159:335–360. doi:10.1007/BF00317655

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Histology, Medical University, 1431, Sofia, Bulgaria

    Dimka Hinova-Palova, Adrian Paloff, Vassil Papantchev & Wladimir Ovtscharoff

  2. P.O. Box 2316, Del Mar, CA, 92014, USA

    Lawrence Edelstein

  3. Deparment of Forensic Medicine, Medical University, 1431, Sofia, Bulgaria

    Stanislav Hristov

Authors
  1. Dimka Hinova-Palova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lawrence Edelstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adrian Paloff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stanislav Hristov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vassil Papantchev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wladimir Ovtscharoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vassil Papantchev.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hinova-Palova, D., Edelstein, L., Paloff, A. et al. Neuronal nitric oxide synthase immunopositive neurons in cat claustrum—a light and electron microscopic study. J Mol Hist 39, 447–457 (2008). https://doi.org/10.1007/s10735-008-9184-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10735-008-9184-z

Keywords

Search

Navigation