Journal of Molecular Histology

, Volume 49, Issue 6, pp 615–630 | Cite as

Electron microscopic study of Golgi-impregnated and gold-toned neurons and fibers in the claustrum of the cat

  • Dimka Hinova-Palova
  • Alexandar IlievEmail author
  • Lawrence Edelstein
  • Boycho Landzhov
  • Georgi Kotov
  • Adrian Paloff
Original Paper


The claustrum is a subcortical nucleus found in the telencephalon of all placental mammals. It is a symmetrical, thin and irregular sheet of grey matter which lies between the inner surface of the insular cortex and the outer surface of the putamen. The claustrum has extensive connections with the visual, auditory, somatosensory and motor regions of the cortex, as well as with subcortical and allocortical regions. The aim of this study was to provide a detailed description of the morphology of different types of Golgi-impregnated and gold-toned neurons and fibers in the dorsal claustrum of the cat employing the combined Golgi-electron microscope Fairén method. We were able to distinguish two major types of neurons: those with dendritic spines (spiny) and those without dendritic spines (aspiny). In both groups we observed large (21–40 µm in diameter), medium-sized (16–21 µm in diameter) and small cells (10–16 µm in diameter), describing their ultrastructural organization and characteristic features, including the presence of terminal boutons. These ultrastructural findings allow us to conclude that large and medium-sized spiny claustral neurons are indeed efferent neurons, projecting to the cortex, while the small spiny and the different types of aspiny neurons are most likely inhibitory local circuit interneurons. The findings in the present study will hopefully contribute to a better understanding of the role of the claustrum.


Claustrum Neurons Ultrastructure Fairén method Cat 


  1. Agster KL, Tomás Pereira I, Saddoris MP, Burwell RD (2016) Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat. II. efferents. Hippocampus 26(9):1213–1230. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189(4):573–591. CrossRefPubMedGoogle Scholar
  3. Arikuni T, Kubota K (1985) Claustral and amygdaloid afferents to the head of the caudate nucleus in macaque monkeys. Neurosci Res 2(4):239–254. CrossRefPubMedGoogle Scholar
  4. Atlan G, Terem A, Peretz-Rivlin N, Groysman M, Citri A (2017) Mapping synaptic cortico-claustral connectivity in the mouse. J Comp Neurol 525(6):1381–1402. CrossRefPubMedGoogle Scholar
  5. Baizer JS, Sherwood CC, Noonan M, Hof PR (2014) Comparative organization of the claustrum: what does structure tell us about function? Front Syst Neurosci 8:117. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Baugh LA, Lawrence JM, Marotta JJ (2011) Novel claustrum activation observed during a visuomotor adaptation task using a viewing window paradigm. Behav Brain Res 223(2):395–402. CrossRefPubMedGoogle Scholar
  7. Braak H, Braak E (1982) Neuronal types in the claustrum of man. Anat Embryol (Berlin) 163(4):447–460. CrossRefGoogle Scholar
  8. Brand S (1981) A serial section Golgi analysis of the primate claustrum. Anat Embryol (Berlin) 162(4):475–488. CrossRefGoogle Scholar
  9. Brown SP, Mathur BN, Olsen SR, Luppi PH, Bickford ME, Citri A (2017) New breakthroughs in understanding the role of functional interactions between the neocortex and the claustrum. J Neurosci 37(45):10877–10881. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Buchanan KJ, Johnson JI (2011) Diversity of spatial relationships of the claustrum and insula in branches of the mammalian radiation. Ann N Y Acad Sci 1225(S1):E30–E63. CrossRefPubMedGoogle Scholar
  11. Chau A, Salazar AM, Krueger F, Cristofori I, Grafman J (2015) The effect of claustrum lesions on human consciousness and recovery of function. Conscious Cogn 36:256–264. CrossRefPubMedGoogle Scholar
  12. Clascá F, Avendaño C, Román-Guindo A, Llamas A, Reinoso-Suárez F (1992) Innervation from the claustrum of the frontal association and motor areas: axonal transport studies in the cat. J Comp Neurol 326(3):402–422. CrossRefPubMedGoogle Scholar
  13. Cozzi B, Roncon G, Granato A, Giurisato M, Castagna M, Peruffo A, Panin M, Ballarin C, Montelli S, Pirone A (2014) The claustrum of the bottlenose dolphin Tursiops truncatus (Montagu 1821). Front Syst Neurosci 8:42. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Crick FC, Koch C (2005) What is the function of the claustrum? Philos Trans R Soc Lond B 360(1458):1271–1279. CrossRefGoogle Scholar
  15. Day-Brown JD, Slusarczyk AS, Zhou N, Quiggins R, Petry HM, Bickford ME (2017) Synaptic organization of striate cortex projections in the tree shrew: a comparison of the claustrum and dorsal thalamus. J Comp Neurol 525(6):1403–1420. CrossRefPubMedGoogle Scholar
  16. Deutch AY, Mathur BN (2015) Editorial: the claustrum: charting a way forward for the brain’s most mysterious nucleus. Front Syst Neurosci 15(9):103. CrossRefGoogle Scholar
  17. Dinopoulos A, Papadopoulos GC, Michaloudi H, Parnavelas JG, Uylings HB, Karamanlidis AN (1992) Claustrum in the hedgehog (Erinaceus europaeus) brain: cytoarchitecture and connections with cortical and subcortical structures. J Comp Neurol 316(2):187–205. CrossRefPubMedGoogle Scholar
  18. Druga R (1966) The claustrum of the cat (Felis domestica). Folia Morphol (Praha) 14:7–16Google Scholar
  19. Edelstein LR, Denaro FJ (2004) The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol 50:675–702. CrossRefPubMedGoogle Scholar
  20. Fairén A, Peters A, Saldanha J (1977) A new procedure for examining Golgi impregnated neurons by light and electron microscopy. J Neurocytol 6(3):311–337. CrossRefPubMedGoogle Scholar
  21. Goll Y, Atlan G, Citri A (2015) Attention: the claustrum. Trends Neurosci 38(8):486–495. CrossRefPubMedGoogle Scholar
  22. Hinova-Palova DV, Dimova R, Ivanov DP (1987) Identification of small neurons (dwarf cells) in the claustrum of the cat. Light and electron microscopic observations. Verh Anat Ges Leipzig 82(Anat Anz Suppl 164):83Google Scholar
  23. Hinova-Palova DV, Paloff A, Christova T, Ovtscharoff W (1997) Topographical distribution of NADPH-diaphorase-positive neurons in the cat’s claustrum. Eur J Morphol 35(2):105–116CrossRefGoogle Scholar
  24. Hinova-Palova DV, Edelstein LR, Paloff AM, Hristov S, Papantchev VG, Ovtscharoff WA (2007) Parvalbumin in the cat claustrum: ultrastructure, distribution and functional implications. Acta Histochem 109(1):61–77. CrossRefPubMedGoogle Scholar
  25. Hinova-Palova D, Edelstein L, Paloff A, Hristov S, Papantchev V, Ovtscharoff W (2008) Neuronal nitric oxide synthase immunopositive neurons in cat claustrum—a light and electron microscopic study. J Mol Histol 39(4):447–457. CrossRefPubMedGoogle Scholar
  26. Hinova-Palova D, Edelstein L, Papantchev V, Landzhov B, Malinova L, Todorova-Papantcheva D, Minkov M, Paloff A, Ovtscharoff W (2012) Light and electron-microscopic study of leucine enkephalin immunoreactivity in the cat claustrum. J Mol Histol 43(6):641–649. CrossRefPubMedGoogle Scholar
  27. Hinova-Palova DV, Edelstein L, Landzhov B, Minkov M, Malinova L, Hristov S, Denaro FJ, Alexandrov A, Kiriakova T, Brainova I, Paloff A, Ovtscharoff W (2014a) Topographical distribution and morphology of NADPH-diaphorase-stained neurons in the human claustrum. Front Syst Neurosci 8:96. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hinova-Palova DV, Edelstein L, Landzhov BV, Braak E, Malinova LG, Minkov M, Paloff A, Ovtscharoff W (2014b) Parvalbumin-immunoreactive neurons in the human claustrum. Brain Struct Funct 219(5):1813–1830. CrossRefPubMedGoogle Scholar
  29. Hinova-Palova DV, Landzhov B, Dzhambazova E, Minkov M, Edelstein L, Malinova L, Paloff A, Ovtscharoff W (2014c) Neuropeptide Y immunoreactivity in the cat claustrum: a light- and electron-microscopic investigation. J Chem Neuroanat 61–62:107–119. CrossRefPubMedGoogle Scholar
  30. Johnson JI, Fenske BA, Jaswa AS, Morris JA (2014) Exploitation of puddles for breakthroughs in claustrum research. Front Syst Neurosci 8:78. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kavounoudias A, Roll JP, Anton JL, Nazarian B, Roth M, Roll R (2008) Proprio-tactile integration for kinesthetic perception: an fMRI study. Neuropsychologia 46(2):567–575. CrossRefPubMedGoogle Scholar
  32. Kim J, Matney CJ, Roth RH, Brown SP (2016) Synaptic organization of the neuronal circuits of the claustrum. J Neurosci 36(3):773–784. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kowiański P, Dziewiatkowski J, Kowiańska J, Moryś J (1999) Comparative anatomy of the claustrum in selected species: a morphometric analysis. Brain Behav Evol 53(1):44–54. CrossRefPubMedGoogle Scholar
  34. Landzhov B, Hinova-Palova D, Edelstein L, Dzhambazova E, Brainova I, Georgiev GP, Ivanova V, Paloff A, Ovtscharoff W (2017) Comparative investigation of neuronal nitric oxide synthase immunoreactivity in rat and human claustrum. J Chem Neuroanat 86:1–14. CrossRefPubMedGoogle Scholar
  35. LeVay S, Sherk H (1981) The visual claustrum of the cat. I. Structure and connections. J Neurosci 1(9):956–980. CrossRefPubMedGoogle Scholar
  36. Mamos L, Narkiewicz O, Moryś J (1986) Neurons of the claustrum in the cat: a Golgi study. Acta Neurobiol Exp (Wars) 46(4):171–178Google Scholar
  37. Markowitsch HJ, Irle E, Bang-Olsen R, Flindt-Egebak P (1984) Claustral efferents to the cat’s limbic cortex studied with retrograde and anterograde tracing techniques. Neuroscience 12(2):409–425. CrossRefPubMedGoogle Scholar
  38. Mathur BN (2014) The claustrum in review. Fron Syst Neurosci 8:48. CrossRefGoogle Scholar
  39. Mathur BN, Reser D, Smith JB (2017) Conference Proceedings: 3rd Annual Society for Claustrum Research Meeting. Claustrum 2:1. CrossRefGoogle Scholar
  40. Moryś J, Berdel B, Maciejewska B, Sadowski M, Sidorowicz M, Kowiañska J, Narkiewicz O (1996) Division of the human claustrum according to its architectonics and morphometric parameters. Folia Morphol (Warsz) 55(2):69–82Google Scholar
  41. Narkiewicz O (1964) Degeneration in the claustrum after regional neocortical ablations in the cat. J Comp Neurol 123:335–336. CrossRefPubMedGoogle Scholar
  42. Norita M, Hirata Y (1976) Some electron microscope findings of the claustrum of the cat. Arch Histol Japonicum 39(1):33–49CrossRefGoogle Scholar
  43. Olson CR, Graybiel AM (1980) Sensory maps in the claustrum of the cat. Nature 288(5790):479–481. CrossRefPubMedGoogle Scholar
  44. Pearson JC, Haines DE (1980) Somatosensory thalamus of a prosimian primate (Galago senegalensis). II. An HRP and Golgi study of the ventral posterolateral nucleus (VPL). J Comp Neurol 190(3):559–580. CrossRefPubMedGoogle Scholar
  45. Peters A, Fairén A (1978) Smooth and sparsely-spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscopic technique. J Comp Neurol 181(1):129–171. CrossRefPubMedGoogle Scholar
  46. Pirone A, Cozzi B, Edelstein L, Peruffo A, Lenzi C, Quilici F, Antonini R, Castagna M (2012) Topography of Gng2- and NetrinG2-expression suggests an insular origin of the human claustrum. PLoS ONE 7(9):e44745. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pirone A, Castagna M, Granato A, Peruffo A, Quilici F, Cavicchioli L, Piano I, Lenzi C, Cozzi B (2014) Expression of calcium-binding proteins and selected neuropeptides in the human, chimpanzee, and crab-eating macaque claustrum. Front Syst Neurosci 8:99. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Pirone A, Magliaro C, Giannessi E, Ahluwalia A (2015) Parvalbumin expression in the claustrum of the adult dog. An immunohistochemical and topographical study with comparative notes on the structure of the nucleus. J Chem Neuroanat 64–65:33–42. CrossRefPubMedGoogle Scholar
  49. Pirone A, Cantile C, Miragliotta V, Lenzi C, Giannessi E, Cozzi B (2016) Immunohistochemical distribution of the cannabinoid receptor 1 and fatty acid amide hydrolase in the dog claustrum. J Chem Neuroanat 74:21–27. CrossRefPubMedGoogle Scholar
  50. Pirone A, Miragliotta V, Ciregia F, Giannessi E, Cozzi B (2018) The catecholaminergic innervation of the claustrum of the pig. J Anat 232(1):158–166. CrossRefPubMedGoogle Scholar
  51. Reser DH, Majka P, Snell S, Chan JM, Watkins K, Worthy K, Quiroga MD, Rosa MG (2017) Topography of claustrum and insula projections to medial prefrontal and anterior cingulate cortices of the common marmoset (Callithrix jacchus). J Comp Neurol 525(6):1421–1441. CrossRefPubMedGoogle Scholar
  52. Smith JB, Alloway KD (2010) Functional specificity of claustrum connections in the rat: interhemispheric communication between specific parts of motor cortex. J Neurosci 30(50):16832–16844. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Smith JB, Alloway KD (2014) Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Front Syst Neurosci 8:93. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Smythies J, Edelstein L, Ramachandran V (eds) (2014) The claustrum. Structural, functional and clinical neuroscience. Academic Press, CambridgeGoogle Scholar
  55. Spahn B, Braak H (1985) Percentage of projection neurons and various types of interneurons in the human claustrum. Acta Anat (Basel) 122(4):245–248. CrossRefGoogle Scholar
  56. Stedehouder J, Kushner SA (2017) Myelination of parvalbumin interneurons: a parsimonious locus of pathophysiological convergence in schizophrenia. Mol Psychiatry 22(1):4–12. CrossRefPubMedGoogle Scholar
  57. Tomás Pereira I, Agster KL, Burwell RD (2016) Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat. I. afferents. Hippocampus 26(9):1189–1212. CrossRefPubMedGoogle Scholar
  58. Torgerson CM, Irimia A, Goh SY, Van Horn JD (2015) The DTI connectivity of the human claustrum. Hum Brain Mapp 36(3):827–838. CrossRefPubMedGoogle Scholar
  59. Valverde F (1970) The Golgi method. A tool for comparative structural analysis. In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, Berlin, pp 12–31CrossRefGoogle Scholar
  60. Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508(2):212–237. CrossRefPubMedGoogle Scholar
  61. Wang Q, Ng L, Harris JA, Feng D, Li Y, Royall JJ, Oh SW, Bernard A, Sunkin SM, Koch C, Zeng H (2017) Organization of the connections between claustrum and cortex in the mouse. J Comp Neurol 525(6):1317–1346. CrossRefPubMedGoogle Scholar
  62. Watson GDR, Smith JB, Alloway KD (2017) Interhemispheric connections between the infralimbic and entorhinal cortices: the endopiriform nucleus has limbic connections that parallel the sensory and motor connections of the claustrum. J Comp Neurol 525(6):1363–1380. CrossRefPubMedGoogle Scholar
  63. White MG, Cody PA, Bubser M, Wang HD, Deutch AY, Mathur BN (2017) Cortical hierarchy governs rat claustrocortical circuit organization. J Comp Neurol 525(6):1347–1362. CrossRefPubMedGoogle Scholar
  64. Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong HW (2014) Neural networks of the mouse neocortex. Cell 156(5):1096–1111. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Anatomy, Histology and EmbryologyMedical University of SofiaSofiaBulgaria
  2. 2.Medimark CorporationDel MarUSA

Personalised recommendations