Cytoarchitecture of the dorsal claustrum of the cat: a quantitative Golgi study

  • Dimka Hinova-Palova
  • Georgi KotovEmail author
  • Boycho Landzhov
  • Lawrence Edelstein
  • Alexandar Iliev
  • Stancho Stanchev
  • Georgi P. Georgiev
  • Vidin Kirkov
  • Teodor Angelov
  • Dimitar Nikolov
  • Khodor Fakih
  • Adrian Paloff
Original Paper


The claustrum is a subcortical nucleus, found in the telencephalon of all placental mammals. Earlier Golgi studies have mostly focused on a qualitative description of the types of neurons. The aim of the present study was to describe the types of neurons found in the dorsal claustrum of the cat using the Golgi impregnation method and to perform a quantitative analysis of the following morphometric parameters: number of terminals (ends), total dendritic length, dendritic complexity, spine density (in spiny projection neurons), varicosity density (in aspiny interneurons). We used specimens from 5 healthy male cats stained according to the Golgi-Cox method. The dendritic trees of the studied neurons were then reconstructed through the Neurolucida software. Values of the studied quantitative parameters were obtained automatically and tested for statistically significant differences. Five types of spiny neurons were observed—large, medium-sized and small multipolar, bipolar and pyramidal-like. In addition, we described three types of aspiny neurons. The quantitative values and the statistical analysis were presented with tables and diagrams. In conclusion, we have presented a detailed analysis of the cytoarchitecture of the DC of the cat and have reported the first quantitative data on a number of morphometric parameters.


Dorsal claustrum Neurons Dendrites Quantitative analysis Golgi stain Neurolucida 



The authors of the present manuscript would like to express their most sincere gratitude to Assoc. Prof. Todor Kundurzhiev, PhD, of the Medical University of Sofia, Bulgaria for his valuable assistance in the preparation of the statistical analysis. We would also like to thank Assoc. Prof. Jordanka Angelova, PhD, of the University of Chemical Technology and Metallurgy, Sofia, Bulgaria for her help in the preparation of the figures related to the statistical analysis.

This work is supported by the Bulgarian Ministry of Education and Science under the National Program for Research ‘Young Scientists and Postdoctoral Students’.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interest.


  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 26:1213–1230. Google Scholar
  2. Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189:573–591. Google Scholar
  3. Arikuni T, Kubota K (1985) Claustral and amygdaloid afferents to the head of the caudate nucleus in macaque monkeys. Neurosci Res 2:239–254. Google Scholar
  4. Armstrong C, Krook-Magnuson E, Soltesz I (2012) Neurogliaform and ivy cells: a major family of nNOS expressing GABAergic neurons. Front Neural Circuits 6:23. Google Scholar
  5. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A et al (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568. Google Scholar
  6. Ashwell KW, Hardman C, Paxinos G (2004) The claustrum is not missing from all monotreme brains. Brain Behav Evol 64:223–241. Google Scholar
  7. Baizer JS (2014) The neurochemical organization of the claustrum. In: Smythies J, Edelstein L, Ramachandran V (eds) The claustrum. Structural, functional and clinical neuroscience. Academic Press, Massachusetts, pp 85–118Google Scholar
  8. 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. Google Scholar
  9. Basu S, Saha PK, Roszkowska M, Magnowska M, Baczynska E, Das N, Plewczynski D, Wlodarczyk J (2018) Quantitative 3-D morphometric analysis of individual dendritic spines. Sci Rep 8:3545. Google Scholar
  10. Bernstein HG, Ortmann A, Dobrowolny H, Steiner J, Brisch R, Gos T, Boqerts B (2016) Bilaterally reduced claustral volumes in schizophrenia and major depressive disorder: a morphometric postmortem study. Eur Arch Psychiatry Clin Neurosci 266:25–33. Google Scholar
  11. Boros BD, Greathouse KM, Gentry EG, Curtis KA, Birchall EL, Gearing M, Herskowitz JH (2017) Dendritic spines provide cognitive resilience against Alzheimer’s disease. Ann Neurol 82:602–614. Google Scholar
  12. Braak H, Braak E (1982) Neuronal types in the claustrum of man. Anat Embryol (Berlin) 163:447–460. Google Scholar
  13. Brand S (1981) A serial section Golgi analysis of the primate claustrum. Anat Embryol (Berlin) 162:475–488. Google Scholar
  14. 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 37:10877–10881. Google Scholar
  15. Cahill ME, Xie Z, Day M, Photowala H, Barbolina MV, Miller CA, Weiss C, Radulovic J, Sweatt JD, Disterhoft JF, Surmeier DJ, Penzes P (2009) Kalirin regulates cortical spine morphogenesis and disease-related behavioral phenotypes. Proc Natl Acad Sci USA 106:13058–13063. Google Scholar
  16. Cascella NG, Sawa A (2014) The claustrum in schizophrenia. In: Smythies J, Edelstein L, Ramachandran V (eds) The claustrum. Structural, functional and clinical neuroscience. Academic Press, Massachusetts, pp 237–243Google Scholar
  17. Cascella NG, Gerner GJ, Fieldstone SC, Sawa A, Schretlen DJ (2011) The insula-claustrum region and delusions in schizophrenia. Schizophr Res 133:77–81. Google Scholar
  18. Chameau P, Inta D, Vitalis T, Monyer H, Wadman WJ, van Hooft JA (2009) The N-terminal region of reelin regulates postnatal dendritic maturation of cortical pyramidal neurons. Proc Natl Acad Sci USA 106:7227–7232. Google Scholar
  19. Crick FC, Koch C (2005) What is the function of the claustrum? Philos Trans R Soc Lond B 360:1271–1279. Google Scholar
  20. Dávila JC, Real MA, Olmos L, Legaz I, Medina L, Guirado S (2005) Embryonic and postnatal development of GABA, calbindin, calretinin, and parvalbumin in the mouse claustral complex. J Comp Neurol 481:42–57. Google Scholar
  21. 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 525:1403–1420. Google Scholar
  22. DiFiglia M, Carey J (1986) Large neurons in the primate neostriatum examined with the combined Golgi-electron microscopic method. J Comp Neurol 244:36–52. Google Scholar
  23. Dillingham CM, Jankowski MM, Chandra R, Frost BE, O’Mara SM (2017) The claustrum: considerations regarding its anatomy, functions and a programme for research. Brain Neurosci Adv 1:1–9. Google Scholar
  24. Druga R (2014) The structure and connections of the claustrum. In: Smythies J, Edelstein L, Ramachandran V (eds) The claustrum. Structural, functional and clinical neuroscience. Academic Press, Massachusetts, pp 29–84Google Scholar
  25. Druga R, Salaj M, Barinka F, Edelstein L, Kubová H (2015) Calretinin immunoreactivity in the claustrum of the rat. Front Neuroanat 8:160. Google Scholar
  26. Druga R, Salaj M, Edelstein L (2017) Calretinin-immunoreactive neurons in the claustrum of the guinea pig. Claustrum 2:1273650. Google Scholar
  27. Edelstein LR, Denaro FJ (2004) The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol 50:675–702. Google Scholar
  28. Ellias SA, Stevens JK (1980) The dendritic varicosity: a mechanism for electrically isolating the dendrites of cat retinal amacrine cells? Brain Res 196:365–372Google Scholar
  29. Frankfurt M, Luine V (2015) The evolving role of dendritic spines and memory: interaction(s) with estradiol. Horm Behav 74:28–36. Google Scholar
  30. Gamberini M, Passarelli L, Bakola S, Impieri D, Fattori P, Rosa MG, Galletti C (2017) Claustral afferents of superior parietal areas PEc and PE in the macaque. J Comp Neurol 525:1475–1488. Google Scholar
  31. Garey LJ, Ong WY, Patel TS, Kanani M, Davis A, Mortimer AM, Barnes TR, Hirsch SR (1998) Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry 65:446–453Google Scholar
  32. Glausier JR, Lewis DA (2013) Dendritic spine pathology in schizophrenia. Neuroscience 22:90–107. Google Scholar
  33. Goll Y, Atlan G, Citri A (2015) Attention: the claustrum. Trends Neurosci 38:486–495. Google Scholar
  34. Hains AB, Vu MA, Maciejewski PK, van Dyck CH, Gottron M, Arnsten AF (2009) Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress. Proc Natl Acad Sci USA 106:17957–17962. Google Scholar
  35. Harris KM, Landis DM (1986) Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience 19:857–872. Google Scholar
  36. Havton LA, Ohara PT (1994) Cell body and dendritic tree size of intracellularly labeled thalamocortical projection neurons in the ventrobasal complex of cat. Brain Res 651:76–84. Google Scholar
  37. 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 109:61–77. Google Scholar
  38. Hinova-Palova DV, Edelstein L, Landzhov BV, Braak E, Malinova LG, Minkov M, Paloff A, Ovtscharoff W (2014) Parvalbumin-immunoreactive neurons in the human claustrum. Brain Struct Funct 219:1813–1830. Google Scholar
  39. Hinova-Palova D, Iliev A, Edelstein L, Landzhov B, Kotov G, Paloff A (2018) Electron microscopic study of Golgi-impregnated and gold-toned neurons and fibers in the claustrum of the cat. J Mol Histol 49:615–630. Google Scholar
  40. Hinova-Palova D, Iliev A, Landzhov B, Kotov G, Stanchev S, Georgiev GP, Kirkov V, Edelstein L, Paloff A (2019a) Ultrastructure of the dorsal claustrum in cat I. Types of neurons. Claustrum 4:1578636. Google Scholar
  41. Hinova-Palova D, Landzhov B, Iliev A, Kotov G, Stanchev S, Kirkov V, Georgiev GP, Edelstein L, Paloff A (2019b) Ultrastructure of the dorsal claustrum in cat. Synaptic organization. Acta Histochem, II. Google Scholar
  42. Ibáñez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koós T, Tepper JM (2011) A novel functionally distinct subtype of striatal neuropeptide Y interneuron. J Neurosci 31:16757–16769. Google Scholar
  43. Jackson J, Kamani MM, Zemelman BV, Burdakov D, Lee AK (2018) Inhibitory control of prefrontal cortex by the claustrum. Neuron 99:1029–1039. Google Scholar
  44. Jacobs B, Schall M, Prather M, Kapler E, Driscoll L, Baca S, Jacobs J, Ford K, Wainwright M, Treml M (2001) Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cereb Cortex 11:558–571. Google Scholar
  45. Kim J, Matney CJ, Roth RH, Brown SP (2016) Synaptic organization of the neuronal circuits of the claustrum. J Neurosci 36:773–784. Google Scholar
  46. Konopaske GT, Lange N, Coyle JT, Benes FM (2014) Prefrontal cortical dendritic spine pathology in schizophrenia and bipolar disorder. JAMA Psychiatry 71:1323–1331. Google Scholar
  47. Kowiański P, Dziewiatkowski J, Moryś JM, Majak K, Wójcik S, Edelstein LR, Lietzau G, Moryś J (2009) Colocalization of neuropeptides with calcium-binding proteins in the claustral interneurons during postnatal development of the rat. Brain Res Bull 80:100–106. Google Scholar
  48. Kubasik-Juraniec J, Dziewiatkowski J, Moryś J, Narkiewicz O (1998) Ultrastructural organization of the visual zone in the claustrum of the cat. Folia Morphol (Warsz) 57:287–299Google Scholar
  49. Kurada L, Bayat A, Joshi S, Koubeissi MZ (2019) The claustrum in relation to seizures and electrical stimulation. Front Neuroanat 13:8. Google Scholar
  50. LeVay S, Sherk H (1981) The visual claustrum of the cat I. Structure and connections. J Neurosci 1:956–980. Google Scholar
  51. Mamos L, Narkiewicz O, Moryś J (1986) Neurons of the claustrum in the cat; a Golgi study. Acta Neurobiol Exp (Wars) 46:171–178. Google Scholar
  52. Mathur BN (2014) The claustrum in review. Front Syst Neurosci 8:48. Google Scholar
  53. Milardi D, Bramanti P, Milazzo C, Finocchio G, Arrigo A, Santoro G, Trimarchi F, Quartarone A, Anastasi G, Gaeta M (2015) Cortical and subcortical connections of the human claustrum revealed in vivo by constrained spherical deconvolution tractography. Cereb Cortex 25:406–414. Google Scholar
  54. Moryś J, Bobinski M, Wegiel J, Wisniewski HM, Narkiewicz O (1996) Alzheimer’s disease severely affects areas of the claustrum connected with the entorhinal cortex. J Hirnforsch 37:173–180Google Scholar
  55. Moyer CE, Shelton MA, Sweet RA (2015) Dendritic spine alterations in schizophrenia. Neurosci Lett 601:46–53. Google Scholar
  56. Norita M, Hirata Y (1976) Some electron microscope findings of the claustrum of the cat. Arch Histol Jpn 39:33–49Google Scholar
  57. Ogomori K, Kitamoto T, Tateishi J, Sato Y, Suetsugu M, Abe M (1989) Beta-protein amyloid is widely distributed in the central nervous system of patients with Alzheimer’s disease. Am J Pathol 134:243–251Google Scholar
  58. Overstreet-Wadiche L, McBain CJ (2015) Neurogliaform cells in cortical circuits. Nat Rev Neurosci 16:458–468. Google Scholar
  59. Patru MC, Reser DH (2015) A new perspective on delusional states—evidence for claustrum involvement. Front Psychiatry 6:158. Google Scholar
  60. Perez-Cruz C, Nolte MW, van Gaalen MM, Rustay NR, Termont A, Tanghe A, Kirchhoff F, Ebert U (2011) Reduced spine density in specific regions of CA1 pyramidal neurons in two transgenic mouse models of Alzheimer’s disease. J Neurosci 31:3926–3934. Google Scholar
  61. Pillai AG, de Jong D, Kanatsou S, Krugers H, Knapman A, Heinzmann JM, Holsboer F, Landgraf R, Joëls M, Touma C (2012) Dendritic morphology of hippocampal and amygdalar neurons in adolescent mice is resilient to genetic differences in stress reactivity. PLoS ONE 7:e38971. Google Scholar
  62. 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. Google Scholar
  63. 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. Google Scholar
  64. Pirone A, Miragliotta V, Cozzi B, Granato A (2019) The claustrum of the pig: an immunohistochemical and a guantitative Golgi study. Anat Rec (Hoboken). Google Scholar
  65. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25:6775–6786. Google Scholar
  66. Puelles L (2017) Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain Behav Evol 90:171–189. Google Scholar
  67. Puelles L, Ayad A, Alonso A, Sandoval JE, Martínez-de-la-Torre M, Medina L, Ferran JL (2016) Selective early expression of the orphan nuclear receptor Nr4a2 identifies the claustrum homolog in the avian mesopallium: impact on sauropsidian/mammalian pallium comparisons. J Comp Neurol 524:665–703. Google Scholar
  68. Radaelli D, Poletti S, Gorni I, Locatelli C, Smeraldi E, Colombo C, Benedetti F (2014) Neural correlates of delusion in bipolar depression. Psychiatry Res 221:1–5. Google Scholar
  69. Rochefort NL, Konnerth A (2012) Dendritic spines: from structure to in vivo function. EMBO Rep 13:699–708. Google Scholar
  70. Seiriki K, Kasai A, Hashimoto T, Schulze W, Niu M, Yamaguchi S, Nakazawa T, Inoue KI, Uezono S, Takada M, Naka Y, Igarashi H, Tanuma M, Waschek JA, Ago Y, Tanaka KF, Hayata-Takano A, Nagayasu K, Shintani N, Hashimoto R, Kunii Y, Hino M, Matsumoto J, Yabe H, Nagai T, Fujita K, Matsuda T, Takuma K, Baba A, Hashimoto H (2017) High-speed and scalable whole-brain imaging in rodents and primates. Neuron 94:1085–1100. Google Scholar
  71. Shankaranarayana Rao BS, Raju RT (2004) The Golgi techniques for staining neurons. In: Raju RT, Kutty BM, Sathyaprabha TN, Shankaranarayana Rao BS (eds) Brain and behaviour. Bangalore, India, pp 108–111Google Scholar
  72. Smith JB, Radhakrishnan H, Alloway KD (2012) Rat claustrum coordinates but does not integrate somatosensory and motor cortical information. J Neurosci 32:8583–8588. Google Scholar
  73. Smith JB, Alloway KD, Hof PR, Orman R, Reser DH, Watakabe A, Watson GDR (2019) The relationship between the claustrum and endopiriform nucleus: a perspective towards consensus on cross-species homology. J Comp Neurol 527:476–499. Google Scholar
  74. Stuart G, Spruston N, Häusser M (2016) Dendrites, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  75. Szalak R, Matysek M, Mozel S, Arciszewski MB (2015) Immunocytochemical detection of calretinin in the claustrum and endopiriform nucleus of the chinchilla. Pol J Vet Sci 18:857–863. Google Scholar
  76. Tepper JM, Koós T, Ibanez-Sandoval O, Tecuapetla F, Faust TW, Assou M (2018) Heterogeneity and diversity of striatal GABAergic interneurons: update 2018. Front Neuroanat 12:91. Google Scholar
  77. Tomás Pereira I, Agster KL, Burwell RD (2016) Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat I. afferents. Hippocampus 26:1189–1212. Google Scholar
  78. Torgerson CM, Irimia A, Goh SY, Van Horn JD (2015) The DTI connectivity of the human claustrum. Hum Brain Mapp 36:827–838. Google Scholar
  79. Van Pelt J, Schierwagen A, Uylings HBM (2001) Modeling dendritic morphological complexity of deep layer cat superior colliculus neurons. Neurocomputing 38–40:403–408. Google Scholar
  80. Venneri A, Shanks M (2014) The claustrum and Alzheimer’s disease. In: Smythies J, Edelstein L, Ramachandran V (eds) The claustrum. Structural, functional and clinical neuroscience. Academic Press, Massachusetts, pp 263–275Google Scholar
  81. Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212–237. Google Scholar
  82. 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 525:1317–1346. Google Scholar
  83. Wasilewska B, Najdzion J (2001) Types of neurons of the claustrum in the rabbit—Nissl, Klüver-Barrera and Golgi studies. Folia Morphol (Warsz) 60:41–45Google Scholar
  84. White MG, Mathur BN (2018) Claustrum circuit components for top-down input processing and cortical broadcast. Brain Struct Funct 223:3945–3958. Google Scholar
  85. White MG, Panicker M, Mu C, Carter AM, Roberts BM, Dharmasri PA, Mathur BN (2018) Anterior cingulate cortex input to the claustrum is required for top-down action control. Cell Rep 22:84–95. Google Scholar
  86. Zaqout S, Kaindl AM (2016) Golgi-Cox staining step by step. Front Neuroanat 10:38. Google Scholar
  87. Zhang ZW, Kang JI, Vaucher E (2011) Axonal varicosity density as an index of local neuronal interactions. PLoS ONE 6:e22543. Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Dimka Hinova-Palova
    • 1
  • Georgi Kotov
    • 1
    Email author
  • Boycho Landzhov
    • 1
  • Lawrence Edelstein
    • 2
  • Alexandar Iliev
    • 1
  • Stancho Stanchev
    • 1
  • Georgi P. Georgiev
    • 3
  • Vidin Kirkov
    • 1
  • Teodor Angelov
    • 1
  • Dimitar Nikolov
    • 4
  • Khodor Fakih
    • 5
  • Adrian Paloff
    • 1
  1. 1.Department of Anatomy, Histology and EmbryologyMedical University of SofiaSofiaBulgaria
  2. 2.Medimark CorporationDel MarUSA
  3. 3.Department of Orthopedics and Traumatology, University Hospital ‘Queen Giovanna-ISUL’Medical University of SofiaSofiaBulgaria
  4. 4.Clinic of Cardiac SurgeryAcibadem City Clinic Tokuda HospitalSofiaBulgaria
  5. 5.Department of Oral and Maxillofacial SurgeryMedical University of SofiaSofiaBulgaria

Personalised recommendations