Vol 61, No 2 (2023)
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Published online: 2023-07-06

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Immunocytochemical localization of calbindin-D28K, calretinin, and parvalbumin in the Mongolian gerbil (Meriones unguiculatus) visual cortex

Jae-Rim Son1, Xin-Yu Kuai1, Chang-Jin Jeon1
Pubmed: 37435896
Folia Histochem Cytobiol 2023;61(2):81-97.

Abstract

Introduction. While most animals of the Muridae family are nocturnal, the gerbil displays diurnal activity and provides a useful model for visual system research. The purpose of this study was to investigate the localization of calcium-binding proteins (CBPs) in the visual cortex of the Mongolian gerbil (Meriones unguiculatus). We also compared the labeling of CBPs to those of gamma-aminobutyric acid (GABA)- and nitric oxide synthase (NOS)-containing neurons.

Material and methods. The study was conducted on twelve adult Mongolian gerbils (3–4 months old). We used horseradish peroxidase immunocytochemistry and two-color fluorescence immunocytochemistry with conventional and confocal microscopy to assess CBPs localization in the visual cortex.

Results. The highest density of calbindin-D28K (CB)- (34.18%) and parvalbumin (PV)-IR (37.51%) neurons was found in layer V, while the highest density of calretinin (CR)-IR (33.85%) neurons was found in layer II. The CB- (46.99%), CR- (44.88%), and PV-IR (50.17%) neurons mainly displayed a multipolar round/oval morphology. Two-color immunofluorescence revealed that only 16.67%, 14.16%, and 39.91% of the CB-, CR-, and PV-IR neurons, respectively, contained GABA. In addition, none of the CB-, CR-, and PV-IR neurons contained NOS.

Conclusions. Our findings indicate that CB-, CR-, and PV-containing neurons in the Mongolian gerbil visual cortex are distributed abundantly and distinctively in specific layers and in a small population of GABAergic neurons but are limited to subpopulations that do not express NOS. These data provide a basis for the potential roles of CBP-containing neurons in the gerbil visual cortex.

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References

  1. Doulberis M, Papaefthymiou A, Polyzos SA, et al. Rodent models of obesity. Minerva Endocrinol. 2020; 45(3): 243–263.
  2. Hickman DL, Johnson J, Vemulapalli TH, et al. Commonly used animal models. Principles of Animal Research. 2017: 117–175.
  3. Julander JG, Siddharthan V. Small-animal models of zika virus. J Infect Dis. 2017; 216(suppl_10): S919–S927.
  4. Mize RR, Jeon CJ, Butler GD, et al. The calcium binding protein calbindin-D 28K reveals subpopulations of projection and interneurons in the cat superior colliculus. J Comp Neurol. 1991; 307(3): 417–436.
  5. Rai V, Moellmer R, Agrawal DK. Clinically relevant experimental rodent models of diabetic foot ulcer. Mol Cell Biochem. 2022; 477(4): 1239–1247.
  6. Yamaoka S, Banadyga L, Bray M, et al. Small animal models for studying filovirus pathogenesis. Curr Top Microbiol Immunol. 2017; 411: 195–227.
  7. Zan Y, Haag JD, Chen KS, et al. Production of knockout rats using ENU mutagenesis and a yeast-based screening assay. Nat Biotechnol. 2003; 21(6): 645–651.
  8. Zhao Y, Qu H, Wang Y, et al. Small rodent models of atherosclerosis. Biomed Pharmacother. 2020; 129: 110426.
  9. Batchelder M, Keller LS, Sauer MB, L WeG, Stevens KA, Wilson RP. editors. The Laboratory Rabbit, Guinea Pig, Hamster, and Other Rodents. Elsevier. Academic Press, Boston 2012: 1131–1155.
  10. Mishra KK, Srivastava S, Aayyagari A, et al. Development of an animal model of Helicobacter pylori (Indian strain) infection. Indian J Gastroenterol. 2019; 38(2): 167–172.
  11. Ayan A, Pekağırbaş M, Aypak S, et al. Dentostomella translucida (Gerbil Pinworm) Infection in Mongolian Gerbil (Meriones Unguiculatus) Schulz and Krepkorgorskaja, 1932. Turkiye Parazitol Derg. 2018; 42(4): 290–293.
  12. Junaid OQ, Vythilingam I, Khaw LT, et al. Effect of Brugia pahangi co-infection with Plasmodium berghei ANKA in gerbils (Meriones unguiculatus). Parasitol Res. 2020; 119(4): 1301–1315.
  13. Rivero FD, Saura A, Prucca CG, et al. Disruption of antigenic variation is crucial for effective parasite vaccine. Nat Med. 2010; 16(5): 551–7, 1p following 557.
  14. Matas D, Doniger T, Sarid S, et al. Sex differences in testosterone reactivity and sensitivity in a non-model gerbil. Gen Comp Endocrinol. 2020; 291: 113418.
  15. Kim H, Park JHa, Shin MC, et al. Fate of astrocytes in the gerbil hippocampus after transient global cerebral ischemia. Int J Mol Sci. 2019; 20(4).
  16. Wolf DC, Carlton WW, Turek JJ. Experimental renal papillary necrosis in the Mongolian gerbil (Meriones unguiculatus). Toxicol Pathol. 1992; 20(3 Pt 1): 341–349.
  17. Gouaref I, Detaille D, Wiernsperger N, et al. The desert gerbil Psammomys obesus as a model for metformin-sensitive nutritional type 2 diabetes to protect hepatocellular metabolic damage: Impact of mitochondrial redox state. PLoS One. 2017; 12(2): e0172053.
  18. Quintar AA, Gonçalves BF, Taboga SR, et al. The mongolian gerbil (Meriones unguiculatus) as a model for inflammation-promoted prostate carcinogenesis. Cell Biol Int. 2017; 41(11): 1234–1238.
  19. Bytyqi AH, Layer PG. Lamina formation in the Mongolian gerbil retina (Meriones unguiculatus). Anat Embryol (Berl). 2005; 209(3): 217–225.
  20. Pan Y, Zhu Q, Xu T, et al. Aggressive behavior and brain neuronal activation in sexually naïve male Mongolian gerbils. Behav Brain Res. 2020; 378: 112276.
  21. Bertorelli R, Adami M, Ongini E. The Mongolian gerbil in experimental epilepsy. Ital J Neurol Sci. 1995; 16(1-2): 101–106.
  22. Dam AM. Estimation of the total number of neurons in different brain areas in the Mongolian gerbil: a model of experimental ischemia. Acta Neurol Scand Suppl. 1992; 137: 34–36.
  23. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 1982; 239(1): 57–69.
  24. Lee CH, Lee TK, Kim DW, et al. Relationship between neuronal damage/death and astrogliosis in the cerebral motor cortex of gerbil models of mild and severe ischemia and reperfusion injury. Int J Mol Sci. 2022; 23(9).
  25. Ahn JiH, Choi JH, Park JHa, et al. Long-Term exercise improves memory deficits via restoration of myelin and microvessel damage, and enhancement of neurogenesis in the aged gerbil hippocampus after ischemic stroke. Neurorehabil Neural Repair. 2016; 30(9): 894–905.
  26. Bäuerle P, von der Behrens W, Kössl M, et al. Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system. J Neurosci. 2011; 31(26): 9708–9722.
  27. Macharadze T, Budinger E, Brosch M, et al. Early sensory loss alters the dendritic branching and spine density of supragranular pyramidal neurons in rodent primary sensory cortices. Front Neural Circuits. 2019; 13: 61.
  28. Cheng S, Fu Y, Zhang Y, et al. Enhancement of de novo sequencing, assembly and annotation of the Mongolian gerbil genome with transcriptome sequencing and assembly from several different tissues. BMC Genomics. 2019; 20(1): 903.
  29. Zorio DAR, Monsma S, Sanes DH, et al. De novo sequencing and initial annotation of the Mongolian gerbil (Meriones unguiculatus) genome. Genomics. 2019; 111(3): 441–449.
  30. Nilsson P, Solbakken MH, Schmid BV, et al. The genome of the great gerbil reveals species-specific duplication of an MHCII gene. Genome Biol Evol. 2020; 12(2): 3832–3849.
  31. Kim EB, Lee SG. The complete mitochondrial genome of the Mongolian gerbil, Meriones unguiculatus (Rodentia: Muridae: Gerbillinae). Mitochondrial DNA A DNA Mapp Seq Anal. 2016; 27(2): 1457–1458.
  32. Li CL, Wang CL, Yan SS, et al. The complete mitochondrial genome of the Tamarisk gerbil, (Rodentia: Muridae). Mitochondrial DNA B Resour. 2017; 1(1): 958–959.
  33. Wang Y, Zhao P, Song Z, et al. Generation of Gene-Knockout Mongolian Gerbils via CRISPR/Cas9 System. Front Bioeng Biotechnol. 2020; 8: 780.
  34. Govardovskii VI, Röhlich P, Szél A, et al. Cones in the retina of the Mongolian gerbil, Meriones unguiculatus: an immunocytochemical and electrophysiological study. Vision Res. 1992; 32(1): 19–27.
  35. Garcia Garrido M, Beck SC, Mühlfriedel R, et al. Towards a quantitative OCT image analysis. PLoS One. 2014; 9(6): e100080.
  36. Huber G, Heynen S, Imsand C, et al. Novel rodent models for macular research. PLoS One. 2010; 5(10): e13403.
  37. Henschke JU, Noesselt T, Scheich H, et al. Possible anatomical pathways for short-latency multisensory integration processes in primary sensory cortices. Brain Struct Funct. 2015; 220(2): 955–977.
  38. Rübsamen R, Gutowski M, Langkau J, et al. Growth of central nervous system auditory and visual nuclei in the postnatal gerbil (Meriones unguiculatus). J Comp Neurol. 1994; 346(2): 289–305.
  39. Ellard CG, Goodale MA, Scorfield DM, et al. Visual cortical lesions abolish the use of motion parallax in the Mongolian gerbil. Exp Brain Res. 1986; 64(3): 599–602.
  40. Mlinar EJ, Goodale MA. Cortical and tectal control of visual orientation in the gerbil: evidence for parallel channels. Exp Brain Res. 1984; 55(1): 33–48.
  41. Hwang IK, Yoo KY, Kim DS, et al. Comparative study on calretinin immunoreactivity in gerbil and rat retina. Anat Histol Embryol. 2005; 34(2): 129–131.
  42. Lee MJ, Lee WT, Jeon CJ. Organization of Neuropeptide Y-Immunoreactive Cells in the Mongolian gerbil () Visual Cortex. Cells. 2021; 10(2).
  43. Baimbridge KG, Celio MR, Rogers JH. Calcium-binding proteins in the nervous system. Trends Neurosci. 1992; 15(8): 303–308.
  44. Kovács-Öller T, Szarka G, Ganczer A, et al. Expression of Ca(2+)-binding buffer proteins in the human and mouse retinal neurons. Int J Mol Sci. 2019; 20(9).
  45. Schäfer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci. 1996; 21(4): 134–140.
  46. Schwaller B. Cytosolic Ca(2+) buffers are inherently ca signal modulators. Cold Spring Harb Perspect Biol. 2020; 12(1).
  47. Kriegsfeld LJ, Mei DF, Yan L, et al. Targeted mutation of the calbindin D28K gene disrupts circadian rhythmicity and entrainment. Eur J Neurosci. 2008; 27(11): 2907–2921.
  48. Stadler F, Schmutz I, Schwaller B, et al. Lack of calbindin-D28k alters response of the murine circadian clock to light. Chronobiol Int. 2010; 27(1): 68–82.
  49. Camp AJ, Wijesinghe R. Calretinin: modulator of neuronal excitability. Int J Biochem Cell Biol. 2009; 41(11): 2118–2121.
  50. Kang KW, Pangeni R, Park J, et al. Selective loss of calretinin-poor cochlear afferent nerve fibers in streptozotocin-induced hyperglycemic mice. J Nanosci Nanotechnol. 2020; 20(9): 5515–5519.
  51. Agetsuma M, Hamm JP, Tao K, et al. Parvalbumin-positive interneurons regulate neuronal ensembles in visual cortex. Cereb Cortex. 2018; 28(5): 1831–1845.
  52. Permyakov EA, Uversky VN, Permyakov SE. Parvalbumin as a pleomorphic protein. Curr Protein Pept Sci. 2017; 18(8): 780–794.
  53. Park HJ, Kong JH, Kang YS, et al. The distribution and morphology of calbindin D28K- and calretinin-immunoreactive neurons in the visual cortex of mouse. Mol Cells. 2002; 14(1): 143–149.
  54. Lee JE, Ahn CH, Lee JY, et al. Nitric oxide synthase and calcium-binding protein-containing neurons in the hamster visual cortex. Mol Cells. 2004; 18(1): 30–39.
  55. Kim HG, Gu YN, Lee KP, et al. Immunocytochemical localization of the calcium-binding proteins calbindin D28K, calretinin, and parvalbumin in bat visual cortex. Histol Histopathol. 2016; 31(3): 317–327.
  56. Gonchar Y, Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex. 1997; 7(4): 347–358.
  57. Park HJ, Lee SN, Lim HR, et al. Calcium-binding proteins calbindin D28K, calretinin, and parvalbumin immunoreactivity in the rabbit visual cortex. Mol Cells. 2000; 10(2): 206–212.
  58. Jeon CJ, Park HJ. Immunocytochemical localization of calcium-binding protein calretinin containing neurons in cat visual cortex. Mol Cells. 1997; 7(6): 721–725.
  59. Yu SH, Lee JY, Jeon CJ. Immunocytochemical localization of calcium-binding proteins, calbindin D28K-, calretinin-, and parvalbumin-containing neurons in the dog visual cortex. Zoolog Sci. 2011; 28(9): 694–702.
  60. Hendrickson AE, Van Brederode JF, Mulligan KA, et al. Development of the calcium-binding protein parvalbumin and calbindin in monkey striate cortex. J Comp Neurol. 1991; 307(4): 626–646.
  61. Meskenaite V. Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol. 1997; 379(1): 113–132.
  62. Glezer II, Hof PR, Morgane PJ. Calretinin-immunoreactive neurons in the primary visual cortex of dolphin and human brains. Brain Res. 1992; 595(2): 181–188.
  63. Leuba G, Saini K. Calcium-binding proteins immunoreactivity in the human subcortical and cortical visual structures. Vis Neurosci. 1996; 13(6): 997–1009.
  64. Picón-Pagès P, Garcia-Buendia J, Muñoz FJ. Functions and dysfunctions of nitric oxide in brain. Biochim Biophys Acta Mol Basis Dis. 2019; 1865(8): 1949–1967.
  65. Lundberg JO, Weitzberg E. Nitric oxide signaling in health and disease. Cell. 2022; 185(16): 2853–2878.
  66. Zhou Li, Zhu DY. Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide. 2009; 20(4): 223–230.
  67. Förstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J. 2012; 33(7): 829–37, 837a.
  68. Kourosh-Arami M, Hosseini N, Mohsenzadegan M, et al. Neurophysiologic implications of neuronal nitric oxide synthase. Rev Neurosci. 2020; 31(6): 617–636.
  69. Choi S, Won JS, Carroll SL, et al. Pathology of nNOS-Expressing GABAergic Neurons in Mouse Model of Alzheimer's Disease. Neuroscience. 2018; 384: 41–53.
  70. Dawson VL, Dawson TM. Nitric oxide in neurodegeneration. Prog Brain Res. 1998; 118: 215–229.
  71. Poon CH, Tsui KaC, Chau SC, et al. Functional roles of neuronal nitric oxide synthase in neurodegenerative diseases and mood disorders. Curr Alzheimer Res. 2021; 18(10): 831–840.
  72. Gonchar Y, Wang Q, Burkhalter A. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. 2007; 1: 3.
  73. Gu YN, Kim HG, Jeon CJ. Localization of nitric oxide synthase-containing neurons in the bat visual cortex and co-localization with calcium-binding proteins. Acta Histochem Cytochem. 2015; 48(4): 125–133.
  74. Kim IB, Oh SJ, Chun MH. Neuronal nitric oxide synthase immunoreactive neurons in the mammalian retina. Microscopy Research and Technique. 2000; 50(2): 112–123, doi: 10.1002/1097-0029(20000715)50:2<112::aid-jemt3>3.0.co;2-s.
  75. Kowiański P, Moryś JM, Wójcik S, et al. Co-localisation of NOS with calcium-binding proteins during the postnatal development of the rat claustrum. Folia Morphol (Warsz). 2003; 62(3): 211–214.
  76. Lee JE, Jeon CJ. Immunocytochemical localization of nitric oxide synthase-containing neurons in mouse and rabbit visual cortex and co-localization with calcium-binding proteins. Mol Cells. 2005; 19(3): 408–417.
  77. Liang Z, Zhang L, Wang X, et al. Distribution and neurochemical features of neuronal nitric oxide synthase-expressing interneurons in the rat dentate gyrus. Brain Res. 2013; 1505: 11–21.
  78. Magno L, Oliveira MG, Mucha M, et al. Multiple embryonic origins of nitric oxide synthase-expressing GABAergic neurons of the neocortex. Front Neural Circuits. 2012; 6: 65.
  79. Mendez-Otero R, Tenorio F, Giraldi-Guimarães A, et al. Patterns of nitric oxide synthase expression in the developing superior colliculus. Rev Bras Biol. 1996; 56(Suppl. 1 pt. 1): 113–122.
  80. Smiley JF, McGinnis JP, Javitt DC. Nitric oxide synthase interneurons in the monkey cerebral cortex are subsets of the somatostatin, neuropeptide Y, and calbindin cells. Brain Res. 2000; 863(1-2): 205–212.
  81. Yousef T, Neubacher U, Eysel UT, et al. Nitric oxide synthase in rat visual cortex: an immunohistochemical study. Brain Res Brain Res Protoc. 2004; 13(1): 57–67.
  82. Daff S. Calmodulin-dependent regulation of mammalian nitric oxide synthase. Biochem Soc Trans. 2003; 31(Pt 3): 502–505.
  83. Piazza M, Guillemette JG, Dieckmann T. Dynamics of nitric oxide synthase-calmodulin interactions at physiological calcium concentrations. Biochemistry. 2015; 54(11): 1989–2000.
  84. Barbaresi P, Mensà E, Lariccia V, et al. Differential distribution of parvalbumin- and calbindin-D28K-immunoreactive neurons in the rat periaqueductal gray matter and their colocalization with enzymes producing nitric oxide. Brain Res Bull. 2013; 99: 48–62.
  85. Bertini G, Peng ZC, Bentivoglio M. The chemical heterogeneity of cortical interneurons: nitric oxide synthase vs. calbindin and parvalbumin immunoreactivity in the rat. Brain Res Bull. 1996; 39(4): 261–266.
  86. Jinno S, Kinukawa N, Kosaka T. Morphometric multivariate analysis of GABAergic neurons containing calretinin and neuronal nitric oxide synthase in the mouse hippocampus. Brain Res. 2001; 900(2): 195–204.
  87. Megías M, Verduga R, Fernández-Viadero C, et al. Neurons co-localizing calretinin immunoreactivity and reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) activity in the hippocampus and dentate gyrus of the rat. Brain Res. 1997; 744(1): 112–120.
  88. Soares-Mota M, Henze I, Mendez-Otero R. Nitric oxide synthase-positive neurons in the rat superior colliculus: colocalization of NOS with NMDAR1 glutamate receptor, GABA, and parvalbumin. J Neurosci Res. 2001; 64(5): 501–507.
  89. Dun NJ, Huang R, Dun SL, et al. Infrequent co-localization of nitric oxide synthase and calcium binding proteins immunoreactivity in rat neocortical neurons. Brain Res. 1994; 666(2): 289–294.
  90. González-Albo MC, Elston GN, DeFelipe J. The human temporal cortex: characterization of neurons expressing nitric oxide synthase, neuropeptides and calcium-binding proteins, and their glutamate receptor subunit profiles. Cereb Cortex. 2001; 11(12): 1170–1181.
  91. Druga R. Neocortical inhibitory system. Folia Biol (Praha). 2009; 55(6): 201–217.
  92. Watanabe M, Maemura K, Kanbara K, et al. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol. 2002; 213: 1–47.
  93. Ichida JM, Rosa M, Casagrande VA. Does the visual system of the flying fox resemble that of primates? The distribution of calcium-binding proteins in the primary visual pathway of Pteropus poliocephalus. J Comp Neurol. 2000; 417(1): 73–87, doi: 10.1002/(sici)1096-9861(20000131)417:1<73::aid-cne6>3.0.co;2-c.
  94. Stichel CC, Singer W, Heizmann CW, et al. Immunohistochemical localization of calcium-binding proteins, parvalbumin and calbindin-D 28k, in the adult and developing visual cortex of cats: a light and electron microscopic study. J Comp Neurol. 1987; 262(4): 563–577.
  95. Goodchild AK, Martin PR. The distribution of calcium-binding proteins in the lateral geniculate nucleus and visual cortex of a New World monkey, the marmoset, Callithrix jacchus. Vis Neurosci. 1998; 15(4): 625–642.
  96. Demeulemeester H, Arckens L, Vandesande F, et al. Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp Brain Res. 1991; 84(3): 538–544.
  97. Park HJ, Hong SK, Kong JH, et al. Localization of calcium-binding protein parvalbumin-immunoreactive neurons in mouse and hamster visual cortex. Mol Cell. 1999; 9(5): 542–547.
  98. Blümcke I, Hof PR, Morrison JH, et al. Distribution of parvalbumin immunoreactivity in the visual cortex of Old World monkeys and humans. J Comp Neurol. 1990; 301(3): 417–432.
  99. Masland RH. Neuronal cell types. Curr Biol. 2004; 14(13): R497–R500.
  100. Wang Y, Toledo-Rodriguez M, Gupta A, et al. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol. 2004; 561(Pt 1): 65–90.
  101. Hayes TL, Lewis DA. Nonphosphorylated neurofilament protein and calbindin immunoreactivity in layer III pyramidal neurons of human neocortex. Cereb Cortex. 1992; 2(1): 56–67.
  102. Gu YN, Lee ES, Jeon CJ. Types and density of calbindin D28k-immunoreactive ganglion cells in mouse retina. Exp Eye Res. 2016; 145: 327–336.
  103. Kwon OJ, Lee ES, Jeon CJ. Density and types of calretinin-containing retinal ganglion cells in rabbit. Neuroscience. 2014; 278: 343–353.
  104. Lee ES, Lee JY, Jeon CJ. Types and density of calretinin-containing retinal ganglion cells in mouse. Neurosci Res. 2010; 66(2): 141–150.
  105. Kim TJ, Jeon CJ. Morphological classification of parvalbumin-containing retinal ganglion cells in mouse: single-cell injection after immunocytochemistry. Invest Ophthalmol Vis Sci. 2006; 47(7): 2757–2764.
  106. Lee ES, Kim TJ, Jeon CJ. Identification of parvalbumin-containing retinal ganglion cells in rabbit. Exp Eye Res. 2013; 110: 113–124.
  107. Lee JY, Choi JS, Ye EA, et al. Organization of calbindin D28K-immunoreactive neurons in the dog superior colliculus. Zoolog Sci. 2007; 24(11): 1103–1114.
  108. Jeon CJ, Pyun JK, Yang HW. Calretinin and calbindin D28K immunoreactivity in the superficial layers of the rabbit superior colliculus. Neuroreport. 1998; 9(17): 3847–3852.
  109. Lee JY, Choi JS, Ahn CH, et al. Calcium-binding protein calretinin immunoreactivity in the dog superior colliculus. Acta Histochem Cytochem. 2006; 39(5): 125–138.
  110. Ellias SA, Stevens JK. The dendritic varicosity: a mechanism for electrically isolating the dendrites of cat retinal amacrine cells? Brain Res. 1980; 196(2): 365–372.
  111. Gu Y, Jukkola P, Wang Q, et al. Polarity of varicosity initiation in central neuron mechanosensation. J Cell Biol. 2017; 216(7): 2179–2199.
  112. Gu C. Rapid and reversible development of axonal varicosities: a new form of neural plasticity. Front Mol Neurosci. 2021; 14: 610857.
  113. Liebert AD, Chow RT, Bicknell BT, et al. Neuroprotective effects against POCD by photobiomodulation: evidence from assembly/disassembly of the cytoskeleton. J Exp Neurosci. 2016; 10: 1–19.
  114. Ralevic V. History of geoff burnstock's research on P2 receptors. Biochem Pharmacol. 2021; 187: 114358.
  115. Zhang ZW, Kang JIl, Vaucher E. Axonal varicosity density as an index of local neuronal interactions. PLoS One. 2011; 6(7): e22543.
  116. Villalobos CA, Wu Q, Lee PH, et al. Parvalbumin and GABA Microcircuits in the Mouse Superior Colliculus. Front Neural Circuits. 2018; 12: 35.
  117. Jeong SJ, Kim HH, Lee WS, et al. Immunocytochemical localization of calbindin D28K, calretinin, and parvalbumin in bat superior colliculus. Acta Histochem Cytochem. 2014; 47(3): 113–123.
  118. Hong SK, Kim JY, Jeon CJ. Immunocytochemical localization of calretinin in the superficial layers of the cat superior colliculus. Neurosci Res. 2002; 44(3): 325–335.
  119. Lee JY, Jeong SJ, Jeon CJ. Parvalbumin-immunoreactive cells in the superior colliculus in dog: distribution, colocalization with GABA, and effect of monocular enucleation. Zoolog Sci. 2014; 31(11): 748–757.
  120. Baden T, Berens P, Franke K, et al. The functional diversity of retinal ganglion cells in the mouse. Nature. 2016; 529(7586): 345–350.
  121. Tran NM, Shekhar K, Whitney IE, et al. Single-cell profiles of retinal ganglion cells differing in resilience to injury reveal neuroprotective genes. Neuron. 2019; 104(6): 1039–1055.e12.
  122. Yan XX, Garey LJ. Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. J Hirnforsch. 1997; 38(2): 165–172.
  123. Wang X, Liu C, Wang X, et al. Density and neurochemical profiles of neuronal nitric oxide synthase-expressing interneuron in the mouse basolateral amygdala. Brain Res. 2017; 1663: 106–113.
  124. Camillo D, Ahmadlou M, Saiepour MH, et al. Visual processing by calretinin expressing inhibitory neurons in mouse primary visual cortex. Sci Rep. 2018; 8(1): 12355.
  125. Shang C, Chen Z, Liu A, et al. Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice. Nat Commun. 2018; 9(1): 1232.
  126. Shang C, Liu Z, Chen Z, et al. BRAIN CIRCUITS. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science. 2015; 348(6242): 1472–1477.
  127. Atallah BV, Bruns W, Carandini M, et al. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron. 2012; 73(1): 159–170.
  128. Bu J, Sathyendra V, Nagykery N, et al. Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol. 2003; 182(1): 220–231.
  129. Wheeler DG, Dixon G, Harper CG. No differences in calcium-binding protein immunoreactivity in the posterior cingulate and visual cortex: schizophrenia and controls. Prog Neuropsychopharmacol Biol Psychiatry. 2006; 30(4): 630–639.
  130. Leuba G, Kraftsik R, Saini K. Quantitative distribution of parvalbumin, calretinin, and calbindin D-28k immunoreactive neurons in the visual cortex of normal and Alzheimer cases. Exp Neurol. 1998; 152(2): 278–291.
  131. Khundakar AA, Hanson PS, Erskine D, et al. Analysis of primary visual cortex in dementia with Lewy bodies indicates GABAergic involvement associated with recurrent complex visual hallucinations. Acta Neuropathol Commun. 2016; 4(1): 66.