Аннотация
Проведено исследование особенностей экспрессии кальций-связывающего белка парвальбумина в пояснично-крестцовом отделе спинного мозга новорождённых и взрослых кошек. В отличие от взрослых животных, у новорожденных иммуномечение к парвальбумину выявлено главным образом в афферентных волокнах, расположенных в дорзальных рогах и медиальной части промежуточного серого вещества. Локализация этих волокон частично повторяет положение ядер Кларка, но не ограничена их классическими границами, охватывая всю протяжённость поясничного отдела и переходя в предполагаемое ядро Штиллинга, расположенное в крестцовом отделе. Таким образом, парвальбумин-иммунопозитивные проприоцептивные волокна у новорожденных, в отличие от взрослых, представляют собой единую систему. Полагаем, что с возрастом, в связи с созреванием и разрастанием элементов поясничного утолщения, связанных, в первую очередь, с локомоторной функцией, происходит перестройка этой непрерывной системы волокон с выделением локальных элементов, таких как ядра Кларка и Штиллинга. Единственными спинальными нейронами, маркированными парвальбумином у новорожденных, являются премоторные интернейроны, расположенные вдоль курватуры пластины IX. Для этих клеток характерно полное или частичное отсутствие экспрессии нейронального белка NeuN, что свидетельствует об особенностях нейрохимического статуса таких нейронов.
Литература
Sherrington CS, Laslett EE (1903) Observations on some spinal reflexes and the interconnection of spinal segments. J Physiol 29:58–96. https://doi.org/10.1113/jphysiol.1903.sp000946
Bosco G, Poppele RE (2001) Proprioception from a spinocerebellar perspective. Physiol Rev 81:539–568. https://doi.org/10.1152/physrev.2001.81.2.539
Niu J, Ding L, Li JJ, Kim H, Liu J, Li H, Moberly A, Badea TC, Duncan ID, Son Y-J, Scherer SS, Luo W (2013) Modality-based organization of ascending somatosensory axons in the direct dorsal column pathway. J Neurosci 33:17691–17709. https://doi.org/10.1523/JNEUROSCI.3429-13.2013
Matsushita M, Yaginuma H (1989) Spinocerebellar projections from spinal border cells in the cat as studied by anterograde transport of wheat germ agglutinin-horseradish peroxidase. J Comp Neurol 288:19–38. https://doi.org/10.1002/cne.902880103
Stecina K, Fedirchuk B, Hultborn H (2013) Information to cerebellum on spinal motor networks mediated by the dorsal spinocerebellar tract. J Physiol 591:5433–5443. https://doi.org/10.1113/jphysiol.2012.249110
Shrestha SS, Bannatyne BA, Jankowska E, Hammar I, Nilsson E, Maxwell DJ (2012) Excitatory inputs to four types of spinocerebellar tract neurons in the cat and the rat thoraco-lumbar spinal cord. J Physiol 590:1737–1755. https://doi.org/10.1113/jphysiol.2011.226852
Clarke JAL (1997) Further researches on the grey substance of the spinal cord. Philos Trans R Soc Lond 149:437–467. https://doi.org/10.1098/rstl.1859.0022
Hogg ID (1944) The development of the nucleus dorsalis (Clarke’s column). J Comp Neurol 81:69–95. https://doi.org/10.1002/cne.900810105
Matsushita M, Hosoya Y (1979) Cells of origin of the spinocerebellar tract in the rat, studied with the method of retrograde transport of horseradish peroxidase. Brain Res 173:185–200. https://doi.org/10.1016/0006-8993(79)90620-6
Molander C, Xu Q, Grant G (1984) The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133–141. https://doi.org/10.1002/cne.902300112
Akopians A, Runyan SA, Phelps PE (2003) Expression of L1 decreases during postnatal development of rat spinal cord. J Comp Neurol 467:375–388. https://doi.org/10.1002/cne.10956
Edgley SA, Grant GM (1991) Inputs to spinocerebellar tract neurones located in Stilling’s nucleus in the sacral segments of the rat spinal cord. J Comp Neurol 305:130–138. https://doi.org/10.1002/cne.903050112
Sengul G, Watson C, Tanaka I, Paxinos G (2012) Atlas of the spinal cord: mouse, rat, rhesus, marmoset, and human. Elsevier Science
Mott F (1888) Microscopical examination of Clarke’s column in man, the monkey, and the dog. J Anat Physiol 22:479–495
Snyder RL, Faull RL, Mehler WR (1978) A comparative study of the neurons of origin of the spinocerebellar afferents in the rat, cat and squirrel monkey based on the retrograde transport of horseradish peroxidase. J Comp Neurol 181:833–852. https://doi.org/10.1002/cne.901810409
Matsushita M, Hosoya Y, Ikeda M (1979) Anatomical organization of the spinocerebellar system in the cat, as studied by retrograde transport of horseradish peroxidase. J Comp Neurol 184:81–106. https://doi.org/10.1002/cne.901840106
Ha H, Liu CN (1968) Cell origin of the ventral spinocerebellar tract. J Comp Neurol 133:185–206. https://doi.org/10.1002/cne.901330204
Xu Q, Grant G (1988) Collateral projections of neurons from the lower part of the spinal cord to anterior and posterior cerebellar termination areas. A retrograde fluorescent double labeling study in the cat. Exp Brain Res 72:562–576. https://doi.org/10.1007/BF00250601
Petras JM, Cummings JF (1977) The origin of spinocerebellar pathways. II. The nucleus centrobasalis of the cervical enlargement and the nucleus dorsalis of the thoracolumbar spinal cord. J Comp Neurol 173:693–716. https://doi.org/10.1002/cne.901730405
Zhang Y, Luo Y, Sasamura K, Sugihara I (2021) Single axonal morphology reveals high heterogeneity in spinocerebellar axons originating from the lumbar spinal cord in the mouse. J Comp Neurol 529:3893–3921. https://doi.org/10.1002/cne.25223
Cooper S, Sherrington CS (1940) Gower’s tract and spinal border cells. Brain 63:123–134. https://doi.org/10.1093/brain/63.2.123
Sprague JM (1953) Spinal border cells and their role in postural mechanism (Schiff-Sherrington phenomenon). J Neurophysiol 16:464–474. https://doi.org/10.1152/jn.1953.16.5.464
Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475. https://doi.org/10.1016/0306-4522(90)90091-h
Ren K, Ruda MA (1994) A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Res Rev 19:163–179. https://doi.org/10.1016/0165-0173(94)90010-8
Clowry GJ, Arnott GA, Clement-Jones M, Fallah Z, Gould S, Wright C (2000) Changing pattern of expression of parvalbumin immunoreactivity during human fetal spinal cord development. J Comp Neurol 423:727–735
Hantman AW, Jessell TM (2010) Clarke’s column neurons as the focus of a corticospinal corollary circuit. Nat Neurosci 13:1233–1239. https://doi.org/10.1038/nn.2637
John A, Brylka H, Wiegreffe C, Simon R, Liu P, Jüttner R, Crenshaw EB, Luyten FP, Jenkins NA, Copeland NG, Birchmeier C, Britsch S (2012) Bcl11a is required for neuronal morphogenesis and sensory circuit formation in dorsal spinal cord development. Dev Camb Engl 139:1831–1841. https://doi.org/10.1242/dev.072850
Dallman MA, Ladle DR (2013) Quantitative analysis of locomotor defects in neonatal mice lacking proprioceptive feedback. Physiol Behav 120:97–105. https://doi.org/10.1016/j.physbeh.2013.07.005
Ni Y, Nawabi H, Liu X, Yang L, Miyamichi K, Tedeschi A, Xu B, Wall NR, Callaway EM, He Z (2014) Characterization of long descending premotor propriospinal neurons in the spinal cord. J Neurosci 34:9404–9417. https://doi.org/10.1523/JNEUROSCI.1771-14.2014
Zhang JH, Morita Y, Hironaka T, Emson PC, Tohyama M (1990) Ontological study of calbindin-D28k-like and parvalbumin-like immunoreactivities in rat spinal cord and dorsal root ganglia. J Comp Neurol 302:715–728. https://doi.org/10.1002/cne.903020404
Clowry GJ, Fallah Z, Arnott G (1997) Developmental expression of parvalbumin by rat lower cervical spinal cord neurones and the effect of early lesions to the motor cortex. Dev Brain Res 102:197–208. https://doi.org/10.1016/s0165-3806(97)00098-9
Veshchitskii A, Shkorbatova P, Merkulyeva N (2022) Neurochemical atlas of the cat spinal cord. Front Neuroanat 16:1034395. https://doi.org/10.3389/fnana.2022.1034395
Veshchitskii A, Musienko P, Merkulyeva N (2023) Distribution of parvalbumin-expressing neuronal populations in the cat cervical and lumbar spinal cord gray matter. J Evol Biochem Physiol 59(4): 1100–1111.
Aoyama M, Hongo T, Kudo N (1988) Sensory input to cells of origin of uncrossed spinocerebellar tract located below Clarke’s column in the cat. J Physiol 398:233–257. https://doi.org/10.1113/jphysiol.1988.sp017040
Matsushita M (1988) Spinocerebellar projections from the lowest lumbar and sacral-caudal segments in the cat, as studied by anterograde transport of wheat germ agglutinin-horseradish peroxidase. J Comp Neurol 274:239–254. https://doi.org/10.1002/cne.902740208
Fu Y, Sengul G, Paxinos G, Watson C (2012) The spinal precerebellar nuclei: calcium binding proteins and gene expression profile in the mouse. Neurosci Lett 518:161–166. https://doi.org/10.1016/j.neulet.2012.05.002
Merkulyeva N, Mikhalkin A, Zykin P (2018) Early postnatal development of the lamination in the lateral geniculate nucleus A-layers in cats. Cell Mol Neurobiol 38:1137–1143. https://doi.org/10.1007/s10571-018-0585-6
Mikhalkin A, Nikitina N, Merkulyeva N (2021) Heterochrony of postnatal accumulation of nonphosphorylated heavy-chain neurofilament by neurons of the cat dorsal lateral geniculate nucleus. J Comp Neurol 529:1430–1441. https://doi.org/10.1002/cne.25028
Merkulyeva N, Mikhalkin A (2024) Transient expression of heavy-chain neurofilaments in the perigeniculate nucleus of cats. Brain Struct Funct. https://doi.org/10.1007/s00429-023-02752-6
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019
Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Dev Camb Engl 116:201–211. https://doi.org/10.1242/dev.116.1.201
Rexed B (1954) A cytoarchitectonic atlas of the spinal cord in the cat. J Comp Neurol 100:297–379. https://doi.org/10.1002/cne.901000205
Réthelyi M, Szentágothai J (1973) Distribution and connections of afferent fibres in the spinal cord. In: Iggo A (ed) Somatosensory System. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 207–252
Chakrabarty S, Shulman B, Martin JH (2009) Activity-dependent codevelopment of the corticospinal system and target interneurons in the cervical spinal cord. J Neurosci 29:8816–8827. https://doi.org/10.1523/JNEUROSCI.0735-09.2009
Knyihár-Csillik E, Rakic P, Csillik B (1999) Illusive transience of parvalbumin expression during embryonic development of the primate spinal cord. Int J Dev Neurosci 17:79–97. https://doi.org/10.1016/s0736-5748(98)00090-2
Siembab VC, Smith CA, Zagoraiou L, Berrocal MC, Mentis GZ, Alvarez FJ (2010) Target selection of proprioceptive and motor axon synapses on neonatal V1-derived Ia inhibitory interneurons and Renshaw cells. J Comp Neurol 518:4675–4701. https://doi.org/10.1002/cne.22441
Floyd TL, Dai Y, Ladle DR (2018) Characterization of calbindin D28k expressing interneurons in the ventral horn of the mouse spinal cord. Dev Dyn 247:185–193. https://doi.org/10.1002/dvdy.24601
Alekseeva OS, Gusel’nikova VV, Beznin GV, Korzhevskii DE (2015) Prospects for the application of the NeuN nuclear protein as a marker of the functional state of nerve cells in vertebrates. J Evol Biochem Physiol 51(5): 357–369.
Shneider NA, Brown MN, Smith CA, Pickel J, Alvarez FJ (2009) Gamma motor neurons express distinct genetic markers at birth and require muscle spindle-derived GDNF for postnatal survival. Neural Develop 4:42. https://doi.org/10.1186/1749-8104-4-42
Taylor A, Ellaway PH, Durbaba R (1999) Why are there three types of intrafusal muscle fibers? Prog Brain Res 123:121–131. https://doi.org/10.1016/s0079-6123(08)62849-6
Merkulyeva N, Mikhalkin A, Nikitina N (2020) Characteristics of the neurochemical state of neurons in the mesencephalic nucleus of the trigeminal nerve in cats. Neurosci Behav Physiol 50(4): 511–515.