Аннотация
Парвальбумин – классический маркер интернейронных популяций центральной нервной системы. При анализе шейных и поясничных отделов спинного мозга кошки (Felis catus) в большинстве пластин серого вещества были выявлены как единичные парвальбумин-иммунопозитивные нейроны, так и целые популяции, имеющие строгую ламинарную/ядерную локализацию. Наиболее выраженные скопления нейронов локализованы в медиальной части пластин V-VI и в пластине VII сегментов шейного и поясничного утолщения. Полагаем, что первое скопление в сегментах C4-C8 и L4-L7 участвует в механизмах модуляции локомоторной активности посредством конвергенции кожной и проприоцептивной афферентации от конечностей. Скопления нейронов в пластине VII представляют собой Ia-интернейроны и интернейроны Реншоу, участвующие в процессах торможения мотонейронов. Менее выраженными популяциями парвальбумин-иммунопозитивных нейронов являются: скопления в пластине III, предположительно связанные с регуляцией кожной чувствительности; скопления в пластине VIII, локализация и морфология которых сходны с нейронами, формирующими комиссуральные и проприоспинальные связи и участвующие в модуляции активности мотонейронов. Иммунопозитивные нейроны также выявлены в прецеребеллярных ядрах: центральном цервикальном и ядре Кларка; в отличие от доминирующих популяций проекционных клеток этих ядер, выявленные нейроны предположительно относятся к интернейронам. Единичные клетки представлены в пластине I сегментов L6-L7, а также в пластинах II, IV, X всех исследованных сегментов. На настоящий момент это самое полное описание популяций парвальбумин-иммунопозитивных нейронов спинного мозга хищных.
Литература
Andressen C, Blümcke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181–208. https://doi.org/10.1007/BF00318606
Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C (1998) Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: A perspective on the contributions of apoptosis and necrosis. Brain Res Bull 46:281–309. https://doi.org/10.1016/s0361-9230(98)00024-0
Leist M, Nicotera P (1998) Apoptosis, excitotoxicity, and neuropathology. Exp Cell Res 239:183–201. https://doi.org/10.1006/excr.1997.4026
Deuticke HJ (1934) Über die sedimentationskonstante von muskelproteinen. Hoppe-Seyler´s Z Für Physiol Chem 224:216–228. https://doi.org/10.1515/bchm2.1934.224.5-6.216
Celio MR, Heizmann CW (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293:300–302. https://doi.org/10.1038/293300a0
Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159–170. https://doi.org/10.1016/j.neuron.2011.12.013
Ince P, Stout N, Shaw P, Slade J, Hunziker W, Heizmann CW, Baimbridge KG (1993) Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathol Appl Neurobiol 19:291–299. https://doi.org/10.1111/j.1365-2990.1993.tb00443.x
Jones EG (2009) Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann N Y Acad Sci 1157:10–23. https://doi.org/10.1111/j.1749-6632.2009.04534.x
Arber S, Ladle DR, Lin JH, Frank E, Jessell TM (2000) ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101:485–498. https://doi.org/10.1016/s0092-8674(00)80859-4
Marsala J, Lukácová N, Kolesár D, Sulla I, Gálik J, Marsala M (2007) The distribution of primary nitric oxide synthase- and parvalbumin- immunoreactive afferents in the dorsal funiculus of the lumbosacral spinal cord in a dog. Cell Mol Neurobiol 27:475–504. https://doi.org/10.1007/s10571-007-9140-6
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 Brain Res Rev 19:163–179. https://doi.org/10.1016/0165-0173(94)90010-8
Ganugula R, Deng M, Arora M, Pan H-L, Kumar MNVR (2019) Polyester nanoparticle encapsulation mitigates paclitaxel-induced peripheral neuropathy. ACS Chem Neurosci 10:1801–1812. https://doi.org/10.1021/acschemneuro.8b00703
Ozeri-Engelhard N, Gradwell MA, Laflamme OD, Upadhyay A, Aoki A, Shrier T, Gandhi M, Gonzalez M, Eisdorfer JT, Abbas- Zadeh G, Yusuf N, Imtiaz Z, Alomary SA, Katz J, Haas M, Hernandez Y, Akay T, Abraira V (2022) Sensory convergence and inhibitory divergence: deep dorsal horn inhibitory interneurons modulate the timing and magnitude of limb coordination during locomotion. Neuroscience
Alvarez FJ, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ, Goulding M (2005) Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 493:177–192. https://doi.org/10.1002/cne.20711
Anelli R, Heckman CJ (2005) The calcium binding proteins calbindin, parvalbumin, and calretinin have specific patterns of expression in the gray matter of cat spinal cord. J Neurocytol 34:369–385. https://doi.org/10.1007/s11068-006-8724-2
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
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
Merkulyeva NS, Mikhalkin AA, Nikitina NI (2020) Characteristics of the neurochemical state of neurons in the mesencephalic nucleus of the trigeminal nerve in cats. Neurosci Behav Physiol 50:511–515. https://doi.org/10.1007/s11055-020-00927-w
Mikhalkin AA, Merkulyeva NS (2021) Peculiarities of age-related dynamics of neurons in the cat lateral geniculate nucleus as revealed in frontal versus sagittal slices. J Evol Biochem Physiol 57:1001–1007. https://doi.org/10.1134/S0022093021050021
Shkorbatova PY, Lyakhovetskii VA, Merkulyeva NS, Veshchitskii AA, Bazhenova EY, Laurens J, Pavlova NV, Musienko PE (2019) Prediction algorithm of the cat spinal segments lengths and positions in relation to the vertebrae. Anat Rec Hoboken NJ 2007 302:1628–1637. https://doi.org/10.1002/ar.24054
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
Craig AD, Krout K, Andrew D (2001) Quantitative response characteristics of thermoreceptive and nociceptive lamina I spinothalamic neurons in the cat. J Neurophysiol 86:1459–1480. https://doi.org/10.1152/jn.2001.86.3.1459
Porseva VV, Emanuilov AI, Maslyukov PM (2020) Subpopulations of calbindin-, calretinin-, and parvalbumin-immunoreactive interneurons in the dorsal horn of the spinal cord in female C57BL/6 mice. Neurosci Behav Physiol 50:961–965. https://doi.org/10.1007/s11055-020-00991-2
Antal M, Freund TF, Polgár E (1990) Calcium-binding proteins, parvalbumin- and calbindin-D 28k-immunoreactive neurons in the rat spinal cord and dorsal root ganglia: a light and electron microscopic study. J Comp Neurol 295:467–484. https://doi.org/10.1002/cne.902950310
Lukáčová N, Kisucká A, Pavel J, Hricová L, Kucharíková A, Gálik J, Maršala M, Langfort J, Chalimoniuk M (2012) Spinal cord transection modifies neuronal nitric oxide synthase expression in medullar reticular nuclei and in the spinal cord and increases parvalbumin immunopositivity in motoneurons below the site of injury in experimental rabbits. Acta Histochem 114:518–524. https://doi.org/10.1016/j.acthis.2011.09.007
Torres-da-Silva KR, Da Silva AV, Barioni NO, Tessarin GWL, De Oliveira JA, Ervolino E, Horta-Junior J a. C, Casatti CA (2016) Neurochemistry study of spinal cord in non-human primate (Sapajus spp.). Eur J Histochem EJH 60:2623. https://doi.org/10.4081/ejh.2016.2623
Hughes DI, Sikander S, Kinnon CM, Boyle KA, Watanabe M, Callister RJ, Graham BA (2012) Morphological, neurochemical and electrophysiological features of parvalbumin-expressing cells: a likely source of axo-axonic inputs in the mouse spinal dorsal horn. J Physiol 590:3927–3951. https://doi.org/10.1113/jphysiol.2012.235655
Laing I, Todd AJ, Heizmann CW, Schmidt HH (1994) Subpopulations of GABAergic neurons in laminae I-III of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin. Neuroscience 61:123–132. https://doi.org/10.1016/0306-4522(94)90065-5
Stachowski NJ, Dougherty KJ (2021) Spinal inhibitory interneurons: gatekeepers of sensorimotor pathways. Int J Mol Sci 22:2667. https://doi.org/10.3390/ijms22052667
Yamamoto T, Carr PA, Baimbridge KG, Nagy JI (1989) Parvalbumin- and calbindin D28k-immunoreactive neurons in the superficial layers of the spinal cord dorsal horn of rat. Brain Res Bull 23:493–508. https://doi.org/10.1016/0361-9230(89)90195-0
Tiong SYX, Polgár E, van Kralingen JC, Watanabe M, Todd AJ (2011) Galanin-immunoreactivity identifies a distinct population of inhibitory interneurons in laminae I-III of the rat spinal cord. Mol Pain 7:36. https://doi.org/10.1186/1744-8069-7-36
Molgaard S, Ulrichsen M, Boggild S, Holm M-L, Vaegter C, Nyengaard J, Glerup S (2014) Immunofluorescent visualization of mouse interneuron subtypes. F1000Research 3:242. https://doi.org/10.12688/f1000research.5349.2
Antal M, Polgár E, Chalmers J, Minson JB, Llewellyn-Smith I, Heizmann CW, Somogyi P (1991) Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. J Comp Neurol 314:114–124. https://doi.org/10.1002/cne.903140111
Kim YJ, Moon DE, Kim OS, Lee YK (1995) Morphology and topographic distribution of calbindinergic and parvalbuminergic neurons in the rabbit cervical cord. Korean J Anesthesiol 29:329. https://doi.org/10.4097/kjae.1995.29.3.329
Rausell E, Bae CS, Viñuela A, Huntley GW, Jones EG (1992) Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations. J Neurosci Off J Soc Neurosci 12:4088–4111. https://doi.org/10.1523/JNEUROSCI.12-10-04088.1992
Satoh J, Tabira T, Sano M, Nakayama H, Tateishi J (1991) Parvalbumin-immunoreactive neurons in the human central nervous system are decreased in Alzheimer’s disease. Acta Neuropathol (Berl) 81:388–395. https://doi.org/10.1007/BF00293459
Dougherty KJ, Sawchuk MA, Hochman S (2009) Phenotypic diversity and expression of GABAergic inhibitory interneurons during postnatal development in lumbar spinal cord of glutamic acid decarboxylase 67-green fluorescent protein mice. Neuroscience 163:909–919. https://doi.org/10.1016/j.neuroscience.2009.06.055
Gradwell MA, Boyle KA, Browne TJ, Bell AM, Leonardo J, Peralta Reyes FS, Dickie AC, Smith KM, Callister RJ, Dayas CV, Hughes DI, Graham BA (2022) Diversity of inhibitory and excitatory parvalbumin interneuron circuits in the dorsal horn. Pain 163:e432–e452. https://doi.org/10.1097/j.pain.0000000000002422
Petitjean H, Pawlowski SA, Fraine SL, Sharif B, Hamad D, Fatima T, Berg J, Brown CM, Jan L-Y, Ribeiro-da-Silva A, Braz JM, Basbaum AI, Sharif-Naeini R (2015) Dorsal horn parvalbumin neurons are gate-keepers of touch-evoked pain after nerve injury. Cell Rep 13:1246–1257. https://doi.org/10.1016/j.celrep.2015.09.080
Cui L, Miao X, Liang L, Abdus-Saboor I, Olson W, Fleming MS, Ma M, Tao Y-X, Luo W (2016) Identification of early RET+ deep dorsal spinal сord interneurons in gating pain. Neuron 91:1413. https://doi.org/10.1016/j.neuron.2016.09.010
Huang J, Chen J, Wang W, Wang W, Koshimizu Y, Wei Y-Y, Kaneko T, Li Y-Q, Wu S-X (2010) Neurochemical properties of enkephalinergic neurons in lumbar spinal dorsal horn revealed by preproenkephalin-green fluorescent protein transgenic mice. J Neurochem 113:1555–1564. https://doi.org/10.1111/j.1471-4159.2010.06715.x
Stewart W, Maxwell DJ (2003) Distribution of and organisation of dorsal horn neuronal cell bodies that possess the muscarinic m2 acetylcholine receptor. Neuroscience 119:121–135. https://doi.org/10.1016/s0306-4522(03)00116-7
Ritz LA, Greenspan JD (1985) Morphological features of lamina V neurons receiving nociceptive input in cat sacrocaudal spinal cord. J Comp Neurol 238:440–452. https://doi.org/10.1002/cne.902380408
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
Hirai N, Hongo T, Sasaki S, Yoshida K (1979) The neck and labyrinthine influences on cervical spinocerebellar tract neurones of the central cervical nucleus in the cat. Prog Brain Res 50:529–536. https://doi.org/10.1016/S0079-6123(08)60851-1
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
McKelvey-Briggs DK, Saint-Cyr JA, Spence SJ, Partlow GD (1989) A reinvestigation of the spinovestibular projection in the cat using axonal transport techniques. Anat Embryol (Berl) 180:281–291. https://doi.org/10.1007/BF00315886
Sato H, Ohkawa T, Uchino Y, Wilson VJ (1997) Excitatory connections between neurons of the central cervical nucleus and vestibular neurons in the cat. Exp Brain Res 115:381–386. https://doi.org/10.1007/pl00005708
Tan S, Faull RLM, Curtis MA (2023) The tracts, cytoarchitecture, and neurochemistry of the spinal cord. Anat Rec Hoboken NJ 2007 306:777–819. https://doi.org/10.1002/ar.25079
Verburgh CA, Kuypers HG, Voogd J, Stevens HP (1989) Spinocerebellar neurons and propriospinal neurons in the cervical spinal cord: a fluorescent double-labeling study in the rat and the cat. Exp Brain Res 75:73–82. https://doi.org/10.1007/BF00248532
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
Chen S, Yang G, Zhu Y, Liu Z, Wang W, Wei J, Li K, Wu J, Chen Z, Li Y, Mu S, OuYang L, Lei W (2016) A comparative study of three interneuron types in the rat spinal cord. PloS One 11:e0162969. https://doi.org/10.1371/journal.pone.0162969
Fahandejsaadi A, Leung E, Rahaii R, Bu J, Geula C (2004) Calbindin-D28K, parvalbumin and calretinin in primate lower motor neurons. Neuroreport 15:443–448. https://doi.org/10.1097/00001756-200403010-00012
Boehme CC (1968) The neural structure of Clarke’s nucleus of the spinal cord. J Comp Neurol 132:445–461. https://doi.org/10.1002/cne.901320306
Loewy AD (1970) A study of neuronal types in Clarke’s column in the adult cat. J Comp Neurol 139:53–79. https://doi.org/10.1002/cne.901390104
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
Han Q, Feng J, Qu Y, Ding Y, Wang M, So K-F, Wu W, Zhou L (2013) Spinal cord maturation and locomotion in mice with an isolated cortex. Neuroscience 253:235–244. https://doi.org/10.1016/j.neuroscience.2013.08.057
Benito-Gonzalez A, Alvarez FJ (2012) Renshaw cells and Ia inhibitory interneurons are generated at different times from p1 progenitors and differentiate shortly after exiting the cell cycle. J Neurosci Off J Soc Neurosci 32:1156–1170. https://doi.org/10.1523/JNEUROSCI.3630-12.2012
Jankowska E (2013) Spinal Interneurons. In: Pfaff DW (ed) Neuroscience in the 21st Century. Springer New York, New York, NY, pp 1063–1099
Hughes DI, Boyle KA, Kinnon CM, Bilsland C, Quayle JA, Callister RJ, Graham BA (2013) HCN4 subunit expression in fast-spiking interneurons of the rat spinal cord and hippocampus. Neuroscience 237:7–18. https://doi.org/10.1016/j.neuroscience.2013.01.028
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
Renshaw B (1946) Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 9:191–204. https://doi.org/10.1152/jn.1946.9.3.191
Matsuyama K, Kobayashi S, Aoki M (2006) Projection patterns of lamina VIII commissural neurons in the lumbar spinal cord of the adult cat: an anterograde neural tracing study. Neuroscience 140:203–218. https://doi.org/10.1016/j.neuroscience.2006.02.005
Lu J, Sherman D, Devor M, Saper CB (2006) A putative flip-flop switch for control of REM sleep. Nature 441:589–594. https://doi.org/10.1038/nature04767
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
Kucharíková A, Schreiberová A, Závodská M, Gedrová Š, Hricová Ľ, Pavel J, Gálik J, Maršala M, Lukáčová N (2014) Repeated Baclofen treatment ameliorates motor dysfunction, suppresses reflex activity and decreases the expression of signaling proteins in reticular nuclei and lumbar motoneurons after spinal trauma in rats. Acta Histochem 116:344–353. https://doi.org/10.1016/j.acthis.2013.08.012
Solbach S, Celio MR (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol (Berl) 184:103–124. https://doi.org/10.1007/BF00942742