Early Postnatal Development of the Lamination in the Lateral Geniculate Nucleus A-Layers in Cats

Abstract

The early postnatal development of the A-layers of the dorsal lateral geniculate nucleus (LGNd) was investigated in kittens aged 0–34 days by immunohistochemistry for the selective marker for neuronal differentiation (NeuN protein) and parvalbumin. We report two new facts about the LGNd development. First, there is a transient stratification of NeuN labelling in layer A, and to a lesser extent in layer A1, in kittens aged 0 and 4 days. Second, a transient population of large cells that are located between the LGNd A-layers (interlaminar cells) showed high expression levels of both NeuN and parvalbumin. These neurons possessed both the morphological and immunohistochemical features, similar to cells in the neighbouring perigeniculate nucleus. Both NeuN-stratification and double-stained interlaminar cells gradually disappeared during the second postnatal week, and almost completely vanished by the opening of the critical period. We discuss a possible linkage between these observed transitory networks and the ON-/OFF- and X-/Y-cells development and propose that the data obtained reflect the functioning of the early environmentally independent geniculate networks.

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References

  1. Alekseeva OS, Gusel VV, Beznin GV, Korzhevskii DE (2015) Prospects for the application of NeuN nuclear protein as a marker of the functional state of nerve cells in vertebrates. J Evol Biochem Physiol 51:357–369. https://doi.org/10.1134/S0022093015050014

    Article  CAS  Google Scholar 

  2. Bickford ME, Wei H, Eisenback MA et al (2008) Synaptic organization of thalamocortical axon collaterals in the perigeniculate nucleus and dorsal lateral geniculate nucleus. J Comp Neurol 508:264–285. https://doi.org/10.1002/cne.21671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Bowling DB, Wieniawa-Narkiewicz E (1986) The distribution of on- and off-centre X- and Y-like cells in the A layers of the cat’s lateral geniculate nucleus. J Physiol 375:561–572. https://doi.org/10.1113/jphysiol.1986.sp016133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Burnat K (2015) Are visual peripheries forever young? Neural Plast 2015:1–13. https://doi.org/10.1155/2015/307929

    Article  Google Scholar 

  5. Chalupa LM (2007) A reassessment of the role of activity in the formation of eye-specific retinogeniculate projections. Brain Res Rev 55:228–236. https://doi.org/10.1016/j.brainresrev.2007.03.003

    Article  PubMed  Google Scholar 

  6. Chapman B (2000) Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287:2479–2482. https://doi.org/10.1126/science.287.5462.2479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Crair MC, Gillespie DC, Stryker MP (1998) The role of visual experience in the development of columns in cat visual cortex. Science 279:566–570. https://doi.org/10.1126/science.279.5350.566

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Crowley JC, Katz LC (2002) Ocular dominance development revisited. Curr Opin Neurobiol 12:104–109. https://doi.org/10.1016/S0959-4388(02)00297-0

    Article  PubMed  CAS  Google Scholar 

  9. Cucchiaro JB, Uhlrich DJ, Sherman SM (1991) Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. J Comp Neurol 310:316–336. https://doi.org/10.1002/cne.903100304

    Article  PubMed  CAS  Google Scholar 

  10. Daniels JD, Pettigrew JD, Norman JL (1978) Development of single-neuron responses in kitten’s lateral geniculate nucleus. J Neurophysiol 41:1373–1393. https://doi.org/10.1152/jn.1978.41.6.1373

    Article  PubMed  CAS  Google Scholar 

  11. Demeulemeester H, Arckens L, Vandesande F et al (1991) Calcium binding proteins as molecular markers for cat geniculate neurons. Exp Brain Res 83:513–520. https://doi.org/10.1007/BF00229828

    Article  PubMed  CAS  Google Scholar 

  12. Enroth-cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517–552. https://doi.org/10.1113/jphysiol.1966.sp008107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Fitzgibbon T (2002) Organization of reciprocal connections between the perigeniculate nucleus and dorsal lateral geniculate nucleus in the cat: a transneuronal transport study. Vis Neurosci 19:511–520. https://doi.org/10.1017/S0952523802194120

    Article  PubMed  CAS  Google Scholar 

  14. Fukuda Y, Stone J (1974) Retinal distribution and central projections of Y-, X-, and W-cells of the cat’s retina. J Neurophysiol 37:749–772. https://doi.org/10.1152/jn.1974.37.4.749

    Article  PubMed  CAS  Google Scholar 

  15. Garraghty PE, Roe A, Sur M (1998) Specification of retinogeniculate X and Y axon arbors in cats: fundamental differences in developmental programs. Brain Res Dev Brain Res 107:227–231. https://doi.org/10.1016/S0165-3806(97)00223-X

    Article  PubMed  CAS  Google Scholar 

  16. Hockfield S, Sur M (1990) Monoclonal antibody Cat-301 identifies Y-cells in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 300:320–330. https://doi.org/10.1002/cne.903000305

    Article  PubMed  CAS  Google Scholar 

  17. Hubel DH, Wiesel TN (1961) Integrative action in the cat’s lateral geniculate body. J Physiol 155:385–398. https://doi.org/10.1113/jphysiol.1961.sp006635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Huberman AD, Dehay C, Berland M et al (2005) Early and rapid targeting of eye-specific axonal projections to the dorsal lateral geniculate nucleus in the fetal macaque. J Neurosci 25:4014–4023. https://doi.org/10.1523/JNEUROSCI.4292-04.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Humphrey AL, Weller RE (1988) Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat. J Comp Neurol 268:448–468. https://doi.org/10.1002/cne.902680312

    Article  PubMed  CAS  Google Scholar 

  20. Kalil R (1978) Development of the dorsal lateral geniculate nucleus in the cat. J Comp Neurol 182:265–291. https://doi.org/10.1002/cne.901820206

    Article  PubMed  CAS  Google Scholar 

  21. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447–452. https://doi.org/10.1016/j.tins.2004.05.013

    Article  PubMed  CAS  Google Scholar 

  22. Kim KK, Adelstein RS, Kawamoto S (2009) Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284:31052–31061. https://doi.org/10.1074/jbc.M109.052969

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Lavezzi AM, Corna MF, Matturri L (2013) Neuronal nuclear antigen (NeuN): a useful marker of neuronal immaturity in sudden unexplained perinatal death. J Neurol Sci 329:45–50. https://doi.org/10.1016/j.jns.2013.03.012

    Article  PubMed  CAS  Google Scholar 

  24. Lee I, Kim J, Lee C (1999) Anatomical characteristics and three-dimensional model of the dog dorsal lateral geniculate body. Anat Rec 256:29–39

    Article  PubMed  CAS  Google Scholar 

  25. Linden DC, Guillery RW, Cucchiaro JB (1981) The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J Comp Neurol 203:189–211. https://doi.org/10.1002/cne.902030204

    Article  PubMed  CAS  Google Scholar 

  26. Mangel SC, Wilson JR, Sherman SM (1983) Development of neuronal response properties in the cat dorsal lateral geniculate nucleus during monocular deprivation. J Neurophysiol 50:240–264. https://doi.org/10.1152/jn.1983.50.1.240

    Article  PubMed  CAS  Google Scholar 

  27. Mastronarde DN (1987) Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. J Neurophysiol 57:357–380. https://doi.org/10.1152/jn.1987.57.2.357

    Article  PubMed  CAS  Google Scholar 

  28. Mastronarde DN, Humphrey AL, Saul AB (1991) Lagged Y cells in the cat lateral geniculate nucleus. Vis Neurosci 7:191–200. https://doi.org/10.1017/S0952523800004028

    Article  PubMed  CAS  Google Scholar 

  29. Merkulyeva N, Veshchitskii A, Makarov F et al (2016) Distribution of 28 kDa calbindin-immunopositive neurons in the cat spinal cord. Front Neuroanat 9:166. https://doi.org/10.3389/fnana.2015.00166

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Mitzdorf U, Singer W (1977) Laminar segregation of afferents to lateral geniculate nucleus of the cat: an analysis of current source density. J Neurophysiol 40:1227–1244. https://doi.org/10.1152/jn.1977.40.6.1227

    Article  PubMed  CAS  Google Scholar 

  31. Montero VM (1989) The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light and electron microscopic observations. Exp Brain Res 75:497–512. https://doi.org/10.1007/BF00249901

    PubMed  CAS  Article  Google Scholar 

  32. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–211

    PubMed  CAS  Google Scholar 

  33. Norman JL, Pettigrew JD, Daniels JD (1977) Early development of X-cells in kitten lateral geniculate nucleus. Science 198:202–204. https://doi.org/10.1126/science.905824

    Article  PubMed  CAS  Google Scholar 

  34. Sanchez-Vives MV, Bal T, Kim U et al (1996) Are the interlaminar zones of the ferret dorsal lateral geniculate nucleus actually part of the perigeniculate nucleus? J Neurosci 16:5923–5941. https://doi.org/10.1523/JNEUROSCI.16-19-05923.1996

    Article  PubMed  CAS  Google Scholar 

  35. Sanderson KJ (1974) Lamination of the dorsal lateral geniculate nucleus in carnivores of the weasel (Mustelidae), raccoon (Procyonidae) and fox (Canidae) families. J Comp Neurol 153:238–266. https://doi.org/10.1002/cne.901530303

    Article  PubMed  CAS  Google Scholar 

  36. Sarnat HB, Nochlin D, Born DE (1998) Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev 20:88–94. https://doi.org/10.1016/S0387-7604(97)00111-3

    Article  PubMed  CAS  Google Scholar 

  37. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019

    Article  PubMed  CAS  Google Scholar 

  38. Shatz CJ (1983) The prenatal development of the cat’s retinogeniculate pathway. J Neurosci 3:482–499. https://doi.org/10.1523/JNEUROSCI.03-03-00482.1983

    Article  PubMed  CAS  Google Scholar 

  39. Sherman SM (1985) Development of retinal projections to the cat’s lateral geniculate nucleus. Trends Neurosci 8:350–355. https://doi.org/10.1016/0166-2236(85)90121-3

    Article  Google Scholar 

  40. Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci 357:1695–1708. https://doi.org/10.1098/rstb.2002.1161

    Article  PubMed  PubMed Central  Google Scholar 

  41. Sherman SM, Koch C (1986) The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res 63:1–20. https://doi.org/10.1007/BF00235642

    Article  PubMed  CAS  Google Scholar 

  42. Sherman SM, Spear PD (1982) Organization of visual pathways in normal and visually deprived cats. Physiol Rev 62:738–855. https://doi.org/10.1152/physrev.1982.62.2.738

    Article  PubMed  CAS  Google Scholar 

  43. So YT, Shapley R (1979) Spatial properties of X and Y cells in the lateral geniculate nucleus of the cat and conduction veolcities of their inputs. Exp Brain Res 36:533–550. https://doi.org/10.1007/BF00238521

    Article  PubMed  CAS  Google Scholar 

  44. Speer CM, Mikula S, Huberman AD, Chapman B (2010) The developmental remodeling of eye-specific afferents in the ferret dorsal lateral geniculate nucleus. Anat Rec 293:1–24. https://doi.org/10.1002/ar.21001

    Article  Google Scholar 

  45. Sretavan DW, Shatz CJ (1986) Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat’s lateral geniculate nucleus. J Neurosci 6:234–251. https://doi.org/10.1523/JNEUROSCI.06-01-00234.1986

    Article  PubMed  CAS  Google Scholar 

  46. Stryker MP, Zahs KR (1983) On and off sublaminae in the lateral geniculate nucleus of the ferret. J Neurosci 3:1943–1951. https://doi.org/10.1523/JNEUROSCI.03-10-01943.1983

    Article  PubMed  CAS  Google Scholar 

  47. Sur M (1988) Development and plasticity of retinal X and Y axon terminations in the cat’s lateral geniculate nucleus. Brain Behav Evol 31:243–251. https://doi.org/10.1159/000116592

    Article  PubMed  CAS  Google Scholar 

  48. Uhlrich DJ, Cucchiaro JB, Humphrey AL, Sherman SM (1991) Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus. J Neurophysiol 65:1528–1541. https://doi.org/10.1152/jn.1991.65.6.1528

    Article  PubMed  CAS  Google Scholar 

  49. Watanabe M, Fukuda Y (2002) Survival and axonal regeneration of retinal ganglion cells in adult cats. Prog Retin Eye Res 21:529–553. https://doi.org/10.1016/S1350-9462(02)00037-X

    Article  PubMed  Google Scholar 

  50. Weyer A, Schilling K (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 73:400–409. https://doi.org/10.1002/jnr.10655

    Article  PubMed  CAS  Google Scholar 

  51. Wilson JR, Friedlander MJ, Sherman SM (1984) Fine structural morphology of identified X- and Y-cells in the cat’s lateral geniculate nucleus. Proc R Soc London Ser B 221:411–436. https://doi.org/10.1098/rspb.1984.0042

    Article  CAS  Google Scholar 

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Acknowledgements

The study was supported by the Russian Foundation for Basic Research (RFBR Grant No. 16-04-01791). The authors thank the Centre for Molecular and Cell Technologies, Research Park, Saint Petersburg State University, for supporting this research. The authors also thank Nikitina Nina for animal care and Schkorbatova Polina for help with immunostaining.

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All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: MN. Acquisition of data: MN, MA. Analysis and interpretation of data: MN, MA. Drafting of the manuscript: MN, MA. Critical revision of the manuscript for important intellectual content: MN, MA. Statistical analysis: MN, MA. Obtained funding: MN, MA. Administrative, technical, and material support: MN, MA, ZP. Study supervision: MN.

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Correspondence to Natalia Merkulyeva.

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Merkulyeva, N., Mikhalkin, A. & Zykin, P. Early Postnatal Development of the Lamination in the Lateral Geniculate Nucleus A-Layers in Cats. Cell Mol Neurobiol 38, 1137–1143 (2018). https://doi.org/10.1007/s10571-018-0585-6

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Keywords

  • Lateral geniculate nucleus
  • Cat
  • Postnatal development
  • NeuN
  • Parvalbumin