Neuronal degeneration in the dorsal lateral geniculate nucleus following lesions of primary visual cortex: comparison of young adult and geriatric marmoset monkeys

Abstract

Neuronal loss in the lateral geniculate nucleus (LGN) is a consequence of lesions of the primary visual cortex (V1). Despite the importance of this phenomenon in understanding the residual capacities of the primate visual system following V1 damage, few quantitative studies are available, and the effect of age at the time of lesion remains unknown. We compared the volume, neuronal number, and neuronal density in the LGN, 6–21 months after unilateral V1 lesions in marmoset monkeys. Stereological sampling techniques and neuronal nuclei (NeuN) staining were used to assess the effects of similar-sized lesions in adult (2–4 years) and geriatric (10–14 years) animals. We found that lesions involving the opercular and caudal calcarine parts of V1 caused robust loss of neurons in topographically corresponding regions of the ipsilateral LGN (lesion projection zones), concomitant with a substantial reduction in the volume of this nucleus. Neuronal density was markedly reduced in the lesion projection zones, relative to the corresponding regions of the contralateral LGN, or the LGN in non-lesioned animals. Moreover, the percentage decrease in neuronal density within the lesion projection zones was significantly greater in the geriatric group, compared with the adult groups. The volume and neuronal density in the contralateral LGN of lesioned adult and geriatric marmosets were similar to those in non-lesioned animals. These results show that the primate LGN becomes more vulnerable to degeneration with advancing age. However, even in geriatric primates there is a population of LGN neurons which survives degeneration, and which could play a role in blindsight.

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References

  1. Ahmad A, Spear PD (1993) Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons. J Comp Neurol 334:631–643

    CAS  Article  PubMed  Google Scholar 

  2. Azzopardi P, Cowey A (2001) Motion discrimination in cortically blind patients. Brain 124:30–46

    CAS  Article  PubMed  Google Scholar 

  3. Benevento LA, Yoshida K (1981) The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. J Comp Neurol 203:455–474

    CAS  Article  PubMed  Google Scholar 

  4. Bogousslavsky J, Regli F, van Melle G (1983) Unilateral occipital infarction: evaluation of the risks of developing bilateral loss of vision. J Neurol Neurosurg Psychiatry 46:78–80

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Bradley PB (1975) Methods in brain research. Wiley & Sons, New York

    Google Scholar 

  6. Briggs F, Usrey WM (2011) Corticogeniculate feedback and visual processing in the primate. J Physiol 589:33–40. doi:10.1113/jphysiol.2010.193599

    CAS  Article  PubMed  Google Scholar 

  7. Caleo M, Menna E, Chierzi S, Cenni MC, Maffei L (2000) Brain-derived neurotrophic factor is an anterograde survival factor in the rat visual system. Curr Biol 10:1155–1161

    CAS  Article  PubMed  Google Scholar 

  8. Chaplin TA, Yu HH, Rosa MGP (2013) Representation of the visual field in the primary visual area of the marmoset monkey: magnification factors, point-image size, and proportionality to retinal ganglion cell density. J Comp Neurol 521:1001–1019. doi:10.1002/cne.23215

    Article  PubMed  Google Scholar 

  9. Cowey A (1964) Projection of the retina on to striate and prestriate cortex in the squirrel monkey, Saimiri sciureus. J Neurophysiol 27:366–393

    CAS  PubMed  Google Scholar 

  10. Cowey A, Alexander I, Stoerig P (2011) Transneuronal retrograde degeneration of retinal ganglion cells and optic tract in hemianopic monkeys and humans. Brain 134:2149–2157. doi:10.1093/brain/awr125

    Article  PubMed  Google Scholar 

  11. Diaz F, Villena A, Gonzalez P, Requena V, Rius F, Perez De Vargas I (1999) Stereological age-related changes in neurons of the rat dorsal lateral geniculate nucleus. Anat Rec 255:396–400

    CAS  Article  PubMed  Google Scholar 

  12. Dineen JT, Hendrickson AE (1981) Age correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. Invest Ophthalmol Vis Sci 21:749–752

    CAS  PubMed  Google Scholar 

  13. Dorph-Petersen KA, Caric D, Saghafi R, Zhang W, Sampson AR, Lewis DA (2009) Volume and neuron number of the lateral geniculate nucleus in schizophrenia and mood disorders. Acta Neuropathol 117:369–384. doi:10.1007/s00401-008-0410-2

    Article  PubMed  Google Scholar 

  14. Finlay BL, Charvet CJ, Bastille I, Cheung DT, Muniz JA, Silveira LCL (2014) Scaling the primate lateral geniculate nucleus: niche and neurodevelopment in the regulation of magnocellular and parvocellular cell number and nucleus volume. J Comp Neurol 522:1839–1857. doi:10.1002/cne.23505

    Article  PubMed  Google Scholar 

  15. Fritsches KA, Rosa MGP (1996) Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus). J Comp Neurol 372:264–282

    CAS  Article  PubMed  Google Scholar 

  16. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209

    CAS  Article  PubMed  Google Scholar 

  17. Giordano S, Darley-Usmar V, Zhang J (2013) Autophagy as an essential cellular antioxidant pathway in neurodegenerative disease. Redox Biol 2:82–90. doi:10.1016/j.redox.2013.12.013.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263

    CAS  Article  PubMed  Google Scholar 

  19. Hagan MA, Rosa MGP, Lui LL (2017) Neural plasticity following lesions of the primate occipital lobe: the marmoset as an animal model for studies of blindsight. Dev Neurobiol, in press. doi:10.1002/dneu.22426.

    PubMed  Google Scholar 

  20. Hendrickson A, Dineen JT (1982) Hypertrophy of neurons in dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys. Neurosci Lett 30:217–222

    CAS  Article  PubMed  Google Scholar 

  21. Hendrickson A, Warner CE, Possin D, Huang J, Kwan WC, Bourne JA (2015) Retrograde transneuronal degeneration in the retina and lateral geniculate nucleus of the V1-lesioned marmoset monkey. Brain Struct Funct 220:351–360. doi:10.1007/s00429-013-0659-7.

  22. Hill CS, Coleman MP, Menon DK (2016) Traumatic axonal injury: mechanisms and translational opportunities. Trends Neurosci 39:311–324. doi:10.1016/j.tins.2016.03.002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Hiona A, Leeuwenburgh C (2004) Effects of age and caloric restriction on brain neuronal cell death/survival. Ann N Y Acad Sci 1019:96–105

    CAS  Article  PubMed  Google Scholar 

  24. Kisvárday ZF, Cowey A, Stoerig P, Somogyi P (1991) Direct and indirect retinal input into degenerated dorsal lateral geniculate nucleus after striate cortical removal in monkey: implications for residual vision. Exp Brain Res 86:271–292

    Article  PubMed  Google Scholar 

  25. LeBlanc J, de Guise E, Gosselin N, Feyz M (2006) Comparison of functional outcome following acute care in young, middle-aged and elderly patients with traumatic brain injury. Brain Inj 20:779–790

    Article  PubMed  Google Scholar 

  26. Li M, He HG, Shi W, Li J, Lv B, Wang CH, Miao QW, Wang ZC, Wang NL, Walter M, Sabel BA (2012) Quantification of the human lateral geniculate nucleus in vivo using MR imaging based on morphometry: volume loss with age. Am J Neuroradiol 33:915–921. doi:10.3174/ajnr.A2884

    CAS  Article  PubMed  Google Scholar 

  27. Matthews MR (1964) Further observations on transneuronal degeneration in the lateral geniculate nucleus of the macaque monkey. J Anat 98:225–263

    Google Scholar 

  28. Matthews MR, Cowan WM, Powell TP (1960) Transneuronal cell degeneration in the lateral geniculate nucleus of the macaque monkey. J Anat 94:145–169

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Mattson MP, Magnus T (2006) Ageing and neuronal vulnerability. Nat Rev Neurosci 7:278–294

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Mihailović LT, Cupić D, Dekleva N (1971) Changes in the numbers of neurons and glial cells in the lateral geniculate nucleus of the monkey during retrograde cell degeneration. J Comp Neurol 142:223–229

    Article  PubMed  Google Scholar 

  31. Mitchell JF, Leopold DA (2015) The marmoset monkey as a model for visual neuroscience. Neurosci Res 93:20–46. doi:10.1016/j.neures.2015.01.008

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nishijima K, Saitoh R, Tanaka S, Ohsato-Suzuki M, Ohno T, Kitajima S (2012) Life span of common marmoset (Callithrix jacchus) at CLEA Japan breeding colony. Biogerontology 13:439–443. doi:10.1007/s10522-012-9388-1

    Article  PubMed  Google Scholar 

  33. Palomer E, Martín-Segura A, Baliyan S, Ahmed T, Balschun D, Venero C, Martin MG, Dotti CG (2016) Aging triggers a repressive chromatin state at Bdnf promoters in hippocampal neurons. Cell Rep 16:2889–2900. doi:10.1016/j.celrep.2016.08.028.

    CAS  Article  PubMed  Google Scholar 

  34. Paxinos G, Watson C, Petrides M, Rosa MGP, Tokuno H (2012) The marmoset brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  35. Perlson E, Maday S, Fu MM, Moughamian AJ, Holzbaur EL (2010) Retrograde axonal transport: pathways to cell death? Trends Neurosci 33:335–344. doi:10.1016/j.tins.2010.03.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Polyak S (1933) A contribution to the cerebral representation of the retina. J Comp Neurol 57:541–617

    Article  Google Scholar 

  37. Popa-Wagner A, Carmichael ST, Kokaia Z, Kessler C, Walker LC (2007) The response of the aged brain to stroke: too much, too soon? Curr Neurovasc Res 4:216–227

    CAS  Article  PubMed  Google Scholar 

  38. Rosa MGP, Tweedale R, Elston GN (2000) Visual responses of neurons in the middle temporal area of new world monkeys after lesions of striate cortex. J Neurosci 20:5552–5563

    CAS  PubMed  Google Scholar 

  39. Royet JP (1991) Stereology: a method for analyzing images. Prog Neurobiol 37:433–474

    CAS  Article  PubMed  Google Scholar 

  40. Satorre J, Cano J, Reinoso-Suárez F (1985) Stability of the neuronal population of the dorsal lateral geniculate nucleus (LGNd) of aged rats. Brain Res 339:375–377

    CAS  Article  PubMed  Google Scholar 

  41. Schmid MC, Mrowka SW, Turchi J, Saunders RC, Wilke M, Peters AJ, Ye FQ, Leopold DA (2010) Blindsight depends on the lateral geniculate nucleus. Nature 466:373–377. doi:10.1038/nature09179

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Schmitz C, Hof PR (2005) Design-based stereology in neuroscience. Neuroscience 130:813–831

    CAS  Article  PubMed  Google Scholar 

  43. Sillito AM, Jones HE (2002) Corticothalamic interactions in the transfer of visual information. Philos Trans R Soc Lond B Biol Sci 357:1739–1752

    Article  PubMed  PubMed Central  Google Scholar 

  44. Sincich LC, Park KF, Wohlgemuth MJ, Horton JC (2004) Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7:1123–1128

    CAS  Article  PubMed  Google Scholar 

  45. Solomon SG (2002) Striate cortex in dichromatic and trichromatic marmosets: neurochemical compartmentalization and geniculate input. J Comp Neurol 450:366–381

    Article  PubMed  Google Scholar 

  46. Solomon SG, Rosa MGP (2014) A simpler primate brain: the visual system of the marmoset monkey. Front Neural Circuits 8:96. doi:10.3389/fncir.2014.00096.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Vanburen JM (1963) Trans-synaptic retrograde degeneration in the visual system of primates. J Neurol Neurosurg Psych 26:402–409

    CAS  Article  Google Scholar 

  48. Warner CE, Goldshmit Y, Bourne JA (2010) Retinal afferents synapse with relay cells targeting the middle temporal area in the pulvinar and lateral geniculate nuclei. Front Neuroanat 4:8. doi:10.3389/neuro.05.008.2010.

    PubMed  PubMed Central  Google Scholar 

  49. Weller RE, Kaas JH (1989) Parameters affecting the loss of ganglion cells of the retina following ablations of striate cortex in primates. Vis Neurosci 3:327–349

    CAS  Article  PubMed  Google Scholar 

  50. White AJ, Wilder HD, Goodchild AK, Sefton AJ, Martin PR (1998) Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. J Neurophysiol 80:2063–2076

    CAS  PubMed  Google Scholar 

  51. Williams RW, Rakic P (1988) Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J Comp Neurol 278:344–352

    CAS  Article  PubMed  Google Scholar 

  52. Wilson JR (1993) Circuitry of the dorsal lateral geniculate nucleus in the cat and monkey. Acta Anat (Basel) 147:1–13.

    CAS  Article  PubMed  Google Scholar 

  53. Wojda U, Salinska E, Kuznicki J (2008) Calcium ions in neuronal degeneration. IUBMB Life 60:575–590. doi:10.1002/iub.91

    CAS  Article  PubMed  Google Scholar 

  54. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blümcke I (1996) NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44:1167–1171

    CAS  Article  PubMed  Google Scholar 

  55. Wong-Riley MT (1972) Changes in the dorsal lateral geniculate nucleus of the squirrel monkey after unilateral ablation of the visual cortex. J Comp Neurol 146:519–548

    CAS  Article  PubMed  Google Scholar 

  56. Yin Y, Sun G, Li E, Kiselyov K, Sun D (2017) ER stress and impaired autophagy flux in neuronal degeneration and brain injury. Ageing Res Rev 34:3–14. doi:10.1016/j.arr.2016.08.008

    CAS  Article  PubMed  Google Scholar 

  57. Yu HH, Chaplin TA, Egan GW, Reser DH, Worthy KH, Rosa MG (2013) Visually evoked responses in extrastriate area MT after lesions of striate cortex in early life. J Neurosci 33:12479–12489. doi:10.1523/JNEUROSCI.0844-13.2013

    CAS  Article  PubMed  Google Scholar 

  58. Yukie M, Iwai E (1981) Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J Comp Neurol 201:81–97

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Rowan Tweedale for many suggestions that improved this manuscript, and acknowledge the contributions of Jonathan Chan and of the Monash Histology Platform, Department of Anatomy and Developmental Biology, for the slide scanning. Supported by research grants from the National Health and Medical Research Council (1066232, 1122220) and Australian Research Council (CE140100007, DE130100493, DE140101505).

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Correspondence to Nafiseh Atapour.

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Atapour, N., Worthy, K.H., Lui, L.L. et al. Neuronal degeneration in the dorsal lateral geniculate nucleus following lesions of primary visual cortex: comparison of young adult and geriatric marmoset monkeys. Brain Struct Funct 222, 3283–3293 (2017). https://doi.org/10.1007/s00429-017-1404-4

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Keywords

  • Lateral geniculate nucleus
  • Degeneration
  • Neuronal loss
  • Primary visual cortex
  • Blindsight
  • Callithrix jacchus