Brain Structure and Function

, Volume 220, Issue 1, pp 351–360 | Cite as

Retrograde transneuronal degeneration in the retina and lateral geniculate nucleus of the V1-lesioned marmoset monkey

  • A. Hendrickson
  • C. E. Warner
  • D. Possin
  • J. Huang
  • W. C. Kwan
  • J. A. BourneEmail author
Original Article


Retrograde transneuronal degeneration (RTD) of retinal ganglion cells and dorsal lateral geniculate (LGN) neurons are well described following a lesion of the primary visual cortex (V1) in both Old World monkeys and humans. Based on previous studies of New World monkeys and prosimians, it was suggested that these species displayed no RTD following a lesion of V1. In this study of the New World marmoset monkey, 1 year after a unilateral V1 lesion either in adults or at 14 days after birth, we observed ~20 % ganglion cell (GC) loss in adult but ~70 % in infants. This finding is similar to the RTD previously described for Old World Macaca monkeys. Furthermore, in infants we find a similar amount of RTD at 3 weeks and 1 year following lesion, demonstrating that RTD is very rapid in neonates. This highlights the importance of trying to prevent the rapid onset of RTD following a lesion of V1 in early life as a strategy for improved functional recovery. Despite differences in GC loss, there was little difference between LGN degeneration in infant versus adult lesions. A wedge on the horizontal meridian corresponding to the LGN foveal representation revealed extensive neuronal loss. Retinal afferent input was labeled by cholera toxin B subunit. Input to the degenerated parvocellular layers was difficult to detect, while input to magnocellular and koniocellular layers was reduced but still apparent. Our demonstration that the New World marmoset monkey shares many of the features of neuroplasticity with Old World Macaca monkeys and humans emphasizes the opportunity and benefit of marmosets as models of visual cortical injury.


Primate Hemianopia Visual system Cortical blindness Stroke 



National Health and Medical Research Council Project Grants (APP1002049 and APP1042893) supported this work. The Australian Regenerative Medicine Institute is supported by grants from the State Government of Victoria and the Australian Government.


  1. Bourne JA, Warner CE, Rosa MGP (2005) Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry. Cereb Cortex 15:740–748PubMedCrossRefGoogle Scholar
  2. Bridge H, Thomas O, Jbabdi S, Cowey A (2008) Changes in connectivity after visual cortical brain damage underlie altered visual function. Brain 131:1433–1444PubMedCrossRefGoogle Scholar
  3. Bridge H, Jindahra P, Barbur J, Plant GT (2011) Imaging reveals optic tract degeneration in hemianopia. Invest Ophthalmol Vis Sci 52:382–388PubMedCrossRefGoogle Scholar
  4. Chan TL, Martin PR, Glunas N, Grünert U (2001) Bipolar cell diversity in the primate retina: morphologic and immunocytochemical analysis of a New World monkey, the marmoset Callithrix jacchus. J Comp Neurol 437:219–239PubMedCrossRefGoogle Scholar
  5. Cowey A (1974) Atrophy of retinal ganglion cells after removal of striate cortex in a rhesus monkey. Perception 3:257–260PubMedCrossRefGoogle Scholar
  6. Cowey A, Stoerig P (1995) Blindsight in monkeys. Nature 373:247–249PubMedCrossRefGoogle Scholar
  7. Cowey A, Stoerig P, Perry VH (1989) Transneuronal retrograde degeneration of retinal ganglion cells after damage to striate cortex in macaque monkeys: selective loss of Pβ cells. Neuroscience 29:65–80PubMedCrossRefGoogle Scholar
  8. Cowey A, Stoerig P, Bannister M (1994) Retinal ganglion cells labelled from the pulvinar nucleus in macaque monkeys. Neuroscience 61:691–705PubMedCrossRefGoogle Scholar
  9. Cowey A, Alexander I, Stoerig P (2011) Transneuronal retrograde degeneration of retinal ganglion cells and optic tract in hemianopic monkeys and humans. Brain 134:2149–2157PubMedCrossRefGoogle Scholar
  10. Dacey DM (1999) Primate retina: cell types, circuits and color opponency. Prog Retin Eye Res 8:737–763CrossRefGoogle Scholar
  11. Dineen JT, Hendrickson AE (1981) Age correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. Investig Ophthalmol Vis Sci 21:749–752Google Scholar
  12. Fritsches KA, Rosa MGP (1996) Visutopic organization of striate cortex in the marmoset monkey (Callithrix jacchus). J Comp Neurol 371:264–282CrossRefGoogle Scholar
  13. Goldshmit Y, Bourne JA (2010) Upregulation of EphA4 on astrocytes potentially mediates astrocytic gliosis after cortical lesion in the marmoset monkey. J Neurotrauma 27:1321–1332PubMedCrossRefGoogle Scholar
  14. Harting JK, Huerta MF, Hashikawa T, van Lieshout DP (1991) Projection of the mammalian superior colliculus supon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J Comp Neurol 304:275–306PubMedCrossRefGoogle Scholar
  15. Hendrickson A, Troilo D, Possin D, Springer A (2006) Development of the neural retina and its vasculature in the marmoset Callithrix jacchus. J Comp Neurol 497:270–286PubMedCrossRefGoogle Scholar
  16. Hendrickson A, Yan YH, Erickson A, Possin D, Pow D (2007) Expression patterns of calretinin, calbindin and parvalbumin and their colocalization in neurons during development of Macaca monkey retina. Exp Eye Res 85:587–601PubMedCrossRefGoogle Scholar
  17. Hendry SHC, Yoshioka T (1994) A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264:575–577PubMedCrossRefGoogle Scholar
  18. Homman-Ludiye J, Bourne JA (2013) The guidance molecule semaphorin3A is differentially involved in the arealization of the mouse and primate neocortex. Cereb Cortex. doi: 10.1093/cercor/bht141
  19. Innocenti GM, Kiper DC, Knyazeva MG, Deonna TW (1999) On nature and limits of cortical developmental plasticity after an early lesion, in a child. Restor Neurol Neurosci 15:219–227PubMedGoogle Scholar
  20. Jindahra P, Petrie A, Plant GT (2009) Retrograde trans-synaptic retinal ganglion cell loss identified by optical coherence tomography. Brain 132:628–634PubMedCrossRefGoogle Scholar
  21. Jindahra P, Petrie A, Plant GT (2012) The time course of retrograde trans-synaptic degeneration following occipital lobe damage in humans. Brain 135:534–541PubMedCrossRefGoogle Scholar
  22. 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 86:271–292PubMedCrossRefGoogle Scholar
  23. Lund JS (1988) Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci 11:253–288PubMedCrossRefGoogle Scholar
  24. Mashiko H, Yoshida AC, Kikuchi SS, Niimi K, Takahashi E, Aruga J, Okano H, Shimogori T (2012) Comparative anatomy of marmoset and mouse cortex from genomic expression. J Neurosci 32:5039–5053PubMedCrossRefGoogle Scholar
  25. Newman JD, Kenkel WM, Aronoff EC, Bock NA, Zametkin MR, Silva AC (2009) A combined histological and MRI brain atlas of the common marmoset monkey, Callithrix jacchus. Brain Res Rev 62:1–18PubMedCentralPubMedCrossRefGoogle Scholar
  26. Park HY, Park YG, Cho AH, Park CK (2013) Transneuronal retrograde degeneration of the retina ganglion cells in patients with cerebral infarction. Ophthalmology 120:1292–1299PubMedCrossRefGoogle Scholar
  27. Paxinos G, Watson C, Petrides M, Rosa MGP, Tokuno H (2012) The marmoset brain in stereotaxic coordinates, 1st edn. Academic Press, New YorkGoogle Scholar
  28. Rodman H (2006) Behavioral and neural alternations following V1 damage in immature primates. In: Lomber ST, Eggermont J (eds) Reprogramming the cerebral cortex. Oxford Press, Oxford, pp 92–113Google Scholar
  29. Rodman H, Sorenson KM, Shim AJ, Hexter DP (2001) Calbindin immunoreactivity in the geniculo-extrastriate system of the macaque: implications for heterogeneity in the koniocellular pathway and recovery from cortical damage. J Comp Neurol 431:168–181PubMedCrossRefGoogle Scholar
  30. Rosa M, Tweedale R (2005) Brain maps, great and small: lessons from comparative studies of primate visual cortical organization. Philos T R Soc B 360:665–691CrossRefGoogle Scholar
  31. Sabel BA (1999) Editorial: residual vision and plasticity after visual system damage. Restor Neurol Neurosci 15:73–79PubMedGoogle Scholar
  32. 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 466:373–377PubMedCentralPubMedCrossRefGoogle Scholar
  33. Striemer CL, Chapman CS, Goodale MA (2009) ‘Real-time’ obstacle avoidance in the absence of primary visual cortex. Proc Natl Acad of Sci (USA) 106:15996–16001CrossRefGoogle Scholar
  34. Szmajda BAB, Grünert UU, Martin PRP (2008) Retinal ganglion cell inputs to the koniocellular pathway. J Comp Neurol 510:251–268PubMedCrossRefGoogle Scholar
  35. Van Buren JM (1963) Trans-synaptic degeneration in the visual system of primates. J Neurol Neurosurg Psych 27:402–413CrossRefGoogle Scholar
  36. Virley D, Hadingham SJ, Roberts JC, Farnfield B, Elliott H, Whelan G, Golder J, David C, Parsons AA, Hunter AJ (2004) A new primate model of focal stroke: endothelin-1-induced middle cerebral artery occlusion and reperfusion in the common marmoset. J Cereb Blood Flow Metab 24:24–41PubMedCrossRefGoogle Scholar
  37. 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 4:8PubMedCentralPubMedGoogle Scholar
  38. Warner CE, Kwan WC, Bourne JA (2012) The early maturation of visual cortical area MT is dependent on input from the retinorecipient medial portion of the inferior pulvinar. J Neurosci 32:17073–17085PubMedCrossRefGoogle Scholar
  39. Weiskrantz L (2004) Roots of blindsight. Prog Brain Res 144:229–241PubMedGoogle Scholar
  40. Weller RE, Kaas JH (1989) Parameters affecting the loss of ganglion cells of the retina following ablations of striate cortex in primates. Vis Neurosci 3:327–349PubMedCrossRefGoogle Scholar
  41. Weller RE, Kaas JH, Wetzel AB (1979) Evidence for the loss of X-cells of the retina after long-term ablation of visual cortex in monkeys. Brain Res 160:134–138PubMedCrossRefGoogle Scholar
  42. Weller RE, Kaas JH, Ward J (1981) Preservation of retinal ganglion cells and normal patterns of retinogeniculate projections in prosimian primates with long-term ablations of striate cortex. Investig Ophthalmol Vis Sci 20:139–148Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • A. Hendrickson
    • 1
  • C. E. Warner
    • 2
  • D. Possin
    • 1
  • J. Huang
    • 1
  • W. C. Kwan
    • 2
  • J. A. Bourne
    • 2
    Email author
  1. 1.Department of OphthalmologyUniversity of WashingtonSeattleUSA
  2. 2.Australian Regenerative Medicine InstituteMonash UniversityClaytonAustralia

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