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Differential induction of c-Fos and c-Jun in the lateral geniculate nucleus of rats following unilateral optic nerve injury with contralateral retinal blockade

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Abstract

The post-injury responses of traumatic optic neuropathy elicit a number of neuronal reactions in the visual system which have not been fully elucidated. This study aimed to investigate the immediate early gene (IEG) expression in the lateral geniculate nucleus (LGN) following unilateral optic nerve (ON) crush in adult rats with or without contralateral blockade of retinal input, and its indication. Intravitreal injection of the B subunit of cholera toxin was used to label the retinogeniculate projection. In group 1 rats whose unilateral (right eye) ON was crushed, a large induction of c-Jun was observed in the bilateral LGN from 2 h to 3 days post crush. Expression of c-Fos was detected ipsilaterally in cells of the intermediate geniculate nucleus and the medial subdivision of ventral LGN mainly innervated by the intact ON. A majority of c-Fos positive cells were also calbindin D-28k immunoreactive neurons. In group 2 rats whose monocular (left eye) spiking was blocked by tetrodotoxin, a sodium channel blocker, prior to the unilateral (right eye) ON crush, the location of c-Fos expression was observed to be shifted to the side of LGN contralateral to the crush, while the expression pattern of c-Jun resembled the pattern of group 1 rats. Thus, the unilateral ON injury induced significant IEG expression in the LGN may involve different mechanisms, under which the emerging of c-Fos depends upon remaining visual input from the retina, while c-Jun appears independent of visual activity.

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Abbreviations

LGN:

Lateral geniculate nucleus

DLG:

Dorsal nucleus of LGN

VLG:

Ventral nucleus of LGN

IGL:

Intergeniculate leaflet of LGN

ON:

Optic nerve

IEG:

Immediate early gene

TTX:

Tetrodotoxin

CTB:

B subunit of cholera toxin

References

  • Ahmed AK, Dong K, Yamadori T (1995) A retrograde double-labelling study of retinal ganglion cells that project ipsilaterally to vLGN and LPN rather than dLGN and SC, in albino rat. Brain Res 674:275–282

    Article  PubMed  CAS  Google Scholar 

  • Bodeutsch N, Siebert H, Dermon C, Thanos S (1998) Unilateral injury to the adult rat optic nerve causes multiple cellular responses in the contralateral site. J Neurobiol 38:116–128

    Article  Google Scholar 

  • Bennett-Clarke CA, Chiaia NL, Jacquin MF, Rhoades RW (1992) Parvalbumin and calbindin immunocytochemistry reveal functionally distinct cell groups and vibrissa-related patterns in the trigeminal brainstem complex of the adult rat. J Comp Neurol 320:323–338

    Article  PubMed  CAS  Google Scholar 

  • Caputto BL, Guido ME (2000) Immediate early gene expression within the visual system: light and circadian regulation in the retina and the suprachiasmatic nucleus. Neurochem Res 25:153–162

    Article  PubMed  CAS  Google Scholar 

  • Drager UC, Olsen JF (1980) Origins of crossed and uncrossed retinal projections in pigmented and albino mice. J Comp Neurol 191:383–412

    Article  PubMed  CAS  Google Scholar 

  • Dragunow M, Faull R (1989) The use of c-Fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261–265

    Article  PubMed  CAS  Google Scholar 

  • Dreher B, Sefton AJ, Ni SY, Nisbett G (1985) The morphology, number, distribution and central projections of Class I retinal ganglion cells in albino and hooded rats. Brain Behav Evol 26:10–48

    Article  PubMed  CAS  Google Scholar 

  • Fite KV, Janusonis S (2002) Optic afferents to the parabrachial nucleus. Brain Res 943:9–14

    Article  PubMed  CAS  Google Scholar 

  • Gamboa FO, Lima D, Batten TF (2001) Neurochemistry of superficial spinal neurons projecting to nucleus of the solitary tract that express c-Fos on chemical somatic and visceral nociceptive input in the rat. Metab Brain Dis 16:151–164

    Article  Google Scholar 

  • Gellrich NC, Schimming R, Zerfowski M, Eysel UT (2002) Quantification of histological changes after calibrated crush of the intraorbital optic nerve in rats. Br J Ophthalmol 86:233–237

    Article  PubMed  Google Scholar 

  • Goldblum D, Mittag T (2002) Prospects for relevant glaucoma models with retinal ganglion cell damage in the rodent eye. Vision Res 42:471–478

    Article  PubMed  Google Scholar 

  • Gonzales D, Satriotomo I, Miki T, Lee KY, Yokoyama T, Touge T, Matsumoto Y, Li HP, Kuriyama S, Takeuchi Y (2006) Changes of Parvalbumin immunoreactive neurons and GFAP immunoreactive astrocytes in the rat lateral geniculate nucleus following monocular enucleation. Neurosci Lett 3395:149–154

    Article  Google Scholar 

  • Hada Y, Yamada K, Imamura K, Mataga N, Watanabe Y, Yamamoto M (1999) Effects of monocular enucleation on Parvalbumin in rat visual system during postnatal development. Invest Ophthalmol Vis Sci 40:2535–2545

    PubMed  CAS  Google Scholar 

  • Harrington M (1997) The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian system. Neurosci Biobehav Rev 21:705–727

    Article  PubMed  CAS  Google Scholar 

  • Hendry SH, Calkins DJ (1998) Neuronal chemistry and functional organization in the primate visual system. Trends Neurosci 21:344–349

    Article  PubMed  CAS  Google Scholar 

  • Herdegen T, Bastmeyer M, Bahr M, Stuermer C, Bravo R, Zimmermann M (1993) Expression of JUN, KROX and CREB transcription factors in goldfish and rat retinal ganglion cells following optic nerve lesion is related to axonal sprouting. J Neurobio 24:528–543

    Article  CAS  Google Scholar 

  • Herdegen T, Skene P, Bahr M (1997) The c-Jun transcription factor-bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci 20:227–231

    Article  PubMed  CAS  Google Scholar 

  • Herdegen T, Leah J (1998) Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF protein. Brain Res Rev 28:370–490

    Article  PubMed  CAS  Google Scholar 

  • Hunt SP, McNaughton LA, Jenkins R (1995) Immediate early gene activation as a window on mechanism in the nervous system. In: Immediate-early genes in the central nervous system. Springer, Berlin, pp 18–50

  • Isenmann S, Bahr M (1997) Expression of c-Jun protein in degenerating retinal ganglion cells after optic nerve lesion in the rat. Exp Neurol 147:28–36

    Article  PubMed  CAS  Google Scholar 

  • Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W (2005) Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 22:661–676

    Article  PubMed  Google Scholar 

  • Kaczmarek L, Chardhuri A (1997) Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity. Brain Res Rev 23:237–256

    Article  PubMed  CAS  Google Scholar 

  • Klocker N, Zerfowski M, Gellrick N, Bahr M (2001) Morphological and functional analysis of an incomplete CNS fiber tract lesion: graded crush of the rat optic nerve. J Neurosci Methods 110:147–153

    Article  PubMed  CAS  Google Scholar 

  • Kupperman BD, Kasamatsu T (1983) Changes in geniculate cell size following brief monocular blockade of retinal activity in kittens. Nature 306:465–468

    Article  Google Scholar 

  • Leung WM, Nathaniel E, Nathaniel EJH (1992) A morphological and morphometric analysis of the optic nerve in the hypothyroid rat. Exp Neurol 117:51–58

    Article  PubMed  CAS  Google Scholar 

  • Li JL, Li YQ, Li JS, Kaneko T, Mizuno N (1999) Calcium-binding protein-immunoreactive projection neurons in the caudal subnucleus of the spinal trigeminal nucleus of the rat. Neurosci Res 35:225–240

    Article  PubMed  CAS  Google Scholar 

  • Ling C, Schneider G, Jhaveri S (1998) Target-specific morphology of retinal axon arbors in the adult hamster. Vis Neurosci 15:559–579

    Article  PubMed  CAS  Google Scholar 

  • McCormick DA, Feeser HR (1990) Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39:103–113

    Article  PubMed  CAS  Google Scholar 

  • Miller N (2001) Optic nerve protection, regeneration, and repair in the 21st century. Am J Ophthalmol 132:811–818

    Article  PubMed  CAS  Google Scholar 

  • Moore RY, Weis R, Moga M (2000) Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420:398–418

    Article  PubMed  CAS  Google Scholar 

  • Narahashi T, Moore J, Scott WR (1964) Tetrodotoxin blockage of sodium conductance increase in lobster giant axon. J Gen Physiol 48:985–996

    Google Scholar 

  • Okoyama S, Moriizumi T (2001) Onset of calbindin-D 28k and parvalbumin expression in the lateral geniculate complex and olivary pretectal nucleus during postnatal development of the rat. Int J Dev Neurosc 19:655–661

    Article  CAS  Google Scholar 

  • Panagis L, Thanos S, Fischer D, Dermon CR (2005) Unilateral optic nerve crush induces bilateral retinal glial cell proliferation. Eur J Neurosci 21:2305–2309

    Article  PubMed  CAS  Google Scholar 

  • Park HT, Baek SY, Kim BS, Kim JB, Kim JJ (1993) Profile of Fos-like immunoreactivity induction by light stimuli in the intergeniculate leaflet is different from that of the suprachiasmatic nucleus. Brain Res 610:334–339

    Article  PubMed  CAS  Google Scholar 

  • Riccio RV, Matthews MA (1985) Effects of intraocular tetrodotoxin on dendritic spines in the developing rat cortex: a Golgi analysis. Dev Brain Res 19:173–182

    Article  CAS  Google Scholar 

  • Sefton A, Dreher B (1995) Visual system. In: The rat nervous system. Academic Press, New York, pp 833–880

  • Saxon DW (2003) Distribution of Fos labeling in the inferior olive following transient blockade of the VIIIth cranial nerve. Brain Res 966:134–149

    Article  PubMed  CAS  Google Scholar 

  • Schwaller B, Meyer M, Schiffmann S (2002) New functions for old proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1:241–258

    Article  PubMed  CAS  Google Scholar 

  • Thurlow GA, Cooper RM (1991) Activity-dependent changes in eye influence during monocular blockade: increases in the effects of visual stimulation on 2-DG uptake in the adult rat geniculostriate system. J Comp Neurol 306:697–707

    Article  PubMed  CAS  Google Scholar 

  • Waetzig V, Herdegen T (2004) Neurodegenerative and physiological actions of c-Jun N-terminal kinases in the mammalian brain. Neurosci Lett 361:64–67

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Tay SSW, Ng YK (2002) c-Fos and c-Jun expressions in nitric oxide synthase immunoreactive neurons in the lateral geniculate nucleus of experimental glaucomatous rats. Exp Brain Res 144:365–372

    Article  PubMed  CAS  Google Scholar 

  • Yip VS, Zhang WP, Woolsey TA, Lowry OH (1987) Quantitative histochemical and microchemical changes in the adult mouse central nervous system after section of the infraorbital and optic nerves. Brain Res 406:157–170

    Article  PubMed  CAS  Google Scholar 

  • Zhao L, Wang N, Jiang L, Long C, Li J (2006) Unilateral optic nerve transection up-regulate Hsp70 protein expression in lateral geniculate nucleus of rats. Neurosci Lett 404:44–49

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This paper was supported by grants from the National Science Foundation of China (30571996, 30600696), National Basic Research Program of China (2007CB512204), Shanghai Science and Technology Committee (07QA14009).

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Correspondence to Xinghuai Sun.

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Dai, Y., Sun, X. & Chen, Q. Differential induction of c-Fos and c-Jun in the lateral geniculate nucleus of rats following unilateral optic nerve injury with contralateral retinal blockade. Exp Brain Res 193, 9–18 (2009). https://doi.org/10.1007/s00221-008-1591-6

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  • DOI: https://doi.org/10.1007/s00221-008-1591-6

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