Eye-specific retinogeniculate segregation proceeds normally following disruption of patterned spontaneous retinal activity

Neural Development

Hwai-Jong Cheng¹  Barbara Chapman¹  Ben K Stafford³  Lauren C Liets¹  Chao Sun¹  Colenso M Speer² 

[1] Department of Neurobiology, Physiology, and Behavior, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA;Current address: Department of Chemistry and Chemical Biology, Harvard University, 12 Oxford Street, Cambridge, MA 02138, USA;Department of Neurosciences, University of California San Diego, 9500 Gilman Drive, San Diego, CA 92093, USA

关键词: Dorsal lateral geniculate nucleus;    Retinal ganglion cell;    Spontaneous activity;    Retinal wave;    Eye-specific segregation;    Retinogeniculate;   

Others  :  1146400
DOI  :  10.1186/1749-8104-9-25

 received in 2014-06-09, accepted in 2014-10-20,  发布年份 2014

【 摘 要 】

Background

Spontaneous retinal activity (SRA) is important during eye-specific segregation within the dorsal lateral geniculate nucleus (dLGN), but the feature(s) of activity critical for retinogeniculate refinement are controversial. Pharmacologically or genetically manipulating cholinergic signaling during SRA perturbs correlated retinal ganglion cell (RGC) spiking and disrupts eye-specific retinofugal refinement in vivo, consistent with an instructive role for SRA during visual system development. Paradoxically, ablating the starburst amacrine cells (SACs) that generate cholinergic spontaneous activity disrupts correlated RGC firing without impacting retinal activity levels or eye-specific segregation in the dLGN. Such experiments suggest that patterned SRA during retinal waves is not critical for eye-specific refinement and instead, normal activity levels are permissive for retinogeniculate development. Here we revisit the effects of ablating the cholinergic network during eye-specific segregation and show that SAC ablation disrupts, but does not eliminate, retinal waves with no concomitant impact on normal eye-specific segregation in the dLGN.

Results

We induced SAC ablation in postnatal ferret pups beginning at birth by intraocular injection of a novel immunotoxin selective for the ferret vesicular acetylcholine transporter (Ferret VAChT-Sap). Through dual-patch whole-cell and multi-electrode array recording we found that SAC ablation altered SRA patterns and led to significantly smaller retinal waves compared with controls. Despite these defects, eye-specific segregation was normal. Further, interocular competition for target territory in the dLGN proceeded in cases where SAC ablation was asymmetric in the two eyes.

Conclusions

Our data demonstrate normal eye-specific retinogeniculate development despite significant abnormalities in patterned SRA. Comparing our current results with earlier studies suggests that defects in retinal wave size, absolute levels of SRA, correlations between RGC pairs, RGC burst frequency, high frequency RGC firing during bursts, and the number of spikes per RGC burst are each uncorrelated with abnormalities in eye-specific segregation in the dLGN. An increase in the fraction of asynchronous spikes occurring outside of bursts and waves correlates with eye-specific segregation defects in studies reported to date. These findings highlight the relative importance of different features of SRA while providing additional constraints for computational models of Hebbian plasticity mechanisms in the developing visual system.

【 授权许可】

   
2014 Speer et al.; licensee BioMed Central Ltd.

【 图 表 】

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Fig. 1.

【 参考文献 】

• [1]Godement P, Salaun J, Imbert M: Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 1984, 230:552-575.
• [2]Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W: Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 2005, 22:661-676.
• [3]Linden DC, Guillery RW, Cucchiaro J: The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J Comp Neurol 1981, 203:189-211.
• [4]Speer CM, Mikula S, Huberman AD, Chapman B: The developmental remodeling of eye-specific afferents in the ferret dorsal lateral geniculate nucleus. Anat Rec (Hoboken) 2010, 293:1-24.
• [5]Wong RO, Chernjavsky A, Smith SJ, Shatz CJ: Early functional neural networks in the developing retina. Nature 1995, 374:716-718.
• [6]Feller MB, Wellis DP, Stellwagen D, Werblin FS, Shatz CJ: Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 1996, 272:1182-1187.
• [7]Galli L, Maffei L: Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 1988, 242:90-91.
• [8]Maffei L, Galli-Resta L: Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. Proc Natl Acad Sci U S A 1990, 87:2861-2864.
• [9]Meister M, Wong RO, Baylor DA, Shatz CJ: Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 1991, 252:939-943.
• [10]Wong RO, Meister M, Shatz CJ: Transient period of correlated bursting activity during development of the mammalian retina. Neuron 1993, 11:923-938.
• [11]Kirkby LA, Sack GS, Firl A, Feller MB: A role for correlated spontaneous activity in the assembly of neural circuits. Neuron 2013, 80:1129-1144.
• [12]Penn AA, Riquelme PA, Feller MB, Shatz CJ: Competition in retinogeniculate patterning driven by spontaneous activity. Science 1998, 279:2108-2112.
• [13]Huberman AD, Stellwagen D, Chapman B: Decoupling eye-specific segregation from lamination in the lateral geniculate nucleus. J Neurosci 2002, 22:9419-9429.
• [14]Huberman AD, Wang GY, Liets LC, Collins OA, Chapman B, Chalupa LM: Eye-specific retinogeniculate segregation independent of normal neuronal activity. Science 2003, 300:994-998.
• [15]Pfeiffenberger C, Cutforth T, Woods G, Yamada J, Renteria RC, Copenhagen DR, Flanagan JG, Feldheim DA: Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping. Nat Neurosci 2005, 8:1022-1027.
• [16]Rebsam A, Petros TJ, Mason CA: Switching retinogeniculate axon laterality leads to normal targeting but abnormal eye-specific segregation that is activity dependent. J Neurosci 2009, 29:14855-14863.
• [17]Dhande OS, Hua EW, Guh E, Yeh J, Bhatt S, Zhang Y, Ruthazer ES, Feller MB, Crair MC: Development of single retinofugal axon arbors in normal and {beta}2 knock-out mice. J Neurosci 2011, 31:3384-3399.
• [18]Chandrasekaran AR, Plas DT, Gonzalez E, Crair MC: Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. J Neurosci 2005, 25:6929-6938.
• [19]Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB, Ullian EM, Baccus SA, Barres BA: Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 2008, 59:425-438.
• [20]Cang J, Renteria RC, Kaneko M, Liu X, Copenhagen DR, Stryker MP: Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 2005, 48:797-809.
• [21]Huberman AD, Speer CM, Chapman B: Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1. Neuron 2006, 52:247-254.
• [22]Bansal A, Singer JH, Hwang BJ, Xu W, Beaudet A, Feller MB: Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J Neurosci 2000, 20:7672-7681.
• [23]Muir-Robinson G, Hwang BJ, Feller MB: Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J Neurosci 2002, 22:5259-5264.
• [24]McLaughlin T, Torborg CL, Feller MB, O’Leary DD: Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 2003, 40:1147-1160.
• [25]Sun C, Warland DK, Ballesteros JM, van der List D, Chalupa LM: Retinal waves in mice lacking the beta2 subunit of the nicotinic acetylcholine receptor. Proc Natl Acad Sci U S A 2008, 105:13638-13643.
• [26]Stafford BK, Sher A, Litke AM, Feldheim DA: Spatial-temporal patterns of retinal waves underlying activity-dependent refinement of retinofugal projections. Neuron 2009, 64:200-212.
• [27]Rossi FM, Pizzorusso T, Porciatti V, Marubio LM, Maffei L, Changeux JP: Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system. Proc Natl Acad Sci U S A 2001, 98:6453-6458.
• [28]Grubb MS, Rossi FM, Changeux JP, Thompson ID: Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron 2003, 40:1161-1172.
• [29]Pfeiffenberger C, Yamada J, Feldheim DA: Ephrin-As and patterned retinal activity act together in the development of topographic maps in the primary visual system. J Neurosci 2006, 26:12873-12884.
• [30]Chandrasekaran AR, Shah RD, Crair MC: Developmental homeostasis of mouse retinocollicular synapses. J Neurosci 2007, 27:1746-1755.
• [31]Mrsic-Flogel TD, Hofer SB, Creutzfeldt C, Cloez-Tayarani I, Changeux JP, Bonhoeffer T, Hubener M: Altered map of visual space in the superior colliculus of mice lacking early retinal waves. J Neurosci 2005, 25:6921-6928.
• [32]Triplett JW, Owens MT, Yamada J, Lemke G, Cang J, Stryker MP, Feldheim DA: Retinal input instructs alignment of visual topographic maps. Cell 2009, 139:175-185.
• [33]Wang L, Rangarajan KV, Lawhn-Heath CA, Sarnaik R, Wang BS, Liu X, Cang J: Direction-specific disruption of subcortical visual behavior and receptive fields in mice lacking the beta2 subunit of nicotinic acetylcholine receptor. J Neurosci 2009, 29:12909-12918.
• [34]Cang J, Niell CM, Liu X, Pfeiffenberger C, Feldheim DA, Stryker MP: Selective disruption of one Cartesian axis of cortical maps and receptive fields by deficiency in ephrin-As and structured activity. Neuron 2008, 57:511-523.
• [35]Cang J, Wang L, Stryker MP, Feldheim DA: Roles of ephrin-as and structured activity in the development of functional maps in the superior colliculus. J Neurosci 2008, 28:11015-11023.
• [36]Cook PM, Prusky G, Ramoa AS: The role of spontaneous retinal activity before eye opening in the maturation of form and function in the retinogeniculate pathway of the ferret. Vis Neurosci 1999, 16:491-501.
• [37]Feller MB: Retinal waves are likely to instruct the formation of eye-specific retinogeniculate projections. Neural Dev 2009, 4:24. BioMed Central Full Text
• [38]Stellwagen D, Shatz CJ: An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 2002, 33:357-367.
• [39]Xu HP, Furman M, Mineur YS, Chen H, King SL, Zenisek D, Zhou ZJ, Butts DA, Tian N, Picciotto MR, Crair MC: An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 2011, 70:1115-1127.
• [40]Wong WT, Myhr KL, Miller ED, Wong RO: Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. J Neurosci 2000, 20:351-360.
• [41]Ford KJ, Felix AL, Feller MB: Cellular mechanisms underlying spatiotemporal features of cholinergic retinal waves. J Neurosci 2012, 32:850-863.
• [42]Stacy RC, Demas J, Burgess RW, Sanes JR, Wong RO: Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J Neurosci 2005, 25:9347-9357.
• [43]Torborg CL, Hansen KA, Feller MB: High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 2005, 8:72-78.
• [44]Bjartmar L, Huberman AD, Ullian EM, Renteria RC, Liu X, Xu W, Prezioso J, Susman MW, Stellwagen D, Stokes CC, Cho R, Worley P, Malenka RC, Ball S, Peachey NS, Copenhagen D, Chapman B, Nakamoto M, Barres BA, Perin MS: Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci 2006, 26:6269-6281.
• [45]Blankenship AG, Hamby AM, Firl A, Vyas S, Maxeiner S, Willecke K, Feller MB: The role of neuronal connexins 36 and 45 in shaping spontaneous firing patterns in the developing retina. J Neurosci 2011, 31:9998-10008.
• [46]Demas J, Sagdullaev BT, Green E, Jaubert-Miazza L, McCall MA, Gregg RG, Wong RO, Guido W: Failure to maintain eye-specific segregation in nob, a mutant with abnormally patterned retinal activity. Neuron 2006, 50:247-259.
• [47]Benjumeda I, Escalante A, Law C, Morales D, Chauvin G, Muca G, Coca Y, Marquez J, Lopez-Bendito G, Kania A, Martínez L, Herrera E: Uncoupling of EphA/ephrinA signaling and spontaneous activity in neural circuit wiring. J Neurosci 2013, 33:18208-18218.
• [48]Koch SM, Dela Cruz CG, Hnasko TS, Edwards RH, Huberman AD, Ullian EM: Pathway-specific genetic attenuation of glutamate release alters select features of competition-based visual circuit refinement. Neuron 2011, 71:235-242.
• [49]Wong RO: Retinal waves and visual system development. Annu Rev Neurosci 1999, 22:29-47.
• [50]Katz LC, Shatz CJ: Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
• [51]Furman M, Xu HP, Crair MC: Competition driven by retinal waves promotes the morphological and functional synaptic development of neurons in the superior colliculus. J Neurophysiol 2013, 110:1441-1454.
• [52]Stellwagen D, Shatz CJ, Feller MB: Dynamics of retinal waves are controlled by cyclic AMP. Neuron 1999, 24:673-685.
• [53]Huberman AD, Murray KD, Warland DK, Feldheim DA, Chapman B: Ephrin-As mediate targeting of eye-specific projections to the lateral geniculate nucleus. Nat Neurosci 2005, 8:1013-1021.
• [54]Sun C, Speer CM, Wang GY, Chapman B, Chalupa LM: Epibatidine application in vitro blocks retinal waves without silencing all retinal ganglion cell action potentials in developing retina of the mouse and ferret. J Neurophysiol 2008, 100:3253-3263.
• [55]Butts DA, Kanold PO, Shatz CJ: A burst-based “Hebbian” learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement. PLoS Biol 2007, 5:e61.
• [56]Caporale N, Dan Y: Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 2008, 31:25-46.
• [57]Lo FS, Ziburkus J, Guido W: Synaptic mechanisms regulating the activation of a Ca(2+)-mediated plateau potential in developing relay cells of the LGN. J Neurophysiol 2002, 87:1175-1185.
• [58]Ziburkus J, Dilger EK, Lo FS, Guido W: LTD and LTP at the developing retinogeniculate synapse. J Neurophysiol 2009, 102:3082-3090.
• [59]Lee H, Brott BK, Kirkby LA, Adelson JD, Cheng S, Feller MB, Datwani A, Shatz CJ: Synapse elimination and learning rules co-regulated by MHC class I H2-Db. Nature 2014, 509:195-200.
• [60]Munz M, Gobert D, Schohl A, Poquerusse J, Podgorski K, Spratt P, Ruthazer ES: Rapid Hebbian axonal remodeling mediated by visual stimulation. Science 2014, 344:904-909.
• [61]Zhang J, Ackman JB, Xu HP, Crair MC: Visual map development depends on the temporal pattern of binocular activity in mice. Nat Neurosci 2012, 15:298-307.
• [62]Ackman JB, Burbridge TJ, Crair MC: Retinal waves coordinate patterned activity throughout the developing visual system. Nature 2012, 490:219-225.
• [63]Liets LC, Olshausen BA, Wang GY, Chalupa LM: Spontaneous activity of morphologically identified ganglion cells in the developing ferret retina. J Neurosci 2003, 23:7343-7350.
• [64]Shoham S, Fellows MR, Normann RA: Robust, automatic spike sorting using mixtures of multivariate t-distributions. J Neurosci Methods 2003, 127:111-122.
• [65]Rasband WS: ImageJ, National Institutes of Health, Bethesda, Maryland, USA, 1997–2014. [http://imagej.nih.gov/ij/ webcite]