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Not a one-trick pony: Diverse connectivity and functions of the rodent lateral geniculate complex

  • ABOOZAR MONAVARFESHANI (a1) (a2), UBADAH SABBAGH (a1) (a3) and MICHAEL A. FOX (a1) (a2)
Abstract

Often mislabeled as a simple relay of sensory information, the thalamus is a complicated structure with diverse functions. This diversity is exemplified by roles visual thalamus plays in processing and transmitting light-derived stimuli. Such light-derived signals are transmitted to the thalamus by retinal ganglion cells (RGCs), the sole projection neurons of the retina. Axons from RGCs innervate more than ten distinct nuclei within thalamus, including those of the lateral geniculate complex. Nuclei within the lateral geniculate complex of nocturnal rodents, which include the dorsal lateral geniculate nucleus (dLGN), ventral lateral geniculate nucleus (vLGN), and intergeniculate leaflet (IGL), are each densely innervated by retinal projections, yet, exhibit distinct cytoarchitecture and connectivity. These features suggest that each nucleus within this complex plays a unique role in processing and transmitting light-derived signals. Here, we review the diverse cytoarchitecture and connectivity of these nuclei in nocturnal rodents, in an effort to highlight roles for dLGN in vision and for vLGN and IGL in visuomotor, vestibular, ocular, and circadian function.

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Corresponding author
*Address correspondence to: Michael A. Fox, Virginia Tech Carilion Research Institute, Director, Developmental and Translational Neurobiology Center, VTCRI, 2 Riverside Circle, Roanoke, VA 24016. E-mail: mafox1@vtc.vt.edu
References
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Altman, J. & Bayer, S.A. (1989). Development of the rat thalamus: VI. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the lateral geniculate and lateral posterior nuclei. Journal of Comparative Neurology 284, 581601.
Arcelli, P., Frassoni, C., Regondi, M., Biasi, S. & Spreafico, R. (1997). GABAergic neurons in mammalian thalamus: A marker of thalamic complexity? Brain Research Bulletin 42, 2737.
Baden, T., Berens, P., Franke, K., Rosón, M.R., Bethge, M. & Euler, T. (2016). The functional diversity of retinal ganglion cells in the mouse. Nature 529, 345350.
Bickford, M.E. (2015). Thalamic circuit diversity: Modulation of the driver/modulator framework. Frontiers in Neural Circuits 9, 86.
Bickford, M.E., Slusarczyk, A., Dilger, E.K., Krahe, T.E., Kucuk, C. & Guido, W. (2010). Synaptic development of the mouse dorsal lateral geniculate nucleus. The Journal of Comparative Neurology 518, 622635.
Bickford, M.E., Zhou, N., Krahe, T.E., Govindaiah, G. & Guido, W. (2015). Retinal and tectal “driver-like” inputs converge in the shell of the mouse dorsal lateral geniculate nucleus. The Journal of Neuroscience 35, 1052310534.
Blasiak, A., Blasiak, T. & Lewandowski, M. (2009). Electrophysiology and pharmacology of the optic input to the rat intergeniculate leaflet in vitro . Acta Physiologica Polonica 60, 171.
Born, G. & Schmidt, M. (2007). GABAergic pathways in the rat subcortical visual system: A comparative study in vivo and in vitro . European Journal of Neuroscience 26, 11831192.
Bourassa, J. & Deschênes, M. (1995). Corticothalamic projections from the primary visual cortex in rats: A single fiber study using biocytin as an anterograde tracer. Neuroscience 66, 253263.
Braak, H. & Bachmann, A. (1985). The percentage of projection neurons and interneurons in the human lateral geniculate nucleus. Human Neurobiology 4, 9195.
Brauer, K. & Schober, W. (1982). Identification of geniculo-tectal relay neurons in the rat’s ventral lateral geniculate nucleus. Experimental Brain Research 45, 8488.
Brauer, K., Schober, W., Leibnitz, L., Werner, L., Lüth, H. & Winkelmann, E. (1983). The ventral lateral geniculate nucleus of the albino rat morphological and histochemical observations. Journal fur Hirnforschung 25, 205236.
Briggs, F. & Usrey, W.M. (2008). Emerging views of corticothalamic function. Current Opinion in Neurobiology 18, 403407.
Brooks, J.M., Su, J., Levy, C., Wang, J.S., Seabrook, T.A., Guido, W. & Fox, M.A. (2013). A molecular mechanism regulating the timing of corticogeniculate innervation. Cell Reports 5, 573581.
Cadusseau, J. & Roger, M. (1991). Cortical and subcortical connections of the pars compacta of the anterior pretectal nucleus in the rat. Neuroscience Research 12, 83100.
Cang, J. & Feldheim, D.A. (2013). Developmental mechanisms of topographic map formation and alignment. Annual Review of Neuroscience 36, 5177.
Card, J.P. & Moore, R.Y. (1982). Ventral lateral geniculate nucleus efferents to the rat suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity. Journal of Comparative Neurology 206, 390396.
Card, J.P. & Moore, R.Y. (1989). Organization of lateral geniculate-hypothalamic connections in the rat. Journal of Comparative Neurology 284, 135147.
Cetin, A. & Callaway, E.M. (2014). Optical control of retrogradely infected neurons using drug-regulated “TLoop” lentiviral vectors. Journal of Neurophysiology 111, 21502159.
Cosenza, R.M. & Moore, R.Y. (1984). Afferent connections of the ventral lateral geniculate nucleus in the rat: An HRP study. Brain Research 310, 367370.
Crabtree, J.W. & Killackey, H.P. (1989). The topographic organization and axis of projection within the visual sector of the rabbit’s thalamic reticular nucleus. European Journal of Neuroscience 1, 94109.
Cruz-Martín, A., El-Danaf, R.N., Osakada, F., Sriram, B., Dhande, O.S., Nguyen, P.L., Callaway, E.M., Ghosh, A. & Huberman, A.D. (2014). A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507, 358361.
De Lima, A.D. & Singer, W. (1987). The serotoninergic fibers in the dorsal lateral geniculate nucleus of the cat: Distribution and synaptic connections demonstrated with immunocytochemistry. Journal of Comparative Neurology 258, 339351.
de Lima, D.A., Montero, V. & Singer, W. (1985). The cholinergic innervation of the visual thalamus: An EM immunocytochemical study. Experimental Brain Research 59, 206212.
Delaunay, D., Heydon, K., Miguez, A., Schwab, M., Nave, K.A., Thomas, J.L., Spassky, N., Martinez, S. & Zalc, B. (2009). Genetic tracing of subpopulation neurons in the prethalamus of mice (Mus musculus). Journal of Comparative Neurology 512, 7483.
Demas, J., Sagdullaev, B.T., Green, E., Jaubert-Miazza, L., McCall, M.A., Gregg, R.G., Wong, R.O. & Guido, W. (2006). Failure to maintain eye-specific segregation in nob, a mutant with abnormally patterned retinal activity. Neuron 50, 247259.
Dhande, O.S., Estevez, M.E., Quattrochi, L.E., El-Danaf, R.N., Nguyen, P.L., Berson, D.M. & Huberman, A.D. (2013). Genetic dissection of retinal inputs to brainstem nuclei controlling image stabilization. The Journal of Neuroscience 33, 1779717813.
Dhande, O.S. & Huberman, A.D. (2014). Retinal ganglion cell maps in the brain: Implications for visual processing. Current Opinion in Neurobiology 24, 133142.
Dilger, E.K., Krahe, T.E., Morhardt, D.R., Seabrook, T.A., Shin, H-S. & Guido, W. (2015). Absence of plateau potentials in dLGN cells leads to a breakdown in retinogeniculate refinement. Journal of Neuroscience 35, 36523662.
Dubin, M.W. & Cleland, B.G. (1977). Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. Journal of Neurophysiology 40, 410427.
Ecker, J.L., Dumitrescu, O.N., Wong, K.Y., Alam, N.M., Chen, S-K., LeGates, T., Renna, J.M., Prusky, G.T., Berson, D.M. & Hattar, S. (2010). Melanopsin-expressing retinal ganglion-cell photoreceptors: Cellular diversity and role in pattern vision. Neuron 67, 4960.
Ellis, E.M., Gauvain, G., Sivyer, B. & Murphy, G.J. (2016). Shared and distinct retinal input to the mouse superior colliculus and dorsal lateral geniculate nucleus. Journal of Neurophysiology 116, 602610.
Emerson, V., Chalupa, L., Thompson, I. & Talbot, R. (1982). Behavioural, physiological, and anatomical consequences of monocular deprivation in the golden hamster (Mesocricetus auratus). Experimental Brain Research 45, 168178.
Engelund, A., Fahrenkrug, J., Harrison, A. & Hannibal, J. (2010). Vesicular glutamate transporter 2 (VGLUT2) is co-stored with PACAP in projections from the rat melanopsin-containing retinal ganglion cells. Cell and Tissue Research 340, 243255.
Erzurumlu, R.S., Jhaveri, S. & Schneider, G.E. (1988). Distribution of morphologically different retinal axon terminals in the hamster dorsal lateral geniculate nucleus. Brain Research 461, 175181.
Estevez, M.E., Fogerson, P.M., Ilardi, M.C., Borghuis, B.G., Chan, E., Weng, S., Auferkorte, O.N., Demb, J.B. & Berson, D.M. (2012). Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. Journal of Neuroscience 32, 1360813620.
Feldheim, D.A., Vanderhaeghen, P., Hansen, M.J., Frisén, J., Lu, Q., Barbacid, M. & Flanagan, J.G. (1998). Topographic guidance labels in a sensory projection to the forebrain. Neuron 21, 13031313.
Fox, M.A. & Guido, W. (2011). Shedding light on class-specific wiring: Development of intrinsically photosensitive retinal ganglion cell circuitry. Molecular Neurobiology 44, 321329.
Fremeau, R.T., Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D., Storm-Mathisen, J. & Edwards, R.H. (2001). The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31, 247260.
Friedlander, M., Lin, C. & Sherman, S. (1980). Dendritic and axonal morphology of physiological classes of geniculo-cortical relay cells. In Experimental Brain Research (Vol. 41, No. 1, pp. A3-A3). 175 Springer Verlag, New York, US.
Friedlander, M., Lin, C., Stanford, L. & Sherman, S.M. (1981). Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80129.
Fujiyama, F., Hioki, H., Tomioka, R., Taki, K., Tamamaki, N., Nomura, S., Okamoto, K. & Kaneko, T. (2003). Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation. Journal of Comparative Neurology 465, 234249.
Gabbott, P. & Bacon, S. (1994a). An oriented framework of neuronal processes in the ventral lateral geniculate nucleus of the rat demonstrated by NADPH diaphorase histochemistry and GABA immunocytochemistry. Neuroscience 60, 417440.
Gabbott, P.L. & Bacon, S.J. (1994b). Two types of interneuron in the dorsal lateral geniculate nucleus of the rat: A combined NADPH diaphorase histochemical and GABA immunocytochemical study. Journal of Comparative Neurology 350, 281301.
Gaillard, F., Karten, H.J. & Sauvé, Y. (2013). Retinorecipient areas in the diurnal murine rodent Arvicanthis niloticus: A disproportionally large superior colliculus. Journal of Comparative Neurology 521, 16991726.
Glees, P. & le Gros Clark, W. (1941). The termination of optic fibres in the lateral geniculate body of the monkey. Journal of Anatomy 75, 295.
Godement, P., Salaün, J. & Imbert, M. (1984). Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. Journal of Comparative Neurology 230, 552575.
Golding, B., Pouchelon, G., Bellone, C., Murthy, S., Di Nardo, A.A., Govindan, S., Ogawa, M., Shimogori, T., Lüscher, C. & Dayer, A. (2014). Retinal input directs the recruitment of inhibitory interneurons into thalamic visual circuits. Neuron 81, 10571069.
Grant, E., Hoerder-Suabedissen, A. & Molnár, Z. (2016). The regulation of corticofugal fiber targeting by retinal inputs. Cerebral Cortex 26, 13361348.
Grubb, M.S. & Thompson, I.D. (2004). Biochemical and anatomical subdivision of the dorsal lateral geniculate nucleus in normal mice and in mice lacking the β2 subunit of the nicotinic acetylcholine receptor. Vision Research 44, 33653376.
Guido, W. (2008). Refinement of the retinogeniculate pathway. The Journal of Physiology 586, 43574362.
Guillery, R. (1969). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschrift für Zellforschung und mikroskopische Anatomie 96, 138.
Guillery, R. & Harting, J.K. (2003). Structure and connections of the thalamic reticular nucleus: Advancing views over half a century. Journal of Comparative Neurology 463, 360371.
Hale, P., Sefton, A.J., Baur, L. & Cottee, L. (1982). Interrelations of the rat’s thalamic reticular and dorsal lateral geniculate nuclei. Experimental Brain Research 45, 217229.
Hallanger, A.E., Levey, A.I., Lee, H.J., Rye, D.B. & Wainer, B.H. (1987). The origins of cholinergic and other subcortical afferents to the thalamus in the rat. Journal of Comparative Neurology 262, 105124.
Hammer, S., Carrillo, G.L., Govindaiah, G., Monavarfeshani, A., Bircher, J.S., Su, J., Guido, W. & Fox, M.A. (2014). Nuclei-specific differences in nerve terminal distribution, morphology, and development in mouse visual thalamus. Neural Development 9, 1.
Hammer, S., Monavarfeshani, A., Lemon, T., Su, J. & Fox, M.A. (2015). Multiple retinal axons converge onto relay cells in the adult mouse thalamus. Cell Reports 12, 15751583.
Harrington, M., DeCoursey, P., Bruce, D. & Buggy, J. (1987). Circadian pacemaker (SCN) transplants into lateral ventricles fail to restore locomotor rhythmicity in arrhythmic hamsters. Soc Neurosci Abstr 13, 465472.
Harrington, M.E. (1997). The ventral lateral geniculate nucleus and the intergeniculate leaflet: Interrelated structures in the visual and circadian systems. Neuroscience & Biobehavioral Reviews 21, 705727.
Harrington, M.E. & Rusak, B. (1986). Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. Journal of Biological Rhythms 1, 309325.
Harting, J.K., Huerta, M.F., Hashikawa, T. & van Lieshout, D.P. (1991a). Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. Journal of Comparative Neurology 304, 275306.
Harting, J.K., Van Lieshout, D., Hashikawa, T. & Weber, J. (1991b). The parabigeminogeniculate projection: Connectional studies in eight mammals. Journal of Comparative Neurology 305, 559581.
Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K.W. & Berson, D.M. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. Journal of Comparative Neurology 497, 326349.
Hickey, T. & Spear, P. (1976). Retinogeniculate projections in hooded and albino rats: An autoradiographic study. Experimental Brain Research 24, 523529.
Holcombe, V. & Guillery, R. (1984). The organization of retinal maps within the dorsal and ventral lateral geniculate nuclei of the rabbit. Journal of Comparative Neurology 225, 469491.
Hong, Y.K. & Chen, C. (2011). Wiring and rewiring of the retinogeniculate synapse. Current Opinion in Neurobiology 21, 228237.
Horel, J.A. (1968). Effects of subcortical lesions on brightness discrimination acquired by rats without visual cortex. Journal of Comparative and Physiological Psychology 65, 103.
Horowitz, S.S., Blanchard, J.H. & Morin, L.P. (2004). Intergeniculate leaflet and ventral lateral geniculate nucleus afferent connections: An anatomical substrate for functional input from the vestibulo-visuomotor system. Journal of Comparative Neurology 474, 227245.
Huberman, A.D., Feller, M.B. & Chapman, B. (2008a). Mechanisms underlying development of visual maps and receptive fields. Annual Review of Neuroscience 31, 479509.
Huberman, A.D., Manu, M., Koch, S.M., Susman, M.W., Lutz, A.B., Ullian, E.M., Baccus, S.A. & Barres, B.A. (2008b). Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59, 425438.
Huberman, A.D., Wei, W., Elstrott, J., Stafford, B.K., Feller, M.B. & Barres, B.A. (2009). Genetic identification of an on–off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62, 327334.
Inamura, N., Ono, K., Takebayashi, H., Zalc, B. & Ikenaka, K. (2011). Olig2 lineage cells generate GABAergic neurons in the prethalamic nuclei, including the zona incerta, ventral lateral geniculate nucleus and reticular thalamic nucleus. Developmental Neuroscience 33, 118129.
Irvin, G.E., Casagrande, V.A. & Norton, T.T. (1993). Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus. Visual Neuroscience 10, 363373.
Jacobs, E.C., Campagnoni, C., Kampf, K., Reyes, S.D., Kalra, V., Handley, V., Xie, Y.Y., Hong-Hu, Y., Spreur, V. & Fisher, R.S. (2007). Visualization of corticofugal projections during early cortical development in a τ-GFP-transgenic mouse. European Journal of Neuroscience 25, 1730.
Jager, P., Ye, Z., Yu, X., Zagoraiou, L., Prekop, H-T., Partanen, J., Jessell, T.M., Wisden, W., Brickley, S.G. & Delogu, A. (2016). Tectal-derived interneurons contribute to phasic and tonic inhibition in the visual thalamus. Nature Communications 7, 13579.
Jaubert-Miazza, L., Green, E., Lo, F., Bui, K., Mills, J. & Guido, W. (2005). Structural and functional composition of the developing retinogeniculate pathway in the mouse. Visual Neuroscience 22, 661.
Jones, E.G. (2012). The Thalamus. Springer Science & Business Media, Berlin, Germany.
Jones, E.G. & Rubenstein, J.L. (2004). Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. Journal of Comparative Neurology 477, 5580.
Jurgens, C.W., Bell, K.A., McQuiston, A.R. & Guido, W. (2012). Optogenetic stimulation of the corticothalamic pathway affects relay cells and GABAergic neurons differently in the mouse visual thalamus. PLoS One 7, e45717.
Kaas, J., Guillery, R. & Allman, J. (1972). Some principles of organization in the dorsal lateral geniculate nucleus. Brain, Behavior and Evolution 6, 283299.
Kay, J.N., De la Huerta, I., Kim, I-J., Zhang, Y., Yamagata, M., Chu, M.W., Meister, M. & Sanes, J.R. (2011). Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. The Journal of Neuroscience 31, 77537762.
Kim, I-J., Zhang, Y., Meister, M. & Sanes, J.R. (2010). Laminar restriction of retinal ganglion cell dendrites and axons: Subtype-specific developmental patterns revealed with transgenic markers. The Journal of Neuroscience 30, 14521462.
Kim, I-J., Zhang, Y., Yamagata, M., Meister, M. & Sanes, J.R. (2008). Molecular identification of a retinal cell type that responds to upward motion. Nature 452, 478482.
Kolmac, C.I., Power, B.D. & Mitrofanis, J. (2000). Dorsal thalamic connections of the ventral lateral geniculate nucleus of rats. Journal of Neurocytology 29, 3141.
Kopp, M.D., Meissl, H., Dehghani, F. & Korf, H.W. (2001). The pituitary adenylate cyclase-activating polypeptide modulates glutamatergic calcium signalling: Investigations on rat suprachiasmatic nucleus neurons. Journal of Neurochemistry 79, 161171.
Krahe, T.E., El-Danaf, R.N., Dilger, E.K., Henderson, S.C. & Guido, W. (2011). Morphologically distinct classes of relay cells exhibit regional preferences in the dorsal lateral geniculate nucleus of the mouse. The Journal of Neuroscience 31, 1743717448.
Legg, C. & Cowey, A. (1977a). Effects of subcortical lesions on visual intensity discriminations in rats. Physiology & Behavior 19, 635646.
Legg, C. & Cowey, A. (1977b). The role of the ventral lateral geniculate nucleus and posterior thalamus in intensity discrimination in rats. Brain Research 123, 261273.
Leist, M., Datunashvilli, M., Kanyshkova, T., Zobeiri, M., Aissaoui, A., Cerina, M., Romanelli, M.N., Pape, H-C. & Budde, T. (2016). Two types of interneurons in the mouse lateral geniculate nucleus are characterized by different h-current density. Scientific Reports 6, 24904.
Lewandowski, M.H. & Usarek, A. (2002). Effects of intergeniculate leaflet lesions on circadian rhythms in the mouse. Behavioural Brain Research 128, 1317.
Ling, C., Hendrickson, M.L. & Kalil, R.E. (2012). Morphology, classification, and distribution of the projection neurons in the dorsal lateral geniculate nucleus of the rat. PloS One 7, e49161.
López-Bendito, G. & Molnár, Z. (2003). Thalamocortical development: How are we going to get there? Nature Reviews Neuroscience 4, 276289.
Lund, R. & Cunningham, T. (1972). Aspects of synaptic and laminar organization of the mammalian lateral geniculate body. Investigative Ophthalmology 11, 291302.
Mackay-Sim, A., Sefton, A.J. & Martin, P.R. (1983). Subcortical projections to lateral geniculate and thalamic reticular nuclei in the hooded rat. Journal of Comparative Neurology 213, 2435.
Martersteck, E.M., Hirokawa, K.E., Evarts, M., Bernard, A., Duan, X., Li, Y., Ng, L., Oh, S.W., Ouellette, B. & Royall, J.J. (2017). Diverse central projection patterns of retinal ganglion cells. Cell Reports 18, 20582072.
Martinez, L.M., Molano-Mazón, M., Wang, X., Sommer, F.T. & Hirsch, J.A. (2014). Statistical wiring of thalamic receptive fields optimizes spatial sampling of the retinal image. Neuron 81, 943956.
Matute, C. & Streit, P. (1985). Selective retrograde labeling with D-[3H]-aspartate in afferents to the mammalian superior colliculus. Journal of Comparative Neurology 241, 3449.
McCormick, D.A. (1992). Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Progress in Neurobiology 39, 337388.
Michel, S., Itri, J., Han, J.H., Gniotczynski, K. & Colwell, C.S. (2006). Regulation of glutamatergic signalling by PACAP in the mammalian suprachiasmatic nucleus. BMC Neuroscience 7, 15.
Mikkelsen, J. (1992). The organization of the crossed geniculogeniculate pathway of the rat: A Phaseolus vulgaris-leucoagglutinin study. Neuroscience 48, 953962.
Mize, R.R. & Horner, L.H. (1984). Retinal synapses of the cat medial interlaminar nucleus and ventral lateral geniculate nucleus differ in size and synaptic organization. Journal of Comparative Neurology 224, 579590.
Montera, V. & Zempel, J. (1985). Evidence for two types of GABA-containing interneurons in the a-laminae of the cat lateral geniculate nucleus: A double-label HRP and GABA-immunocytochemical study. Experimental Brain Research 60, 603609.
Montero, V. & Singer, W. (1985). Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Experimental Brain Research 59, 151165.
Moore, R.Y. & Card, J.P. (1994). Intergeniculate leaflet: An anatomically and functionally distinct subdivision of the lateral geniculate complex. Journal of Comparative Neurology 344, 403430.
Moore, R.Y. & Speh, J.C. (1993). GABA is the principal neurotransmitter of the circadian system. Neuroscience Letters 150, 112116.
Moore, R.Y., Weis, R. & Moga, M.M. (2000). Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. Journal of Comparative Neurology 420, 398418.
Morgan, J.L., Berger, D.R., Wetzel, A.W. & Lichtman, J.W. (2016). The fuzzy logic of network connectivity in mouse visual thalamus. Cell 165, 192206.
Morin, L. & Blanchard, J. (1998). Interconnections among nuclei of the subcortical visual shell: The intergeniculate leaflet is a major constituent of the hamster subcortical visual system. Journal of Comparative Neurology 396, 288309.
Morin, L. & Blanchard, J. (1999). Forebrain connections of the hamster intergeniculate leaflet: Comparison with those of ventral lateral geniculate nucleus and retina. Visual Neuroscience 16, 10371054.
Morin, L.P. (2013). Neuroanatomy of the extended circadian rhythm system. Experimental Neurology 243, 420.
Morin, L.P. & Studholme, K.M. (2014). Retinofugal projections in the mouse. Journal of Comparative Neurology 522, 37333753.
Muir-Robinson, G., Hwang, B.J. & Feller, M.B. (2002). Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. The Journal of Neuroscience 22, 52595264.
Nakagawa, Y. & Shimogori, T. (2012). Diversity of thalamic progenitor cells and postmitotic neurons. European Journal of Neuroscience 35, 15541562.
Nakamura, H. & Kawamura, S. (1988). The ventral lateral geniculate nucleus in the cat: Thalamic and commissural connections revealed by the use of WGA-HRP transport. Journal of Comparative Neurology 277, 509528.
Nassi, J.J. & Callaway, E.M. (2009). Parallel processing strategies of the primate visual system. Nature Reviews Neuroscience 10, 360372.
Niimi, K., Kanaseki, T. & Takimoto, T. (1963). The comparative anatomy of the ventral nucleus of the lateral geniculate body in mammals. Journal of Comparative Neurology 121, 313323.
Olsen, S.R., Bortone, D.S., Adesnik, H. & Scanziani, M. (2012). Gain control by layer six in cortical circuits of vision. Nature 483, 4752.
Osterhout, J.A., Josten, N., Yamada, J., Pan, F., Wu, S-w., Nguyen, P.L., Panagiotakos, G., Inoue, Y.U., Egusa, S.F. & Volgyi, B. (2011). Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 71, 632639.
Papadopoulos, G.C. & Parnavelas, J.G. (1990a). Distribution and synaptic organization of dopaminergic axons in the lateral geniculate nucleus of the rat. Journal of Comparative Neurology 294, 356361.
Papadopoulos, G.C. & Parnavelas, J.G. (1990b). Distribution and synaptic organization of serotoninergic and noradrenergic axons in the lateral geniculate nucleus of the rat. Journal of Comparative Neurology 294, 345355.
Petrof, I. & Sherman, S.M. (2013). Functional significance of synaptic terminal size in glutamatergic sensory pathways in thalamus and cortex. The Journal of physiology 591, 31253131.
Pfeiffenberger, C., Yamada, J. & Feldheim, D.A. (2006). Ephrin-As and patterned retinal activity act together in the development of topographic maps in the primary visual system. The Journal of Neuroscience 26, 1287312884.
Pinault, D. (2004). The thalamic reticular nucleus: Structure, function and concept. Brain Research Reviews 46, 131.
Piscopo, D.M., El-Danaf, R.N., Huberman, A.D. & Niell, C.M. (2013). Diverse visual features encoded in mouse lateral geniculate nucleus. The Journal of Neuroscience 33, 46424656.
Puelles, L. & Rubenstein, J.L. (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends in Neurosciences 26, 469476.
Rafols, J.A. & Valverde, F. (1973). The structure of the dorsal lateral geniculate nucleus in the mouse. A golgi and electron microscopic study. Journal of Comparative Neurology 150, 303331.
Rebsam, A., Bhansali, P. & Mason, C.A. (2012). Eye-specific projections of retinogeniculate axons are altered in albino mice. Journal of Neuroscience 32, 48214826.
Rebsam, A., Petros, T.J. & Mason, C.A. (2009). Switching retinogeniculate axon laterality leads to normal targeting but abnormal eye-specific segregation that is activity dependent. Journal of Neuroscience 29, 1485514863.
Reese, B. (1988). ‘Hidden lamination’ in the dorsal lateral geniculate nucleus: The functional organization of this thalamic region in the rat. Brain Research Reviews 13, 119137.
Reese, B. & Cowey, A. (1983). Projection lines and the ipsilateral retino-geniculate pathway in the hooded rat. Neuroscience 10, 12331247.
Ribak, C.E. & Peters, A. (1975). An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Research 92, 341368.
Rivlin-Etzion, M., Zhou, K., Wei, W., Elstrott, J., Nguyen, P.L., Barres, B.A., Huberman, A.D. & Feller, M.B. (2011). Transgenic mice reveal unexpected diversity of on-off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. The Journal of Neuroscience 31, 87608769.
Rompani, S.B., Müllner, F.E., Wanner, A., Zhang, C., Roth, C.N., Yonehara, K. & Roska, B. (2017). Different modes of visual integration in the lateral geniculate nucleus revealed by single-cell-initiated transsynaptic tracing. Neuron 93, 767776. e766.
Roth, M.M., Dahmen, J.C., Muir, D.R., Imhof, F., Martini, F.J. & Hofer, S.B. (2016). Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex. Nature Neuroscience 19, 299307.
Sanes, J.R. & Masland, R.H. (2015). The types of retinal ganglion cells: Current status and implications for neuronal classification. Annual Review of Neuroscience 38, 221246.
Schmidt, T.M., Chen, S-K. & Hattar, S. (2011). Intrinsically photosensitive retinal ganglion cells: Many subtypes, diverse functions. Trends in Neurosciences 34, 572580.
Seabrook, T.A., El-Danaf, R.N., Krahe, T.E., Fox, M.A. & Guido, W. (2013a). Retinal input regulates the timing of corticogeniculate innervation. The Journal of Neuroscience 33, 1008510097.
Seabrook, T.A., Krahe, T.E., Govindaiah, G. & Guido, W. (2013b). Interneurons in the mouse visual thalamus maintain a high degree of retinal convergence throughout postnatal development. Neural Development 8, 1.
Shanks, J.A., Ito, S., Schaevitz, L., Yamada, J., Chen, B., Litke, A. & Feldheim, D.A. (2016). Corticothalamic axons are essential for retinal ganglion cell axon targeting to the mouse dorsal lateral geniculate nucleus. The Journal of Neuroscience 36, 52525263.
Sherman, S.M. (1985). Functional organization of the W-, X-, and Y-cell pathways in the cat: A review and hypothesis. Progress in Psychobiology and Physiological Psychology 11, 233314.
Sherman, S.M. (2004). Interneurons and triadic circuitry of the thalamus. Trends in Neurosciences 27, 670675.
Sherman, S.M. (2005). Thalamic relays and cortical functioning. Progress in Brain Research 149, 107126.
Sherman, S.M. (2016). Thalamus plays a central role in ongoing cortical functioning. Nature Neuroscience 16, 533541.
Sherman, S.M. & Guillery, R. (2002). The role of the thalamus in the flow of information to the cortex. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 357, 16951708.
Singh, R., Su, J., Brooks, J., Terauchi, A., Umemori, H. & Fox, M.A. (2012). Fibroblast growth factor 22 contributes to the development of retinal nerve terminals in the dorsal lateral geniculate nucleus. Frontiers in molecular neuroscience 4, 61.
Stelzner, D.J., Baisden, R.H. & Goodman, D.C. (1976). The ventral lateral geniculate nucleus, pars lateralis of the rat. Cell and Tissue Research 170, 435454.
Stevens, B., Allen, N.J., Vazquez, L.E., Howell, G.R., Christopherson, K.S., Nouri, N., Micheva, K.D., Mehalow, A.K., Huberman, A.D. & Stafford, B. (2007). The classical complement cascade mediates CNS synapse elimination. Cell 131, 11641178.
Su, J., Haner, C.V., Imbery, T.E., Brooks, J.M., Morhardt, D.R., Gorse, K., Guido, W. & Fox, M.A. (2011). Reelin is required for class-specific retinogeniculate targeting. The Journal of Neuroscience 31, 575586.
Su, J., Klemm, M.A., Josephson, A.M. & Fox, M.A. (2013). Contributions of VLDLR and LRP8 in the establishment of retinogeniculate projections. Neural Development 8, 1.
Swanson, L., Cowan, W. & Jones, E. (1974). An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. Journal of Comparative Neurology 156, 143163.
Taylor, A., Jeffery, G. & Lieberman, A. (1986). Subcortical afferent and efferent connections of the superior colliculus in the rat and comparisons between albino and pigmented strains. Experimental Brain Research 62, 131142.
Thankachan, S. & Rusak, B. (2005). Juxtacellular recording/labeling analysis of physiological and anatomical characteristics of rat intergeniculate leaflet neurons. The Journal of Neuroscience 25, 91959204.
Thompson, A.D., Picard, N., Min, L., Fagiolini, M. & Chen, C. (2016). Cortical feedback regulates feedforward retinogeniculate refinement. Neuron 91, 10211033.
Towns, L.C., Burton, S., Kimberly, C. & Fetterman, M. (1982). Projections of the dorsal lateral geniculate and lateral posterior nuclei to visual cortex in the rabbit. Journal of Comparative Neurology 210, 8798.
Triplett, J.W., Wei, W., Gonzalez, C., Sweeney, N.T., Huberman, A.D., Feller, M.B. & Feldheim, D.A. (2014). Dendritic and axonal targeting patterns of a genetically-specified class of retinal ganglion cells that participate in image-forming circuits. Neural Development 9, 2.
Van Hooser, S.D. & Nelson, S.B. (2006). The squirrel as a rodent model of the human visual system. Visual Neuroscience 23, 765778.
Virolainen, S-M., Achim, K., Peltopuro, P., Salminen, M. & Partanen, J. (2012). Transcriptional regulatory mechanisms underlying the GABAergic neuron fate in different diencephalic prosomeres. Development 139, 37953805.
Vrang, N., Mrosovsky, N. & Mikkelsen, J.D. (2003). Afferent projections to the hamster intergeniculate leaflet demonstrated by retrograde and anterograde tracing. Brain Research Bulletin 59, 267288.
Vue, T.Y., Aaker, J., Taniguchi, A., Kazemzadeh, C., Skidmore, J.M., Martin, D.M., Martin, J.F., Treier, M. & Nakagawa, Y. (2007). Characterization of progenitor domains in the developing mouse thalamus. Journal of Comparative Neurology 505, 7391.
Wang, S., Eisenback, M., Datskovskaia, A., Boyce, M. & Bickford, M.E. (2002). GABAergic pretectal terminals contact GABAergic interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience Letters 323, 141145.
Weyand, T.G. (2016). The multifunctional lateral geniculate nucleus. Reviews in the neurosciences 27, 135157.
Wilson, J., Friedlander, M. & Sherman, S. (1984). Fine structural morphology of identified X- and Y-cells in the cat’s lateral geniculate nucleus. Proceedings of the Royal Society of London Series B, Biological Sciences 221, 411436.
Xu, H-p., Furman, M., Mineur, Y.S., Chen, H., King, S.L., Zenisek, D., Zhou, Z.J., Butts, D.A., Tian, N., Picciotto, M.R. & Crair, M.C. (2011). An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 70, 11151127.
Yuge, K., Kataoka, A., Yoshida, A.C., Itoh, D., Aggarwal, M., Mori, S., Blackshaw, S. & Shimogori, T. (2011). Region-specific gene expression in early postnatal mouse thalamus. Journal of Comparative Neurology 519, 544561.
Zhang, J., Ackman, J.B., Xu, H-P. & Crair, M.C. (2012). Visual map development depends on the temporal pattern of binocular activity in mice. Nature Neuroscience 15, 298307.
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Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
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