Nuclei-specific differences in nerve terminal distribution, morphology, and development in mouse visual thalamus

Neural Development

Volumn 9, Issue 1, 2014, Pages

  Hammer, Sarah ^a,b   Carrillo, Gabriela L ^a,c   Govindaiah, Gubbi ^d   Monavarfeshani, Aboozar ^a,c   Bircher, Joseph S ^a   Su, Jianmin ^a   Guido, William ^d   Fox, Michael A ^a,c  

^a VIRGINIA TECH CARILION SCHOOL OF MEDICINE   (United States)

^b Roanoke Valley Governor's School for Science and Technology   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d University of Louisville School of Medicine   (United States)

Author keywords

Axon; Lateral geniculate nucleus; Nerve terminal; Retina; Retinal terminal; Retinogeniculate; Thalamus

Indexed keywords

CHOLERA TOXIN B SUBUNIT; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; GREEN FLUORESCENT PROTEIN; NEUROTRANSMITTER; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VESICULAR NEUROTRANSMITTER TRANSPORTER; GLUTAMATE DECARBOXYLASE;

ADULT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETIC ANALYSIS; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LATERAL GENICULATE BODY; MORPHOLOGY; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NERVE FIBER TRANSPORT; NERVE GROWTH; NERVE POTENTIAL; NERVE STIMULATION; NONHUMAN; OLIVARY NUCLEUS; OPTIC TRACT; PRIORITY JOURNAL; RETINA; RETINA NERVE CELL; SCANNING ELECTRON MICROSCOPY; SERIAL BLOCK FACE SCANNING ELECTRON MICROSCOPY; SUPERIOR COLLICULUS; SUPRACHIASMATIC NUCLEUS; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; THALAMUS NUCLEUS; VISUAL THALAMUS; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; ELECTROSTIMULATION; GENICULATE BODY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL INHIBITION; PHYSIOLOGY; SYNAPTOSOME; ULTRASTRUCTURE; VISUAL SYSTEM;

ANIMALS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GENICULATE BODIES; GLUTAMATE DECARBOXYLASE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; OPTIC TRACT; PRESYNAPTIC TERMINALS; VISUAL PATHWAYS;

EID: 84903866880     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-9-16     Document Type: Article

References (80)

1. Sherman SM, Guillery RW. The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci 2002, 357:1695-1708.
2. Sherman SM. Interneurons and triadic circuitry of the thalamus. Trends Neurosci 2004, 27:670-675.
3. Erisir A, Van Horn SC, Bickford ME, Sherman SM. Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: a comparison with corticogeniculate terminals. J Comp Neurol 1997, 377:535-549.
4. Erisir A, Van Horn SC, Sherman SM. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc Natl Acad Sci U S A 1997, 94:1517-1520.
5. Van Horn SC, Erisir A, Sherman SM. Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 2000, 416:509-520.
6. Bickford ME, Slusarczyk A, Dilger EK, Krahe TE, Kucuk C, Guido W. Synaptic development of the mouse dorsal lateral geniculate nucleus. J Comp Neurol 2010, 518:622-635.
7. Fitzpatrick D, Penny GR, Schmechel DE. Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 1984, 4:1809-1829.
8. Montero VM, Singer W. Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res 1985, 59:151-165.
9. Gabbott PL, Somogyi J, Stewart MG, Hamori J. GABA-immunoreactive neurons in the dorsal lateral geniculate nucleus of the rat: characterization by combined Golgi-impregnation and immunocytochemistry. Exp Brain Res 1986, 61:311-322.
10. Moore RY, Speh JC. GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 1993, 150:112-116.
11. Fremeau RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 2001, 31:247-260.
12. Land PW, Kyonka E, Shamalla-Hannah L. Vesicular glutamate transporters in the lateral geniculate nucleus: expression of VGLUT2 by retinal terminals. Brain Res 2004, 996:251-254.
13. Guillery RW. The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z Zellforsch Mikrosk Anat 1969, 96:1-38.
14. Lund RD, Cunningham TJ. Aspects of synaptic and laminar organization of the mammalian lateral geniculate body. Invest Ophthalmol 1972, 11:291-302.
15. Robson JA, Mason CA. The synaptic organization of terminals traced from individual labeled retino-geniculate axons in the cat. Neuroscience 1979, 4:99-111.
16. Hamos JE, Van Horn SC, Raczkowski D, Sherman SM. Synaptic circuits involving an individual retinogeniculate axon in the cat. J Comp Neurol 1987, 259:165-192.
17. Famiglietti EV. Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Res 1970, 20:181-191.
18. Montero VM, Scott GL. Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study. Neuroscience 1981, 6:2561-2577.
19. Seabrook TA, Krahe TE, Govindaiah G, Guido W. Interneurons in the mouse visual thalamus maintain a high degree of retinal convergence throughout postnatal development. Neural Dev 2013, 8:24.
20. Rafols JA, Valverde F. The structure of the dorsal lateral geniculate nucleus in the mouse. A Golgi and electron microscopic study. J Comp Neurol 1973, 150:303-332.
21. Niimi K, Kanaseki T, Takimoto T. The comparative anatomy of the ventral nucleus of the lateral geniculate body in mammals. J Comp Neurol 1963, 121:313-323.
22. Harrington ME. The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci Biobehav Rev 1997, 21:705-727.
23. Fox MA, Guido W. Shedding light on class-specific wiring: development of intrinsically photosensitive retinal ganglion cell circuitry. Mol Neurobiol 2011, 44:321-329.
24. Cosenza RM, Moore RY. Afferent connections of the ventral lateral geniculate nucleus in the rat: an HRP study. Brain Res 1984, 310:367-370.
25. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 2006, 497:326-349.
26. 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.
27. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA. Genetic identification of an On-Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 2009, 62:327-334.
28. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR. Molecular identification of a retinal cell type that responds to upward motion. Nature 2008, 452:478-482.
29. Kim IJ, Zhang Y, Meister M, Sanes JR. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J Neurosci 2010, 30:1452-1462.
30. Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M, Chu MW, Meister M, Sanes JR. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J Neurosci 2011, 31:7753-7762.
31. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 2010, 67:49-60.
32. Osterhout JA, Josten N, Yamada J, Pan F, Wu SW, Nguyen PL, Panagiotakos G, Inoue YU, Egusa SF, Volgyi B, Inoue T, Bloomfield SA, Barres BA, Berson DM, Feldheim DA, Huberman AD. Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 2011, 71:632-639.
33. Triplett JW, Wei W, Gonzalez C, Sweeney NT, Huberman AD, Feller MB, Feldheim DA. Dendritic and axonal targeting patterns of a genetically-specified class of retinal ganglion cells that participate in image-forming circuits. Neural Dev 2014, 9:2.
34. Sweeney NT, Tierney H, Feldheim DA. Tbr2 is required to generate a neural circuit mediating the pupillary light reflex. J Neurosci 2014, 34:5447-5453.
35. Jacobs EC, Campagnoni C, Kampf K, Reyes SD, Kalra V, Handley V, Xie YY, Hong-Hu Y, Spreur V, Fisher RS, Campagnoni AT. Visualization of corticofugal projections during early cortical development in a tau-GFP-transgenic mouse. Eur J Neurosci 2007, 25:17-30.
36. Seabrook T, El Danaf R, Krahe TE, Fox MA, Guido W. Retinal input regulates the timing of corticogeniculate innervation. J Neurosci 2013, 33:10085-10097.
37. Su J, Haner CV, Imbery TE, Brooks JM, Morhardt DR, Gorse K, Guido W, Fox MA. Reelin is required for class-specific retinogeniculate targeting. J Neurosci 2011, 31:575-586.
38. Fukuda T, Aika Y, Heizmann CW, Kosaka T. GABAergic axon terminals at perisomatic and dendritic inhibitory sites show different immunoreactivities against two GAD isoforms, GAD67 and GAD65, in the mouse hippocampus: a digitized quantitative analysis. J Comp Neurol 1998, 395:177-194.
39. Hardwick C, French SJ, Southam E, Totterdell S. A comparison of possible markers for chandelier cartridges in rat medial prefrontal cortex and hippocampus. Brain Res 2005, 1031:238-244.
40. Fish KN, Sweet RA, Lewis DA. Differential distribution of proteins regulating GABA synthesis and reuptake in axon boutons of subpopulations of cortical interneurons. Cereb Cortex 2011, 21:2450-2460.
41. de Lima AD, Montero VM, Singer W. The cholinergic innervation of the visual thalamus: an EM immunocytochemical study. Exp Brain Res 1985, 59:206-212.
42. Grant E, Hoerder-Suabedissen A, Molnar Z. Development of the corticothalamic projections. Front Neurosci 2012, 6:53.
43. Bourassa J, Deschenes M. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 1995, 66:253-263.
44. Wang SW, Kim BS, Ding K, Wang H, Sun D, Johnson RL, Klein WH, Gan L. Requirement for math5 in the development of retinal ganglion cells. Genes Dev 2001, 15:24-29.
45. Brooks JM, Su J, Levy C, Wang JS, Seabrook TA, Guido W, Fox MA. A molecular mechanism regulating the timing of corticogeniculate innervation. Cell Rep 2013, 5:573-581.
46. Sherman SM, Guillery RW. On the actions that one nerve cell can have on another: distinguishing " drivers" from " modulators" . Proc Natl Acad Sci U S A 1998, 95:7121-7126.
47. Petrof I, Sherman SM. Functional significance of synaptic terminal size in glutamatergic sensory pathways in thalamus and cortex. J Physiol 2013, 591:3125-3131.
48. Su J, Klemm MA, Josephson AM, Fox MA. Contributions of VLDLR and LRP8 in the establishment of retinogeniculate projections. Neural Dev 2013, 8:11.
49. 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.
50. Reese BE. 'Hidden lamination' in the dorsal lateral geniculate nucleus: the functional organization of this thalamic region in the rat. Brain Res 1988, 472:119-137.
51. Erzurumlu RS, Jhaveri S, Schneider GE. Distribution of morphologically different retinal axon terminals in the hamster dorsal lateral geniculate nucleus. Brain Res 1988, 461:175-181.
52. Dhande OS, Huberman AD. Retinal ganglion cell maps in the brain: implications for visual processing. Curr Opin Neurobiol 2014, 24:133-142.
53. Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL, Barres BA, Huberman AD, Feller MB. Transgenic mice reveal unexpected diversity of on-off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J Neurosci 2011, 31:8760-8769.
54. Hong YK, Kim IJ, Sanes JR. Stereotyped axonal arbors of retinal ganglion cell subsets in the mouse superior colliculus. J Comp Neurol 2011, 519:1691-1711.
55. Mize RR, Horner LH. Retinal synapses of the cat medial interlaminar nucleus and ventral lateral geniculate nucleus differ in size and synaptic organization. J Comp Neurol 1984, 224:579-590.
56. 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 beta2 knock-out mice. J Neurosci 2011, 31:3384-3399.
57. Chen C, Regehr WG. Developmental remodeling of the retinogeniculate synapse. Neuron 2000, 28:955-966.
58. Stelzner DJ, Baisden RH, Goodman DC. The ventral lateral geniculate nucleus, pars lateralis of the rat. Synaptic organization and conditions for axonal sprouting. Cell Tissue Res 1976, 170:435-454.
59. Singh R, Su J, Brooks J, Terauchi A, Umemori H, Fox MA. Fibroblast growth factor 22 contributes to the development of retinal nerve terminals in the dorsal lateral geniculate nucleus. Front Mol Neurosci 2012, 4:61.
60. Guido W. Refinement of the retinogeniculate pathway. J Physiol 2008, 586:4357-4362.
61. Hong YK, Chen C. Wiring and rewiring of the retinogeniculate synapse. Curr Opin Neurobiol 2011, 21:228-237.
62. Frost DO. Anomalous visual connections to somatosensory and auditory systems following brain lesions in early life. Brain Res 1982, 255:627-635.
63. Frost DO. Development of anomalous retinal projections to nonvisual thalamic nuclei in Syrian hamsters: a quantitative study. J Comp Neurol 1986, 252:95-105.
64. Campbell G, Frost DO. Target-controlled differentiation of axon terminals and synaptic organization. Proc Natl Acad Sci U S A 1987, 84:6929-6933.
65. Campbell G, Frost DO. Synaptic organization of anomalous retinal projections to the somatosensory and auditory thalamus: target-controlled morphogenesis of axon terminals and synaptic glomeruli. J Comp Neurol 1988, 272:383-408.
66. Yang Z, Ding K, Pan L, Deng M, Gan L. Math5 determines the competence state of retinal ganglion cell progenitors. Dev Biol 2003, 264:240-254.
67. Varea E, Nacher J, Blasco-Ibanez JM, Gomez-Climent MA, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ. PSA-NCAM expression in the rat medial prefrontal cortex. Neuroscience 2005, 136:435-443.
68. Xu X, Roby KD, Callaway EM. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 2006, 499:144-160.
69. Su J, Gorse K, Ramirez F, Fox MA. Collagen XIX is expressed by interneurons and contributes to the formation of hippocampal synapses. J Comp Neurol 2010, 518:229-253.
70. Voinescu PE, Kay JN, Sanes JR. Birthdays of retinal amacrine cell subtypes are systematically related to their molecular identity and soma position. J Comp Neurol 2009, 517:737-750.
71. Fortune T, Lurie DI. Chronic low-level lead exposure affects the monoaminergic system in the mouse superior olivary complex. J Comp Neurol 2009, 513:542-558.
72. Su J, Stenbjorn RS, Gorse K, Su K, Hauser KF, Ricard-Blum S, Pihlajaniemi T, Fox MA. Target-derived matricryptins organize cerebellar synapse formation through alpha3beta1 integrins. Cell Rep 2012, 2:223-230.
73. Marcucci F, Zou DJ, Firestein S. Sequential onset of presynaptic molecules during olfactory sensory neuron maturation. J Comp Neurol 2009, 516:187-198.
74. Garbelli R, Inverardi F, Medici V, Amadeo A, Verderio C, Matteoli M, Frassoni C. Heterogeneous expression of SNAP-25 in rat and human brain. J Comp Neurol 2008, 506:373-386.
75. Jakovcevski I, Siering J, Hargus G, Karl N, Hoelters L, Djogo N, Yin S, Zecevic N, Schachner M, Irintchev A. Close homologue of adhesion molecule L1 promotes survival of Purkinje and granule cells and granule cell migration during murine cerebellar development. J Comp Neurol 2009, 513:496-510.
76. Gallart-Palau X, Tarabal O, Casanovas A, Sabado J, Correa FJ, Hereu M, Piedrafita L, Caldero J, Esquerda JE. Neuregulin-1 is concentrated in the postsynaptic subsurface cistern of C-bouton inputs to alpha-motoneurons and altered during motoneuron diseases. Faseb J 2014, [epub ahead of print].
77. Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S, Longair M, Tomancak P, Hartenstein V, Douglas RJ. TrakEM2 software for neural circuit reconstruction. PLoS ONE 2012, 7:e38011.
78. Dilger EK, Shin HS, Guido W. Requirements for synaptically evoked plateau potentials in relay cells of the dorsal lateral geniculate nucleus of the mouse. J Physiol 2011, 589:919-937.
79. Turner JP, Salt TE. Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurons in vitro. J Physiol 1998, 510(Pt 3):829-843.
80. Govindaiah, Cox CL. Synaptic activation of metabotropic glutamate receptors regulates dendritic outputs of thalamic interneurons. Neuron 2004, 41:611-623.