Differential expression of vesicular glutamate transporters 1 and 2 may identify distinct modes of glutamatergic transmission in the macaque visual system

Journal of Chemical Neuroanatomy

Volumn 50-51, Issue 1, 2013, Pages 21-38

  Balaram, Pooja ^a   Hackett, Troy A ^b   Kaas, Jon H ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lateral geniculate nucleus; Primate; Pulvinar; Superior colliculus; VGLUT; Visual cortex

Indexed keywords

CYTOCHROME C OXIDASE; MESSENGER RNA; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; GLUTAMATERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; LATERAL GENICULATE BODY; MACACA; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURE ACTIVITY RELATION; SUPERIOR COLLICULUS; SYNAPTIC TRANSMISSION; VISUAL CORTEX; VISUAL SYSTEM;

ANIMALS; BLOTTING, WESTERN; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACACA FASCICULARIS; SYNAPTIC TRANSMISSION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84877610009     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2013.02.007     Document Type: Article

References (135)

1. Adams M.M., Hof P.R., Gattass R., et al. Visual cortical projections and chemoarchitecture of macaque monkey pulvinar. Journal of Comparative Neurology 2000, 419:377-393.
2. +-dependent inorganic phosphate cotransporter. Journal of Neurochemistry 2000, 74:2622-2625.
3. Anderson J.C., Martin K.A.C. The synaptic connections between cortical areas V1 and V2 in macaque monkey. Journal of Neuroscience 2009, 29:11283-11293.
4. Balaram P., Hackett T.A., Kaas J.H. VGLUT1 mRNA and protein expression in the visual system of prosimian galagos (Otolemur garnetti). Eye Brain 2011, 3:81-98.
5. Balaram P., Takahata T., Kaas J.H. VGLUT2 mRNA and protein expression in the visual thalamus and midbrain of prosimian galagos (Otolemur garnetti). Eye Brain 2011, 3:5-15.
6. Baldwin M.K., Balaram P., Kaas J.H. Projections of the superior colliculus to the pulvinar in prosimian galagos (Otolemur garnetti) and VGLUT2 staining of the visual pulvinar. Journal of Comparative Neurology 2013, 521:1664-1682.
7. Baldwin M.K., Wong P., Reed J.L., Kaas J.H. Superior colliculus connections with visual thalamus in gray squirrels (Sciurus carolinensis): evidence for four subdivisions within the pulvinar complex. Journal of Comparative Neurology 2011, 519:1071-1094.
8. Barroso-Chinea P., Castle M., Aymerich M.S., et al. Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. Journal of Comparative Neurology 2007, 501:703-715.
9. Bellocchio E.E., Reimer R.J., Fremeau R.T., Edwards R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 2000, 289:957-960.
10. Bender D.B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Research 1983, 279:258-261.
11. Benevento L.A., Fallon J.H. The ascending projections of the superior colliculus in the rhesus monkey (Macaca Mulatta). Journal of Comparative Neurology 1975, 160:339-361.
12. Benevento L.A., Standage G.P. The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 1983, 217:307-336.
13. Benevento L.A., Yoshida K. The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 1981, 203:455-474.
14. Berman R.A., Wurtz R.H. Functional identification of a pulvinar path from superior colliculus to cortical area MT. Journal of Neuroscience 2010, 30:6342-6354.
15. Bernard A., Lubbers L.S., Tanis K.Q., et al. Transcriptional architecture of the primate neocortex. Neuron 2012, 73:1083-1099.
16. Bickford M.E., Ramcharan E., Godwin D.W., et al. Neurotransmitters contained in the subcortical extraretinal inputs to the monkey lateral geniculate nucleus. Journal of Comparative Neurology 2000, 424:701-717.
17. Blakely R.D., Edwards R.H. Vesicular and plasma membrane transporters for neurotransmitters. Cold Spring Harbor Perspectives in Biology 2012, 4:a005595.
18. Blasdel G.G., Lund J.S. Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 1983, 3:1389-1413.
19. Brodmann K. Vergleichende Lokalisationlehre der Grosshirnrinde 1909, Barth, Leipzig.
20. Bryant K.L., Suwyn C., Reding K.M., et al. Evidence for Ape and Human specializations in geniculostriate projections from VGLUT2 immunohistochemistry. Brain, Behavior and Evolution 2012, 80:210-221.
21. Bullier J., Kennedy H. Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Experimental Brain Research 1983, 53:168-172.
22. Bullier J. Communications between cortical areas of the visual system. The Visual Neurosciences 2004, 522-540. MIT Press, Cambridge, MA. L.M. Chalupa, J.S. Werner (Eds.).
23. Callaway E.M. Local circuits in primary visual cortex of the macaque monkey. Annual Review of Neuroscience 1998, 21:47-74.
24. Campos-Ortega J.A., Hayhow W.R. On the organization of the visual cortical projection to the pulvinar in Macaca mulatta. Brain, Behavior and Evolution 1972, 6:394-423.
25. Casagrande V.A., Kaas J.H. The afferent, efferent, and intrinsic connections of primary visual cortex in primates. Cerebral cortex 1994, Plenum Press. A. Peters, Rockland KS (Eds.).
26. Casagrande V.A., Khaytin I., Boyd J. The evolution of parallel visual pathways in the brains of primates. Evolution of the nervous system 2006, Elsevier, Inc. T.M. Preuss, J.H. Kaas (Eds.).
27. Casagrande V.A., Norton T.T. Lateral geniculate nucleus: a review of its physiology and function. Vision and Visual Disfunction 1991, J.R. MacMillan Press. Leventhal (Ed.).
28. Casagrande V.A., Yazar F., Jones K.D., Ding Y. The morphology of the koniocellular axon pathway in the macaque monkey. Cerebral Cortex 2007, 17:2334-2345.
29. Casagrande V.A. A third parallel visual pathway to primate area V1. Trends in Neurosciences 1994, 17:305-310.
30. Conley M., Fitzpatrick D. Morphology of retinogeniculate axons in the macaque. Visual Neuroscience 1989, 2:287-296.
31. Covic E.N., Sherman S.M. Synaptic properties of connections between the primary and secondary auditory cortices in mice. Cerebral Cortex 2011, 21:2425-2441.
32. Crick F., Koch C. Constraints on cortical and thalamic projections: the no-strong-loops hypothesis. Nature 1998, 391:245-250.
33. Cusick C.G., Scripter J.L., Darensbourg J.G., Weber J.T. Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr. Journal of Comparative Neurology 1993, 336:1-30.
34. Danbolt N.C., Storm-Mathisen J., Ottersen O.P. Sodium/potassium-coupled glutamate transporters, a newfamily of eukaryotic proteins: do they have new physiological roles and could they be new targets for pharmacological intervention?. Progress in Brain Research 1994, 100:53-60.
35. Davanger S., Manahan-Vaughan D., Mulle C., et al. Protein trafficking, targeting, and interaction at the glutamate synapse. Neuroscience 2009, 158:1-3.
36. DeYoe E.A., Van Essen D.C. Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 1985, 317:58-61.
37. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1991, 1:1-47.
38. Fitzpatrick D., Usrey W.M., Schofield B.R., Einstein G. The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex. Visual Neuroscience 1994, 11:307-315.
39. Fremeau R.T., Kam K., Qureshi T., et al. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 2004, 304:1815-1819.
40. Fremeau R.T., Troyer M.D., Pahner I., et al. The expression of vesicular glutamate transporters define two classes of excitatory synapse. Neuron 2001, 31:247-260.
41. Fremeau R.T., Voglmaier S., Seal R.P., Edwards R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends in Neurosciences 2004, 27:98-103.
42. Fremeau R.T., Burman J., Qureshi T., et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proceedings of the National Academy of Science 2002, 99:14488-14493.
43. Fries W. Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. Journal of Comparative Neurology 1984, 230:55-76.
44. Fyk-Kolodziej B., Szhagaryan A., Qin P., Pourcho R.G. Immunocytochemical localization of three vesicular glutamate transporters in the cat retina. Journal of Comparative Neurology 2004, 475:518-530.
45. Garcia-Marin V., Ahmed T.H., Afzal Y.C., Hawken M.J. Distribution of vesicular glutamate transporter 2 (VGluT2) in the primary visual cortex of the macaque and human. Journal of Comparative Neurology 2013, 521:130-151.
46. Graham J., Lin C.S., Kaas J.H. Subcortical projections of six visual cortical areas in the owl monkey, Aotus Trivirgatus. Journal of Comparative Neurology 1989, 187:557-580.
47. Graham J. Some topographical connections of the striate cortex with subcortical structures in Macaca fascicularis. Experimental Brain Research 1982, 47:1-14.
48. Gras C., Herzog E., Bellenchi G.C., Bernard V., Ravassard P., Pohl M., et al. A third vesicular glutamate transporter expressed by cholinergic and serotonergic neurons. Journal of Neuroscience 2002, 22:5442-5451.
49. Graziano A., Liu X., Murray K.D., Jones E.D. Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse. Journal of comparative neurology 2008, 507:1258-1276.
50. Gutierrez C., Yaun A., Cusick C.G. Neurochemical subdivisions of the inferior pulvinar in macaque monkeys. Journal of Comparative Neurology 1995, 363:545-562.
51. Hackett T.A., de la Mothe L.A. Regional and laminar distribution of the vesicular glutamate transporter, VGLuT2, in the macaque monkey auditory cortex. Journal of Comparative Neurology 2009, 38:106-116.
52. Hackett T.A., Takahata T., Balaram P. VGLUT1 and VGLUT2 mRNA expression in the primate auditory pathway. Hearing Research 2011, 274:129-141.
53. Harting J.K., Casagrande V.A., Weber J.T. The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate neurons. Brain Research 1978, 150:593-599.
54. Harting J.K., Huerta M.F., Frankfurter A.J., et al. Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. Journal of Comparative Neurology 1980, 192:853-882.
55. Harting J.K., Huerta M.F., Hashikawa T., Van Lieshout D.P. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. Journal of Comparative Neurology 1991, 304:275-306.
56. Hässler R. Comparative anatomy of the central visual system in day- and night-active primates. Evolution of the forebrain 1967, 419-434. Thieme, Stuttgart. Hassler, Stephen (Eds.).
57. Hendrickson A.E., Wilson J.R., Ogren M.P. The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 1978, 182:123-136.
58. Herzog E., Bellenchi G.C., Gras C., et al. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. Journal of Neuroscience 2001, 21:RC181.
59. Herzog E., Gilchrist J., Gras C., et al. Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 2004, 123:983-1002.
60. Hevner R.F., Daza R.A., Rubenstein J.L., et al. Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Developmental Neuroscience 2003, 25:139-151.
61. Hevner R.F. Layer-specific markers as probes for neuron-type identity in human neocortex and malformations of cortical development. Journal of Neuropathology and Experimental Neurology 2007, 66:101-109.
62. Hnasko T.S., Edwards R.H. Neurotransmitter corelease: mechanism and physiological role. Annual Review of Physiology 2012, 74:225-243.
63. Hubel D.H., LeVay S., Wiesel T.N. Mode of termination of retinotectal fibers in macaque monkey: an autoradiographic study. Brain Research 1975, 96:25-40.
64. Ito T., Bishop D.C., Oliver D.L. Expression of glutamate and inhibitory amino acid vesicular transporters in the rodent auditory brainstem. Journal of Comparative Neurology 2011, 519:316-340.
65. Ito T., Oliver D.L. Origins of glutamatergic terminals in the inferior colliculus identified by retrograde transport and expression of VGLUT1 and VGLUT2 genes. Frontiers in Neuroanatomy 2010, 4:135.
66. Kaas J.H., Huerta M.F., Weber J.T., Harting J.K. Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 1978, 182:517-554.
67. Kaas J.H., Lyon D.C. Pulvinar contributions to the dorsal and ventral streams of visual processing in primates. Brain Research Reviews 2007, 55:285-296.
68. Kaas J.H. The evolution of visual cortex in primates. The primate visual system 2005, CRC Press. Kremers (Ed.).
69. Kaas J.H., Huerta M.F. The subcortical visual system of primates. Comparative Primate Biology 1988, A.R. Liss, Inc. Erwin, Steklis (Eds.).
70. Kaneko T., Fujiyama F. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neuroscience Research 2001, 42:243-250.
71. Krubitzer L.A., Kaas J.H. Cortical integration of parallel pathways in the visual system of primates. Brain Research 1989, 478:161-165.
72. Kubota Y., Kawaguchi Y. Three classes of GABAergic interneurons in neocortex and striatum. Japanese Journal of Physiology 1994, 44:S145-S148.
73. Lein E.S., Hawrylycz M.J., Ao N., et al. Genome-wide atlas of gene expression I the adult mouse brain. Nature 2007, 445:168-176.
74. Levitt J.B., Lund J.S., Yoshioka T. Anatomical substrates for early stages in cortical processing of visual information in the macaque monkey. Behavioural Brain Research 1996, 76:5-19.
75. Levitt J.B., Yoshioka T., Lund J.S. Connections between the pulvinar complex and cytochrome oxidase defined compartments in visual area V2 of macaque monkey. Experimental Brain Research 1995, 104:419-430.
76. Lin C.S., Kaas J.H. The inferior pulvinar complex in owl monkeys: architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex. Journal of Comparative Neurology 1979, 187:655-678.
77. Livingstone M.S., Hubel D.H. Specificity of cortico-cortical connections in monkey visual system. Nature 1983, 304:531-534.
78. Lock T.M., Baizer J.S., Bender D.B. Distribution of corticotectal cells in macaque. Experimental Brain Research 2003, 151:455-470.
79. Lund J.S., Lund R.D., Hendrickson A.E., et al. The origin of efferent pathways from the primary visual cortex, Area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 1975, 164:287-304.
80. Lund J.S. Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 1988, 11:253-288.
81. Lund R.D. Synaptic patterns in the superficial layers of the superior colliculus of the monkey, Macaca mulatta. Experimental Brain Research 1972, 15:194-211.
82. Lund J.S., Boothe R.G. Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 1975, 159:305-334.
83. Lyon D.C., Nassi J.J., Callaway E.M. A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. Neuron 2010, 65:270-279.
84. Marion R., Li K., Purushothaman G., et al. Morphological and neurochemical comparisons between pulvinar and V1 projections. Journal of Comparative Neurology 2012, 521:813-832.
85. Marrocco R.T., McClurkin J.W., Young R.A. Spatial properties of superior colliculus cells projecting to the inferior pulvinar and parabigeminal nucleus of the monkey. Brain Research 1981, 222:150-154.
86. Masterson S.P., Li J., Bickford M.E. Synaptic organization of the tectorecipient zone of the rat lateral posterior nucleus. Journal of Comparative Neurology 2009, 515:647-663.
87. Maunsell J.H.R., Van Essen D.C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 1983, 3:2563-2586.
88. May P.J. The mammalian superior colliculus: laminar structure and connections. Progress in Brain Research 2006, 151:31-378.
89. Ogren M.P., Hendrickson A.E. The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey. Brain Research 1977, 137:343-350.
90. Ogren M.P., Hendrickson A.E. The morphology and distribution of striate cortex terminals in the inferior and lateral subdivisions of the Macaca monkey pulvinar. Journal of Comparative neurology 1979, 188:179-199.
91. Olszewski J. The thalamus of Macaca Mulatta 1952, S. Karger, Basel, Switzerland.
92. Partlow G.D., Colonnier M., Szabo J. Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study. Journal of Comparative Neurology 1977, 72:285-318.
93. Pollack J.G., Hickey T.L. The distribution of retino-collicular axon terminals in the rhesus monkey. Journal of Comparative Neurology 1979, 185:587-602.
94. Poppel E., Held R., Frost D. Residual visual function after brain wounds involving the central visual pathway in man. Nature 1985, 243:295-296.
95. Reimer R.J., Fremeau R.T., Bellocchio E.E., Edwards R.H. The essence of excitation. Current Opinion in Cell Biology 2001, 13:417-421.
96. Rockland K.S., Pandya D.N. Laminar origins and terminations of cortical connections of the occipical lobe in the rhesus monkey. Brain Research 1979, 179:3-20.
97. Rockland K.S. The organization of feedback connections from area V2 (18) to V1 (17). Cerebral cortex 1994, Plenum Press, New York, NY. A. Peters, E.G. Jones (Eds.).
98. Salin P.A., Bullier J. Corticocortical connections in the visual system: structure and function. Physical Review 1995, 75:107-142.
99. Santos M.S., Li H., Voglmaier S.M. Synaptic vesicle protein trafficking at the glutamate synapse. Neuroscience 2009, 158:189-203.
100. Schäfer M.K., Varoqui H., Defamie N., et al. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. Journal of Biological Chemistry 2002, 277:50734-50748.
101. Seal R.P., Edwards R.H. The diverse roles of vesicular glutamate transporter 3. Handbook of Experimental Pharmacology 2006, 175:137-150.
102. Sherman S.M. Thalamic relays and cortical functioning. Progress in Brain Research 2005, 149:107-126.
103. Sherman S.M. Current Opinions in Neurobiology. 2012, 22:575-579.
104. Sherman S.M., Guillery R.W. Functional organization of thalamocortical relays. Journal of Neurophysiology 1996, 76:1367-1395.
105. Sherman S.M., Guillery R.W. On the actions that one nerve cell can have on another: Distinguishing "drivers" from "modulators". Proceedings of the National Academy of Sciences 1998, 95:7121-7126.
106. Sherman S.M., Guillery R.W. 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 2002, 357:1695-1708.
107. Sherman S.M., Guillery R.W. Exploring the thalamus and its role in cortical function 2006, MIT Press, Cambridge, MA.
108. Sherman S.M., Guillery R.W. Distinct functions for direct and transthalamic corticocortical connections. Journal of Neurophysiology 2011, 106:1068-1077.
109. Sherman S.M. The thalamus is more than just a relay. Current Opinion in Neurobiology 2007, 17:417-422.
110. Shipp S. Corticopulvinar connections of areas V5, V4, and V3 in the macaque monkeys: a dual model of retinal and cortical topographies. Journal of Comparative Neurology 2001, 439:469-490.
111. Sincich L.C., Horton J.C. Divided by cytochrome oxidase: a map of the projections from V1 to V2 in macaques. Science 2002, 295:1734-1737.
112. Sincich L.C., Jocson C.M., Horton J.C. V1 interpatch projections to V2 thick stripes and pale stripes. Journal of Neuroscience 2010, 30:6963-6974.
113. Sincich L.C., Park K.F., Wohlgemuth M.J., Horton J.C. Bypassing V1: a direct geniculate input to area MT. Nature Neuroscience 2004, 7:1123-1128.
114. Stepniewska I., Kaas J.H. Architectonic subdivisions of the inferior pulvinar in New World and Old World monkeys. Visual Neuroscience 1997, 14:1043-1060.
115. Stepniewska I., Qi H.X., Kaas J.H. Do superior colliculus projection zones in the inferior pulvinar project to MT in primates?. European Journal of Neuroscience 1999, 11:469-480.
116. Stepniewska I., Qi H.X., Kaas J.H. Projections of the superior colliculus to subdivisions of the inferior pulvinar in New World and Old World monkeys. Visual Neuroscience 2000, 17:529-549.
117. Stepniewska I. The pulvinar complex. The primate visual system 2004, CRC Press, Boca Raton, FL. J.H. Kaas, C.E. Collins (Eds.).
118. Stoerig P., Cowey A. Blindsight. Current Biology 2007, 17:R822-R824.
119. Storace D.A., Higgins N.C., Chikar J.A., et al. Gene expression identifies distinct ascending glutamatergic pathways to frequency-organized auditory cortex in the rat brain. Journal of Neuroscience 2012, 32:15759-15768.
120. Symonds L.L., Kaas J.H. Connections of striate cortex in the prosimian, Galago senegalensis. Journal of Comparative Neurology 1978, 181:477-512.
121. Tamietto M., Cauda F., Corazzini L.L., et al. Collicular vision guides nonconscious behavior. Journal of Cognitive Neuroscience 2010, 22:888-902.
122. Tigges M., Tigges J. The retinofugal fibers and their terminal nuclei in Galago crassicaudatus (primates). Journal of Comparative Neurology 1970, 138:87-101.
123. Tochitani S., Liang F., Watakabe A., et al. The occ1 gene is preferentially expressed in the primary visual cortex in an activity-dependent manner: a pattern of gene expression related to the cytoarchitectonic area in the adult macaque neocortex. European Journal of Neuroscience 2001, 13:297-307.
124. Trojanowski J.O., Jacobson S. Peroxidase labeled subcortical afferents to pulvinar in rhesus monkey. Brain Research 1975, 97:144-150.
125. Valverde F. The organizing principles of the primary visual cortex in the monkey. Cerebral cortex. Vol. 3. Visual cortex 1985, 207-252. Plenum Press, New York. A. Peters, E.D. Jones (Eds.).
126. Van Essen D.C. Corticocortical and thalamocortical information flow in the primate visual system. Progress in Brain Research 2005, 149:173-185.
127. Van Essen D.C. Functional organization of primate visual cortex. Cerebral cortex. Vol. 3. Visual cortex 1985, 259-320. Plenum Press, New York. A. Peters, E.D. Jones (Eds.).
128. Van Horn S.C., Sherman S.M. Differences in projection patterns between large and small corticothalamic terminals. Journal of Comparative neurology 2004, 440:321-341.
129. Varoqui H., Schafer M.K., Zhu H., et al. Identification of the differentiation-associated Na+/Pi trasporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. Journal of Neuroscience 2002, 22:142-155.
130. Viaene A.N., Petrof I., Sherman S.M. Synaptic properties of thalamic input to the subgranular layers of primary somatosensory and auditory cortices in the mouse. Journal of Neuroscience 2011, 31:12738-12747.
131. Viaene A.N., Petrof I., Sherman S.M. Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices. Journal of Neurophysiology 2011, 105:279-292.
132. Wilson M.E., Toyne M.J. Retinotectal and corticotectal projections. I. Macaca Mulatta. Brain Research 1970, 24:395-406.
133. Wong-Riley M. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 1979, 171:11-28.
134. Yamamori T. Selective gene expression in regions of primate neocortex: implications for cortical specialization. Progress in Neurobiology 2011, 96:164.
135. Yukie M., Iwai E. Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. Journal of Comparative Neurology 1981, 201:81-97.