Vesicular glutamate transporters (VGLUTs) reuptake glutamate into synaptic vesicles at excitatory synapses. VGLUT2 is localized in the cortical terminals of neuronal somas located in the main sensory nuclei of the thalamus. Thus, immunolabeling of cortex with antibodies to VGLUT2 can reveal geniculostriate terminal distributions in species in which connectivity cannot be studied with tract-tracing techniques, permitting broader comparative studies of cortical specializations. Here, we used VGLUT2 immunohistochemistry to compare the organization of geniculostriate afferents in primary visual cortex in hominid primates (humans, chimpanzees, and an orangutan), Old World monkeys (rhesus macaques and vervets), and New World monkeys (squirrel monkeys). The New and Old World monkeys had a broad, dense band of terminal-like labeling in cortical layer 4C, a narrow band of labeling in layer 4A, and additional labeling in layers 2/3 and 6, consistent with results from conventional tract-tracing studies in these species. By contrast, although the hominid primates had a prominent layer 4C band, labeling of layer 4A was sparse or absent. Labeling was also present in layers 2/3 and 6, although labeling of layer 6 was weaker in hominids and possibly more individually variable than in Old and New World monkeys. These findings are consistent with previous observations from cytochrome oxidase histochemistry and a very small number of connectivity studies, suggesting that the projections from the parvocellular layers of the lateral geniculate nucleus to layer 4A were strongly reduced or eliminated in humans and apes following their evolutionary divergence from the other anthropoid primates.

Keywords:
Architectonics, Area 17, Blobs, Brain evolution, Hominid specialization, Primary visual cortex, Vesicular glutamate transporter, VGLUT2, Visual cortex
1.
Balaram P, Takahata T, Kaas JH (2011): VGLUT2 mRNA and protein expression in the visual thalamus and midbrain of prosimian galagos (Otolemur garnetti). Eye Brain 2011:5–15.
2.
Barroso-Chinea P, Castle M, Aymerich MS, Perez-Manso M, Erro E, Tunon T, Lanciego JL (2007): Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. J Comp Neurol 501:703–715.
3.
Billings-Gagliardi S, Chan-Palay V, Palay SL (1974): A review of lamination in area 17 of the visual cortex Macaca mulatta. J Neurocytol 3:619–629.
4.
Blasdel GG, Lund JS (1983): Terminations of afferent axons in macaque striate cortex. J Neurosci 3:1389–1413.
5.
Blümcke I, Hof PR, Morrison JH, Celio MR (1990): Distribution of parvalbumin immunoreactivity in the visual cortex of Old World monkeys and humans. J Comp Neurol 301:417–432.
6.
Brodmann K (1909): Vergleichende Lokalisationslehre der Grosshirnrhinde. Leipzig, Barth [Garey LJ (1994) Localisation in the Cerebral Cortex. London, Smith-Gordon].
7.
Callaway EM (1998): Local circuits in primary visual cortex of the macaque monkey. Annu Rev Neurosci 21:47–74.
8.
Carroll EW, Wong-Riley MTT (1984): Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. J Comp Neurol 222:1–17.
9.
Casagrande VA (1994): A third parallel visual pathway to primate area V1. Trends Neurosci 17:305–310.
10.
Casagrande VA, Kaas JH (1994): The afferent, intrinsic, and efferent connections of primary visual cortex in primates; in Peters A, Rockland K (eds): Cerebral Cortex. Primary Visual Cortex in Primates. New York, Plenum, vol 10, pp 201–259.
11.
Casagrande VA, Khaytin I, Boyd J ( 2007): The evolution of parallel visual pathways in the brains of primates; in Preuss TM, Kaas J (eds): Evolution of the Nervous System. New York, Academic Press, vol 4, pp 87–108.
12.
Condo GJ, Casagrande VA (1990): Organization of cytochrome oxidase staining in the visual cortex of nocturnal primates (Galago crassicaudatus and Galago senegalensis): I. Adult patterns. J Comp Neurol 293:632–645.
13.
Diamond IT, Conley M, Itoh K, Fitzpatrick D (1985): Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. J Comp Neurol 242:584–610.
14.
Ding Y, Casagrande VA (1997): The distribution and morphology of LGN K pathway axons within the layers and CO blobs of owl monkey V1. Vis Neurosci 14:691–704.
15.
Ferster D, Levay S, (1978): The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat. J Comp Neurol 182:923–944.
16.
Florence SL, Casagrande VA, (1987): Organization of individual afferent axons in layer IV of striate cortex in a primate. J Neurosci 7:3850–3868.
17.
Freund TF, Martin KA, Soltesz I, Somogyi P, Whitteridge DI (1989): Arborization pattern and postysynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey. J Comp Neurol 289:315–336.
18.
Fitzpatrick D, Itoh K, Diamond IT (1983): The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). J Neurosci 3:2563–2586.
19.
Fryer HJ, Kelly GM, Molinaro L, Hockfield S (1992): The high molecular weight Cat-301 chondroitin sulfate proteoglycan from brain is related to the large aggregating proteoglycan from cartilage, aggrecan. J Biol Chem 267:9874–9883.
20.
Gil Z, Connors BW, Amitai Y (1999): Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385–397.
21.
Graziano A, Liu XB, Murray KD, Jones EG (2008): Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse. J Comp Neurol 507:1258–1276.
22.
Hackett TA, de la Mothe LA (2009): Regional and laminar distribution of the vesicular glutamate transporter, VGluT2, in the macaque monkey auditory cortex. J Chem Neuroanat 38:106–116.
23.
Hackett TA, Takahata T, Balaram P (2011): VGLUT1 and VGLUT2 mRNA expression in the primate auditory pathway. Hear Res 274:129–141.
24.
Hässler R, Wagner A (1965): Experimentelle und morphologische Befunde über die vierfache kortikale Projektion des visuellen Systems. 8th Int Congr Neurol 3:77–96.
25.
Hendrickson AE (1985): Dots, stripes, and columns in monkey visual cortex. Trends Neurosci 8:406–410.
26.
Hevner RF, Wong-Riley MTT (1990): Regulation of cytochrome oxidase protein levels by activity in the macaque monkey visual system. J Neurosci 10:1331–1340.
27.
Horton JC (1984): Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philos Trans R Soc Lond B Biol Sci 304:199–253.
28.
Horton JC, Hedley-Whyte ET (1984): Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philos Trans R Soc Lond B Biol Sci 304:255–272.
29.
Horton JC, Hubel DH (1981): Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292:762–764.
30.
Hrabovszky E, Csapo AK, Kallo I, Wilhelm T, Turi GF, Liposits Z (2006a): Localization and osmotic regulation of vesicular glutamate transporter-2 in magnocellular neurons of the rat hypothalamus. Neurochem Int 48:753–761.
31.
Hrabovszky E, Kallo I, Turi GF, May K, Wittmann G, Fekete C, Liposits Z (2006b): Expression of vesicular glutamate transporter-2 in gonadotrope and thyrotrope cells of the rat pituitary. Regulation by estrogen and thyroid hormone status. Endocrinology 147:3818–3825.
32.
Humphrey AL, Sur M, Uhlrich DJ, Sherman SM (1985): Termination patterns of individual X- and Y-cell axons in the visual cortex of the cat: projections to area 18, to the 17/18 border region, and to both areas 17 and 18. J Comp Neurol 233:190–212.
33.
Jones EG, Hendry SHC (1989): Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1:222–246.
34.
Jones EG, Hendry SHC, Liu XB, Hodgins S, Potkin SG, Tourtellotte WW (1992): A method for fixation of previously fresh-frozen human adult and fetal brains that preserves histological quality and immunoreactivity. J Neurosci Methods 44:133–144.
35.
Kaas JH, Lin CS, Casagrande VA (1976): The relay of ipsilateral and contralateral retinal input from the lateral geniculate nucleus to striate cortex in the owl monkey: a transneuronal transport study. Brain Res 106:371–378.
36.
Kaneko T, Fujiyama F (2002): Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 42:243–250.
37.
Kaneko T, Fujiyama F, Hioki H (2002): Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444:39–62.
38.
Kawasaki H, Crowley JC, Livesey FJ, Katz LC (2004): Molecular organization of the ferret visual thalamus. J Neurosci 24:9962–9970.
39.
Lachica EA, Casagrade VA (1992): Direct W-like geniculate projections to the cytochrome oxidase (CO) blobs in primate visual cortex: axon morphology. J Comp Neurol 319:141–158.
40.
Livingstone MS, Hubel DH (1982): Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc Natl Acad Sci USA 79:6098–6101.
41.
Lund JS (1973): Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). J Comp Neurol 147:455–496.
42.
Mason CA, Robson JA (1979): Morphology of retino-geniculate axons in the cat. Neuroscience 4:79–97.
43.
Miklossy J (1992): Thalamocortical connections and rostral visual areas in man; in Gulyas B, Ohoson D, Rowland PE (eds): The Functional Organization of the Human Visual Cortex. Oxford, Pergamon, pp 123–136.
44.
Nahmani M, Erisir A (2005): VGluT2 immunochemistry identifies thalamocortical terminals in layer 4 of adult and developing visual cortex. J Comp Neurol 484:458–473.
45.
Peeters R, Simone L, Nelissen K, Fabbri-Destro M, Vanduffel W, Rizzolatti G, Orban G (2009): The representation of tool use in humans and monkeys: common and uniquely human features. J Neurosci 29:11523–11539.
46.
Preuss TM (2004): Specializations of the human visual system: The monkey model meets human reality; in Kaas JH, Collins CE (eds): The Primate Visual System. Boca Raton, CRC, pp 231–259.
47.
Preuss TM (2007): Evolutionary specializations of primate brain systems; in Ravosa MJ, Dagasto M (eds): Primate Origins: Adaptations and Evolution. New York, Springer, pp 625–675.
48.
Preuss TM, Coleman GQ (2002): Human-specific organization of primary visual cortex: alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb Cortex 12:671–691
49.
Preuss TM, Huixin Q, Kaas JH (1999): Distinctive compartmental organization of human primary visual cortex. Proc Natl Acad Sci USA 96:11601–11606.
50.
Sadakata T, Kakegawa W, Mizoguchi A, Washida M, Katoh-Semba R, Shutoh F, Okamoto T, Nakashima H, Kimura K, Tanaka M, Sekine Y, Itohara S, Yuzake M, Nagao S, Furuichi T (2007): Impaired cerebellar development and function in mice lacking CAPS2, a protein involved in neurotrophin release. J Neurosci 27:2472–2482.
51.
Tigges J, Tigges M (1979): Ocular dominance columns in the striate cortex of chimpanzee (Pan troglodytes). Brain Res 166:386–390.
52.
Tootell RBH, Mendola JD, Hadjikhani NK, Ledden PJ, Lliu AK, Reppas JB, Sereon MI, Dale AM (1997): Functional analysis of V3A and related areas in human visual cortex. J Neurosci 17:7060–7078.
53.
Vanduffel W, Fize D, Peuskens H, Denys K, Sunaert S, Todd JT, Orban GA (2002): Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science 298:413–415.
54.
Watson RE Jr, Wiegand SJ, Clough RW, Hoffman GE (1986): Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155–159.
55.
Weber JT, Huerta MF, Kaas JH, Harting JK (1983): The projections of the lateral geniculate nucleus of the squirrel monkey: studies of the interlaminar zones and the S layers. J Comp Neurol 213:135–145.
56.
Wong P, Kaas JH (2009): An architectonic study of the neocortex of the short-tailed opossum (Monodelphis domestica). Brain Behav Evol 73:206–228.
57.
Wong-Riley MTT (1979): Changes in the visual system of monocularly sutured or enucleated cats demonstrable with the cytochrome oxidase technique. Anat Rec 190:586.
58.
Wong-Riley MTT (1989): Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94–101.
59.
Wong-Riley MTT (1994): Primate visual cortex: dynamic metabolic organization and plasticity revealed by cytochrome oxidase, in Peters A, Rockland K (eds): Cerebral Cortex, Primary Visual Cortex in Primates. New York, Plenum, vol 10, pp 141–200.
60.
Wong-Riley MTT, Antuono P, Ho KC, Egan R, Hevner R, Liebl W, Huang Z, Rachel R, Jones J (1997): Cytochrome oxidase in Alzheimer’s disease: biochemical, histochemical, and immunohistochemical analyses of the visual and other systems. Vision Res 37:3593–3608.
61.
Wong-Riley MTT, Hevner RF, Cutlan R, Earnest M, Egan R, Frost J, Nguyen T (1993): Cytochrome oxidase in the human visual cortex: distribution in the developing and adult brain. Vis Neurosci 10:41–58.
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