Immunohistochemical parcellation of the ferret (Mustela putorius) visual cortex reveals substantial homology with the cat (Felis catus)

Journal of Comparative Neurology

Volumn 518, Issue 21, 2010, Pages 4439-4462

  Homman Ludiye, Jihane ^a   Manger, Paul R ^b   Bourne, James A ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Carnivore; CSPG; Extrastriate area; Immunohistochemistry; Nonphosphorylated neurofilament

Indexed keywords

CHONDROITIN SULFATE; NEUROFILAMENT PROTEIN;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CAT; CELL SURFACE; CINGULATE GYRUS; CONTROLLED STUDY; FERRET; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VISUAL CORTEX;

ANIMALS; BRAIN MAPPING; CATS; FERRETS; HUMANS; IMMUNOHISTOCHEMISTRY; VISUAL CORTEX;

EID: 77957923174     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22465     Document Type: Article

References (93)

1. Albus K, Beckmann R. 1980. Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location. J Physiol 299:247-276.
2. Asher RA, Scheibe RJ, Keiser HD, Bignami A. 1995. On the existence of a cartilage-like proteoglycan and link proteins in the central nervous system. Glia 13:294-308.
3. Beck PD, Kaas JH. 1998. Cortical connections of the dorsomedial visual area in New World owl monkeys (Aotus trivirgatus) and squirrel monkeys (Saimiri sciureus). J Comp Neurol 400:18-34.
4. Bininda-Emonds OR, Gittleman JL, Purvis A. 1999. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev Camb Philos Soc 74:143-175.
5. Bininda-Emonds ORP, Gittleman JL, Kelly CK. 2001. Flippers versus feet: comparative trends in aquatic and non-aquatic carnivores. J Anim Ecol 70:386-400.
6. Bourne JA, Rosa MGP. 2003. Neurofilament protein expression in the geniculostriate pathway of a New World monkey (Callithrix jacchus). Exp Brain Res 150:19-24.
7. Bourne JA, Rosa MGP. 2006. Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT). Cereb Cortex 16:405-414.
8. Bourne JA, Warner CE, Rosa MGP. 2005. Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry. Cereb Cortex 15:740-748.
9. Bourne JA, Warner CE, Upton DJ, Rosa MGP. 2007. Chemoarchitecture of the middle temporal visual area in the marmoset monkey (Callithrix jacchus): laminar distribution of calcium-binding proteins (calbindin, parvalbumin) and nonphosphorylated neurofilament. J Comp Neurol 500:832-849.
10. Brigandt I. 2003. Homology in comparative, molecular, and evolutionary developmental biology: the radiation of a concept. J Exp Zool B Mol Dev Evol 299:9-17.
11. Brosseau-Lachaine O, Faubert J, Casanova C. 2001. Functional sub-regions for optic flow processing in the postero-medial lateral suprasylvian cortex of the cat. Cereb Cortex 11:989-1001.
12. Bruckner G, Grosche J, Schmidt S, Hartig W, Margolis RU, Delpech B, Seidenbecher CI, Czaniera R, Schachner M. 2000. Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J Comp Neurol 428:616-629.
13. Burman KJ, Lui LL, Rosa MGP, Bourne JA. 2007. Development of non-phosphorylated neurofilament protein expression in neurones of the New World monkey dorsolateral frontal cortex. Eur J Neurosci 25:1767-1779.
14. Campbell MJ, Morrison JH. 1989. Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191-205.
15. Campbell MJ, Hof PR, Morrison JH. 1991. A subpopulation of primate corticocortical neurons is distinguished by somatodendritic distribution of neurofilament protein. Brain Res 539:133-136.
16. Cantone G, Xiao J, Levitt JB. 2006. Retinotopic organization of ferret suprasylvian cortex. Vis Neurosci 23:61-77.
17. Carmichael ST, Price JL. 1994. Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366-402.
18. Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L. 1998. Perineuronal nets: past and present. Trends Neurosci 21:510-515.
19. Changizi MA, Shimojo S. 2005. Parcellation and area-area connectivity as a function of neocortex size. Brain Behav Evol 66:88-98.
20. Chaudhuri A, Zangenehpour S, Matsubara JA, Cynader MS. 1996. Differential expression of neurofilament protein in the visual system of the vervet monkey. Brain Res 709: 17-26.
21. Cusick CG, Seltzer B, Cola M, Griggs E. 1995. Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: evidence for subdivisions of superior temporal polysensory cortex. J Comp Neurol 360:513-535.
22. Dean HL, Crowley JC, Platt ML. 2004. Visual and saccade-related activity in macaque posterior cingulate cortex. J Neurophysiol 92:3056-3068.
23. Del Rio MR, DeFelipe J. 1994. A study of SMI 32-stained pyramidal cells, parvalbumin-immunoreactive chandelier cells, and presumptive thalamocortical axons in the human temporal neocortex. J Comp Neurol 342:389-408.
24. Deyoe EA, Hockfield S, Garren H, Van Essen DC. 1990. Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey. Vis Neurosci 5:67-81.
25. Dreher B, Wang C, Turlejski KJ, Djavadian RL, Burke W. 1996. Areas PMLS and 21a of cat visual cortex: two functionally distinct areas. Cereb Cortex 6:585-599.
26. Ebbesson SO. 1980. The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity. Cell Tissue Res 213:179-212.
27. Elston GN, Tweedale R, Rosa MGP. 1999. Cellular heterogeneity in cerebral cortex: a study of the morphology of pyramidal neurones in visual areas of the marmoset monkey. J Comp Neurol 415:33-51.
28. Fox K, Daw NW. 1993. Do NMDA receptors have a critical function in visual cortical plasticity? Trends Neurosci 16:6.
29. 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(14).
30. Gattass R, Sousa AP, Gross CG. 1988. Visuotopic organization and extent of V3 and V4 of the macaque. J Neurosci 8: 1831-1845.
31. Goldstein ME, Sternberger LA, Sternberger NH. 1987. Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H). J Neuroimmunol 14:135-148.
32. Guedes R, Watanabe S, Creutzfeldt OD. 1983. Functional role of association fibres for a visual association area: the posterior suprasylvian sulcus of the cat. Exp Brain Res 49: 13-27.
33. Guimaraes A, Zaremba S, Hockfield S. 1990. Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J Neurosci 10:3014-3024.
34. Hendry SH, Hockfield S, Jones EG, McKay R. 1984. Monoclonal antibody that identifies subsets of neurones in the central visual system of monkey and cat. Nature 307: 267-269.
35. Hendry SH, Jones EG, Hockfield S, McKay RD. 1988. Neuronal populations stained with the monoclonal antibody Cat-301 in the mammalian cerebral cortex and thalamus. J Neurosci 8:518-542.
36. Hockfield S, McKay RD. 1983. A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc Natl Acad Sci USA 80:5758-5761.
37. Hockfield S, Tootell RB, Zaremba S. 1990. Molecular differences among neurons reveal an organization of human visual cortex. Proc Natl Acad Sci USA 87:3027-3031.
38. Hof PR, Morrison JH. 1990. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: II. Primary and secondary visual cortex. J Comp Neurol 301: 55-64.
39. Hof PR, Morrison JH. 1995. Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161-186.
40. Hof PR, Nimchinsky EA, Morrison JH. 1995. Neurochemical phenotype of corticocortical connections in the macaque monkey: quantitative analysis of a subset of neurofilament protein-immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices. J Comp Neurol 362: 109-133.
41. Hof PR, Ungerleider LG, Webster MJ, Gattass R, Adams MM, Sailstad CA, Morrison JH. 1996. Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. J Comp Neurol 376:112-127.
42. Horn AK, Eberhorn A, Hartig W, Ardeleanu P, Messoudi A, Buttner-Ennever JA. 2008. Perioculomotor cell groups in monkey and man defined by their histochemical and functional properties: reappraisal of the Edinger-Westphal nucleus. J Comp Neurol 507:1317-1335.
43. Hupfeld D, Distler C, Hoffmann KP. 2007. Deficits of visual motion perception and optokinetic nystagmus after posterior suprasylvian lesions in the ferret (Mustela putorius furo). Exp Brain Res 182:509-523.
44. Innocenti GM, Manger PR, Masiello I, Colin I, Tettoni L. 2002. Architecture and callosal connections of visual areas 17, 18, 19 and 21 in the ferret (Mustela putorius). Cereb Cortex 12:411-422.
45. Kaas JH, Hall WC, Killackey H, Diamond IT. 1972. Visual cortex of the tree shrew (Tupaia glis): architectonic subdivisions and representations of the visual field. Brain Res 42: 491-496.
46. Kalb RG, Hockfield S. 1988. Molecular evidence for early activity-dependent development of hamster motor neurons. J Neurosci 8:2350-2360.
47. Kalb RG, Hockfield S. 1990a. Induction of a neuronal proteoglycan by the NMDA receptor in the developing spinal cord. Science 250:294-296.
48. Kalb RG, Hockfield S. 1990b. Large diameter primary afferent input is required for expression of the Cat-301 proteoglycan on the surface of motor neurons. Neuroscience 34: 391-401.
49. Kalb RG, Hockfield S. 1994. Electrical activity in the neuro-muscular unit can influence the molecular development of motor neurons. Dev Biol 162:539-548.
50. Kaneko T, Caria MA, Asanuma H. 1994. Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex. J Comp Neurol 345:172-184.
51. Kobayashi Y, Amaral DG. 2000. Macaque monkey retrosplenial cortex: I. Three-dimensional and cytoarchitectonic organization. J Comp Neurol 426:339-365.
52. Koppe G, Bruckner G, Brauer K, Hartig W, Bigl V. 1997. Developmental patterns of proteoglycan-containing extracellular matrix in perineuronal nets and neuropil of the postnatal rat brain. Cell Tissue Res 288:33-41.
53. Lander C, Kind P, Maleski M, Hockfield S. 1997. A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J Neurosci 17:1928-1939.
54. Lander C, Zhang H, Hockfield S. 1998. Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J Neurosci 18:174-183.
55. Lewis JW, Van Essen DC. 2000. Mapping of architectonic sub-divisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol 428:79-111.
56. Li B, Li BW, Chen Y, Wang LH, Diao YC. 2000. Response properties of PMLS and PLLS neurons to simulated optic flow patterns. Eur J Neurosci 12:1534-1544.
57. Lomber SG. 2001. Behavioral cartography of visual functions in cat parietal cortex: areal and laminar dissociations. Prog Brain Res 134:265-284.
58. Lomber SG, Payne BR. 2004. Cerebral areas mediating visual redirection of gaze: cooling deactivation of 15 loci in the cat. J Comp Neurol 474:190-208.
59. Manger PR, Kiper D, Masiello I, Murillo L, Tettoni L, Hunyadi Z, Innocenti GM. 2002a. The representation of the visual field in three extrastriate areas of the ferret (Mustela putorius) and the relationship of retinotopy and field boundaries to callosal connectivity. Cereb Cortex 12:423-437.
60. Manger PR, Masiello I, Innocenti GM. 2002b. Areal organization of the posterior parietal cortex of the ferret (Mustela putorius). Cereb Cortex 12:1280-1297.
61. Manger PR, Nakamura H, Valentiniene S, Innocenti GM. 2004. Visual areas in the lateral temporal cortex of the ferret (Mustela putorius). Cereb Cortex 14:676-689.
62. Manger PR, Engler G, Moll CK, Engel AK. 2005. The anterior ectosylvian visual area of the ferret: a homologue for an enigmatic visual cortical area of the cat? Eur J Neurosci 22:706-714.
63. Manger PR, Engler G, Moll CK, Engel AK. 2008. Location, architecture, and retinotopy of the anteromedial lateral suprasylvian visual area (AMLS) of the ferret (Mustela putorius). Vis Neurosci 25:27-37.
64. Matthews RT, Kelly GM, Zerillo CA, Gray G, Tiemeyer M, Hockfield S. 2002. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 22: 7536-7547.
65. McKay RD, Hockfield SJ. 1982. Monoclonal antibodies distinguish antigenically discrete neuronal types in the vertebrate central nervous system. Proc Natl Acad Sci USA 79:6747-6751.
66. McLoughlin N, Cotton P, Schiessl I. 2005. A continuous smooth map of space in the primary visual cortex of the common marmoset. Perception 34:967-974.
67. Montero VM. 1980. Patterns of connections from the striate cortex to cortical visual areas in superior temporal sulcus of macaque and middle temporal gyrus of owl monkey. J Comp Neurol 189:45-59.
68. Nimchinsky EA, Hof PR, Young WG, Morrison JH. 1996. Neurochemical, morphologic, and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey. J Comp Neurol 374:136-160.
69. Palmer LA, Rosenquist AC, Tusa RJ. 1978. The retinotopic organization of lateral suprasylvian visual areas in the cat. J Comp Neurol 177:237-256.
70. Payne BR. 1993. Evidence for visual cortical area homologs in cat and macaque monkey. Cereb Cortex 3:1-25.
71. Philipp R, Distler C, Hoffmann KP. 2006. A motion-sensitive area in ferret extrastriate visual cortex: an analysis in pigmented and albino animals. Cereb Cortex 16:779-790.
72. Rauschecker JP, von Grunau MW, Poulin C. 1987. Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing. J Neurosci 7:943-958.
73. Rosa MGP. 1999. Topographic organisation of extrastriate areas in the flying fox: implications for the evolution of mammalian visual cortex. J Comp Neurol 411:503-523.
74. Rosa MGP, Palmer SM, Gamberini M, Tweedale R, Pinon MC, Bourne JA. 2005. Resolving the organization of the New World monkey third visual complex: the dorsal extrastriate cortex of the marmoset (Callithrix jacchus). J Comp Neurol 483:164-191.
75. Sia Y, Bourne JA. 2008. The rat temporal association cortical area 2 (Te2) comprises two subdivisions that are visually responsive and develop independently. Neuroscience 156: 118-128.
76. Singer W, Tretter F. 1976. Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats. J Neurophysiol 39:613-630.
77. Soares JG, Rosado De Castro PH, Fiorani M, Nascimento-Silva S, Gattass R. 2008. Distribution of neurofilament proteins in the lateral geniculate nucleus, primary visual cortex, and area MT of adult cebus monkeys. J Comp Neurol 508:605-614.
78. Spear PD, Baumann TP. 1975. Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat. J Neurophysiol 38:1403-1420.
79. Sternberger L. 1986. Immunocytochemistry. New York: John Wiley & Sons.
80. Sternberger LA, Sternberger NH. 1983. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 80: 6126-6130.
81. Strong NP, Malach R, Lee P, Van Sluyters RC. 1984. Horizontal optokinetic nystagmus in the cat: recovery from cortical lesions. Brain Res 315:179-192.
82. Sur M, Frost DO, Hockfield S. 1988. Expression of a surface-associated antigen on Y-cells in the cat lateral geniculate nucleus is regulated by visual experience. J Neurosci 8: 874-882.
83. Toyama K, Mizobe K, Akase E, Kaihara T. 1994. Neuronal responsiveness in areas 19 and 21a, and the posteromedial lateral suprasylvian cortex of the cat. Exp Brain Res 99:289-301.
84. Tusa RJ, Palmer LA. 1980. Retinotopic organization of areas 20 and 21 in the cat. J Comp Neurol 193:147-164.
85. Tusa RJ, Palmer LA, Rosenquist AC. 1978. The retinotopic organization of area 17 (striate cortex) in the cat. J Comp Neurol 177:213-235.
86. Tusa RJ, Demer JL, Herdman SJ. 1989. Cortical areas involved in OKN and VOR in cats: cortical lesions. J Neurosci 9: 1163-1178.
87. Updyke BV. 1986. Retinotopic organization within the cat's posterior suprasylvian sulcus and gyrus. J Comp Neurol 246:265-280.
88. Van der Gucht E, Vandesande F, Arckens L. 2001. Neurofilament protein: a selective marker for the architectonic parcellation of the visual cortex in adult cat brain. J Comp Neurol 441:345-368.
89. Van der Gucht E, Hof PR, Van Brussel L, Burnat K, Arckens L. 2007. Neurofilament protein and neuronal activity markers define regional architectonic parcellation in the mouse visual cortex. Cereb Cortex 17:2805-2819.
90. Vanduffel W, Payne BR, Lomber SG, Orban GA. 1997. Functional impact of cerebral connections. Proc Natl Acad Sci USA 94:7617-7620.
91. Villeneuve MY, Vanni MP, Casanova C. 2009. Modular organization in area 21a of the cat revealed by optical imaging: comparison with the primary visual cortex. Neuroscience 164:1320-1333.
92. Walls GL. 1942. The vertebrate eye and its adaptative radiation. New York: Hafner.
93. Zaremba S, Guimaraes A, Kalb RG, Hockfield S. 1989. Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 2:1207-1219.