Scaling of inhibitory interneurons in areas V1 and V2 of anthropoid primates as revealed by calcium-binding protein immunohistochemistry

Brain, Behavior and Evolution

Volumn 69, Issue 3, 2007, Pages 176-195

  Sherwood, Chet C ^a   Raghanti, Mary Ann ^b   Stimpson, Cheryl D ^a   Bonar, Christopher J ^c   De Sousa, Alexandra A ^a   Preuss, Todd M ^d   Hof, Patrick R ^e,f  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b KENT STATE UNIVERSITY   (United States)

^c CLEVELAND METROPARKS ZOO   (United States)

^d EMORY UNIVERSITY   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f NEW YORK CONSORTIUM IN EVOLUTIONARY PRIMATOLOGY   (United States)

Author keywords

Calbindin; Calretinin; Evolution; Mammals; Parvalbumin; Primates; Visual cortex

Indexed keywords

CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; PARVALBUMIN;

AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CELL DENSITY; CELL VOLUME; CELLULAR DISTRIBUTION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MALE; MAMMAL; MOLECULAR EVOLUTION; MONKEY; NONHUMAN; NORMAL HUMAN; PHYLOGENY; PRIMATE; PRIORITY JOURNAL; SCALE UP; SOMATIC CELL; STAINING; VISUAL CORTEX;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL COUNT; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; PHYLOGENY; PRIMATES; SPECIES SPECIFICITY; VISUAL CORTEX;

CERCOPITHECIDAE; HOMO; MAMMALIA; PLATYRRHINI; PRIMATES; SIMIIFORMES;

EID: 33847742581     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000096986     Document Type: Article

References (97)

1. Allman JM, Kaas JH (1971) Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Res 35:89-106.
2. Allman JM, McGuinness E (1988) Visual cortex in primates. In: Comparative Primate Biology, Neurosciences (Steklis H, Erwin J, ed), pp 279-326. New York: Alan R. Liss.
3. Andressen C, Blümcke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181-208.
4. Ballesteros-Yanez I, Munoz A, Contreras J, Gonzalez J, Rodriguez-Veiga E, DeFelipe J (2005) Double bouquet cell in the human cerebral cortex and a comparison with other mammals. J Comp Neurol 486:344-360.
5. Boynton GM, Hegde J (2004) Visual cortex: the continuing puzzle of area V2. Curr Biol 14:R523-524.
6. Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde. Leipzig: Barth.
7. Carder RK, Leclerc SS, Hendry SH (1996) Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. Cereb Cortex 6:271-287.
8. Changizi MA (2001) Principles underlying mammalian neocortical scaling. Biol Cybern 84:207-215.
9. DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28k, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1-19.
10. DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299-316.
11. DeFelipe J, Gonzalez-Albo MC, del Rio MR, Elston GN (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412:515-526.
12. DeFelipe J, Hendry SH, Jones EG (1989) Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res 503:49-54.
13. del Rio MR, DeFelipe J (1996) Colocalization of calbindin D-28k, calretinin, and GABA immunoreactivities in neurons of the human temporal cortex. J Comp Neurol 369:472-482.
14. del Rio MR, DeFelipe J (1997a) Colocalization of parvalbumin and calbindin D-28k in neurons including chandelier cells of the human temporal neocortex. J Chem Neuroanat 12:165-173.
15. del Rio MR, DeFelipe J (1997b) Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J Chem Neuroanat 13:243-251.
16. Dorph-Petersen KA, Nyengaard JR, Gundersen HJ (2001) Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204:232-246.
17. Douglas R, Martin KAC (1992) Exploring cortical microcircuits: A combined anatomical, physiological, and computational approach. In: Single Neuron Computation (McKenna T, Davies J, Zornetzer SF, eds), pp 381-412. San Diego, CA: Academic Press.
18. Elston GN (2003) Pyramidal cell heterogeneity in the visual cortex of the nocturnal New World owl monkey (Aotus trivirgatus). Neuroscience 117:213-219.
19. Elston GN, Rosa MG (1997) The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432-452.
20. Elston GN, Benavides-Piccione R, Elston A, Zietsch B, Defelipe J, Manger P, Casagrande V, Kaas JH (2006) Specializations of the granular prefrontal cortex of primates: Implications for cognitive processing. Anat Rec 288A:26-35.
21. Elston GN, Elston A, Kaas JH, Casagrande V (2005) Regional specialization in pyramidal cell structure in the visual cortex of the galago: an intracellular injection study of striate and extrastriate areas with comparative notes on New World and Old World monkeys. Brain Behav Evol 66:10-21.
22. Elston GN, Rosa MG, Calford MB (1996) Comparison of dendritic fields of layer III pyramidal neurons in striate and extrastriate visual areas of the marmoset: a Lucifer yellow intracellular injection. Cereb Cortex 6:807-813.
23. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47.
24. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1-15.
25. Gabbott PL, Bacon SJ (1996) Local circuit neurons in the medial prefrontal cortex (areas 24a, b, c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J Comp Neurol 364:609-636.
26. Gabbott PL, Dickie BG, Vaid RR, Headlam AJ, Bacon SJ (1997a) Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J Comp Neurol 377:465-499.
27. Gabbott PL, Jays PR, Bacon SJ (1997b) Calretinin neurons in human medial prefrontal cortex (areas 24a, b, c, 32′, and 25). J Comp Neurol 381:389-410.
28. Garland T, Ives AR (2000) Using the past to predict the present: Confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346-364.
29. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18-32.
30. Garland T, Midford PE, Ives AR (1999) An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am Zool 39:374-388.
31. Glezer, II, Hof PR, Leranth C, Morgane PJ (1993) Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. Cereb Cortex 3:249-272.
32. Gonchar Y, Burkhalter A (1997) Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7:347-358.
33. Goodman M, Grossman LI, Wildman DE (2005) Moving primate genomics beyond the chimpanzee genome. Trends Genet 21:511-517.
34. Gundersen HJ (1988) The nucleator. J Microsc 151:3-21.
35. Harvey PH, Krebs JR (1990) Comparing brains. Science 249:140-146.
36. Hässler R (1967) Comparative anatomy in the central visual systems in day- and night-active primates. In: Evolution of the Forebrain (Hässler R, Stephan H, eds), pp 419-434. Stuttgart: Thieme.
37. Hendry SH, Carder RK (1993) Neurochemical compartmentation of monkey and human visual cortex: similarities and variations in calbindin immunoreactivity across species. Vis Neurosci 10:1109-1120.
38. Hendry SHC, Jones EG, Emson PC, Lowson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467-472.
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, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287A:1153-1163.
41. Hof PR, Glezer, II, Condé F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77-116.
42. Howard CV, Reed MG (1998) Unbiased Stereology - Three-Dimensional Measurement in Microscopy. New York: Springer-Verlag.
43. Hutsler JJ, Lee DG, Porter KK (2005) Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species. Brain Res 1052:71-81.
44. Kaas JH (2005) The future of mapping sensory cortex in primates: three of many remaining issues. Phil Trans R Soc Lond B Biol Sci 360:653-664.
45. Kondo H, Hashikawa T, Tanaka K, Jones EG (1994) Neurochemical gradient along the monkey occipito-temporal cortical pathway. Neuroreport 5:613-616.
46. Kondo H, Tanaka K, Hashikawa T, Jones EG (1999) Neurochemical gradients along monkey sensory cortical pathways: calbindin-immunoreactive pyramidal neurons in layers II and III. Eur J Neurosci 11:4197-4203.
47. Kubota Y, Jones EG (1993) Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex. Brain Res 600:339-344.
48. Lee TS (2003) Computations in the early visual cortex. J Physiol Paris 97:121-139.
49. Letinic K, Zoncu R, Rakic P (2002) Origin of GABAergic neurons in the human neocortex. Nature 417:645-649.
50. Leuba G, Saini K (1997) Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures. J Chem Neuroanat 13:41-52.
51. Li CX, Callaway JC, Waters RS (2002) Removal of GABAergic inhibition alters subthreshold input in neurons in forepaw barrel subfield (FBS) in rat first somatosensory cortex (SI) after digit stimulation. Exp Brain Res 145:411-428.
52. Lund JS, Lewis DA (1993) Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328:282-312.
53. Lund JS, Yoshioka T, Levitt JB (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb Cortex 3:148-162.
54. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
55. Morrison JH, Hof PR, Huntley GW (1998) Neurochemical organization of the primate visual cortex. In: Handbook of Chemical Neuroanatomy (Bloom FE, Björklund A, Hökfelt T, eds), pp 299-430. Amsterdam: Elsevier.
56. Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701-722.
57. Mouton PR (2002) Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists. Baltimore, MD: The Johns Hopkins University Press.
58. Nunn CL, Barton RA (2001) Comparative methods for studying primate adaptation and allometry. Evol Anthropol 10:81-98.
59. Pagel MD (1992) A method for the analysis of comparative data. J Theor Biol 156:431-442.
60. Patz S, Grabert J, Gorba T, Wirth MJ, Wahle P (2004) Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an early period of postnatal development. Cereb Cortex 14:342-351.
61. Peterson DA, Dickinson-Anson HA, Leppert JT, Lee KF, Gage FH (1999) Central neuronal loss and behavioral impairment in mice lacking neurotrophin receptor p75. J Comp Neurol 404:1-20.
62. Preuss TM (2000) Taking the measure of diversity: comparative alternatives to the model-animal paradigm in cortical neuroscience. Brain Behav Evol 55:287-299.
63. 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.
64. Preuss TM, Kaas JH (1996) Cytochrome oxidase 'blobs' and other characteristics of primary visual cortex in a lemuroid primate, Cheirogaleus medius. Brain Behav Evol 47:103-112.
65. Preuss TM, Qi H, Kaas JH (1999) Distinctive compartmental organization of human primary visual cortex. Proc Natl Acad Sci USA 96:11601-11606.
66. Price T (1997) Correlated evolution and independent contrasts. Phil Trans R Soc Lond B Biol Sci 352:519-529.
67. Prothero J (1997) Scaling of cortical neuron density and white matter volume in mammals. J Hirnforsch 38:513-524.
68. Purvis A, Webster AJ (1999) Phylogenetically independent comparisons and primate phylogeny. In: Comparative Primate Socioecology (Lee PC, ed), pp 44-68. Cambridge, UK: Cambridge University Press.
69. Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191-223.
70. Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in structure of the neocortex. Brain 103:221-244.
71. Rosa MG, Krubitzer LA (1999) The evolution of visual cortex: where is V2? Trends Neurosci 22:242-248.
72. Rosa MG, Fritsches KA, Elston GN (1997) The second visual area in the marmoset monkey: visuotopic organisation, magnification factors, architectonical boundaries, and modularity. J Comp Neurol 387:547-567.
73. Rosa MG, 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.
74. Sato H, Katsuyama N, Tamura H, Hata Y, Tsumoto T (1995) Mechanisms underlying direction selectivity of neurons in the primary visual cortex of the macaque. J Neurophysiol 74:1382-1394.
75. Schmitz C, Hof PR (2000) Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 20:93-114.
76. Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (1998) Limbic frontal cortex in hominoids: a comparative study of area 13. Am J Phys Anthropol 106:129-155.
77. Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (2001) Prefrontal cortex in humans and apes: a comparative study of area 10. Am J Phys Anthropol 114:224-241.
78. Sherwood CC, Hof PR (in press) The evolution of neuron types and cortical histology in apes and humans. In: The Evolution of Primate Nervous Systems. Evolution of Nervous Systems, Vol. 4 (Preuss TM, Kaas JH, eds), Amsterdam: Elsevier.
79. Sherwood CC, Holloway RL, Erwin JM, Hof PR (2004) Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II. Stereologic analysis of chemoarchitecture. Brain Behav Evol 63:82-106.
80. Sherwood CC, Lee PWH, Rivara C-B, Holloway RL, Gilissen EPE, Simmons RMT, Hakeem A, Allman JM, Erwin JM, Hof PR (2003) Evolution of specialized pyramidal neurons in primate visual and motor cortex. Brain Behav Evol 61:28-44.
81. Sincich LC, Horton JC (2005) The circuitry of V1 and V2: integration of color, form, and motion. Annu Rev Neurosci 28:303-326.
82. Sokal RR, Rohlf FJ (1995) Biometry: The Principles and Practice of Statistics in Biological Research. San Francisco, CA: W.H. Freeman.
83. Somogyi P, Tamas G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26:113-135.
84. Stephan H, Frahm HD, Baron G (1981) New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol 35:1-29.
85. Tosi AJ, Melnick DJ, Disotell TR (2004) Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). J Hum Evol 46:223-237.
86. Tower DB (1954) Structural and functional organization of mammalian cerebral cortex: the correlation of neurone density with brain size. J Comp Neurol 101:19-52.
87. Tower DB, Young OM (1973) The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis and the question of constant density of glial cells in cerebral cortices of mammalian species from mouse to whale. J Neurochem 20:269-278.
88. Tsumoto T, Eckart W, Creutzfeldt OD (1979) Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp Brain Res 34:351-363.
89. Van Brederode JF, Mulligan KA, Hendrickson AE (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298:1-22.
90. Van Essen DC, Anderson CH, Felleman DJ (1992) Information processing in the primate visual system: an integrated systems perspective. Science 255:419-423.
91. Wang J, Caspary D, Salvi RJ (2000a) GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex. Neuroreport 11:1137-1140.
92. Wang Y, Fujita I, Murayama Y (2000b) Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex. Nat Neurosci 3:807-813.
93. Warton DI, Weber NC (2002) Common slope tests for bivariate structural relationships. Biometrical J 44:161-174.
94. West MJ, Slomianka L, Gundersen HJG (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
95. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.
96. Zilles K, Rehkämper G (1988) The brain, with special reference to the telencephalon. In: Orang-utan Biology (Schwartz JH, ed), pp 157-176. New York: Oxford University Press.
97. Zilles K, Palomero-Gallagher N, Schleicher A (2004) Transmitter receptors and functional anatomy of the cerebral cortex. J Anat 205:417-432.