Systematic, cross-cortex variation in neuron numbers in rodents and primates

Cerebral Cortex

Volumn 25, Issue 1, 2015, Pages 147-160

  Charvet, Christine J ^a   Cahalane, Diarmuid J ^a   Finlay, Barbara L ^a  

^a Behavioral and Evolutionary Neuroscience Group Department of Psychology Cornell University ^*  (United States)

Author keywords

Cortex; Development; Gradient; Numbers

Indexed keywords

AGOUTI; ARTICLE; BRAIN CORTEX; BRAIN REGION; BRAIN WEIGHT; CEBUS APELLA; FOREBRAIN; GLIA; HIPPOCAMPUS; NEOCORTEX; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RHESUS MONKEY; RODENT; STEREOLOGY; STEREOMETRY; STRIATE CORTEX; SYRIAN HAMSTER; ANIMAL; AOTUS; CEBUS; CELL COUNT; COMPARATIVE STUDY; CUNICULIDAE; CYTOLOGY; DASYPROCTIDAE; MESOCRICETUS; SAGUINUS; SPECIES DIFFERENCE;

ANIMALS; AOTUS TRIVIRGATUS; CEBUS; CELL COUNT; CUNICULIDAE; DASYPROCTIDAE; MESOCRICETUS; NEOCORTEX; NEUROGLIA; NEURONS; SAGUINUS; SPECIES SPECIFICITY;

EID: 84922389585     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht214     Document Type: Article

References (67)

1. Abercrombie M. 1946. Estimation of nuclear populations from microtome sections. Anat Rec. 94:239-247.
2. Bayer SA, Altman J. 1990. Development of layer I and the subplate in the rat neocortex. Exp Neurol. 107:48-62.
3. Bayer SA, Altman J. 1991. Neocortical development. New York: Raven.
4. Beaulieu C, Colonnier M. 1989. Number and ize of neurons and synapses in the motor cortex of cats raised in different environmental complexities. J Comp Neurol. 289:178-187.
5. Benes FM, Lange N. 2001. Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci. 24:11-17.
6. Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A. 2007. The delayed rise of present-day mammals. Nature. 446:507-512.
7. Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry RW, Huchon D. 2009. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol Biol. 9:71. doi: 10. 1186/ 1471-2148-9-71.
8. Cahalane DJ, Charvet CJ, Finlay BL. 2012. Systematic, balancing gradients in neuron density and number across the primate isocortex. Front Neuroanat. 6:28. doi: 10. 3389/fnana. 2012. 00028.
9. Cahalane DJ, Clancy B, Kingsbury MA, Graf E, Sporns O, Finlay BL. 2011. Network structure implied by initial axon outgrowth in rodent cortex: empirical measurement and models. PLoS One. 6:16113. doi:10. 1371/journal. pone. 0016113.
10. Campi KL, Collins CE, Todd WD, Kaas J, Krubitzer L. 2011. Comparison of area 17 cellular composition in laboratory and wild-caught rats including diurnal and nocturnal species. Brain Behav Evol. 77:116-130. doi: 10. 1159/000324862.
11. Carlo CN, Stevens CF. 2013. Structural uniformity of neocortex, revisited. Proc Natl Acad Sci USA. 110:1488-1493. doi: 10. 1073/ pnas. 1221398110.
12. Caviness VS, Nowakowski RS, Bhide PG. 2009. Neocortical neurogenesis: morphogenetic gradients and beyond. Trends Neurosci. 32:443-450.
13. Chalfin BP, Cheung DT, Muniz JAPC, de Lima Silveira LC, Finlay BL. 2007. Scaling of neuron number and volume of the pulvinar complex in new world primates: comparisons with humans, other primates, and mammals. J Comp Neurol. 504:265-274.
14. Charvet CJ, Striedter GF. 2011. Developmental modes and developmental mechanisms can channel brain evolution. Front Neuroanat. 5:4. doi: 10. 3389/fnana. 2011. 00004.
15. Charvet CJ, Striedter GF. 2008. Developmental species differences in brain cell cycle rates between northern bobwhite quail (Colinus virginianus) and parakeets (Melopsittacus undulatus): implications for mosaic brain evolution. Brain Behav Evol. 72:295-306.
16. Charvet CJ, Striedter GF, Finlay BL. 2011. Evo-devo and brain scaling: candidate developmental mechanisms for variation and constancy in vertebrate brain evolution. Brain Behav Evol. 78:248-257. doi: 10. 1159/000329851.
17. Chenn A, Walsh CA. 2002. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 297:365-369.
18. Christensen JR, Larsen KB, Lisanby SH, Scalia J, Arango V, Dwork AJ, Pakkenberg B. 2007. Neocortical and hippocampal neuron and glial cell numbers in the rhesus monkey. Anat Rec. 290:330-340.
19. Clancy B, Darlington RB, Finlay BL. 2001. Translating developmental time across mammalian species. Neuroscience. 105:7-17.
20. Collins CE. 2011. Variability in neuron densities across the cortical sheet in primates. Brain Behav Evol. 78:37-50.
21. Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH. 2010. Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci USA. 107:15927-15932.
22. Collins CE, Leitch DB, Wong P, Kaas JH, Herculano-Houzel S. 2013. Faster scaling of visual neurons in cortical areas relative to subcortical structures in non-human primate brains. Brain Struct Funct. 218:805-816.
23. Dehay C, Giroud P, Berland M, Smart I, Kennedy H. 1993. Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature. 366:464-466.
24. Dyer MA, Martins R, da Silva Filho M, Muniz JA, Silveira LC, Cepko CL, Finlay BL. 2009. Developmental sources of conservation and variation in the evolution of the primate eye. Proc Natl Acad Sci USA. 106:8963-8968. Doi: 10. 1073/pnas. 0901484106
25. Finlay BL. 1992. Cell death and the creation of regional differences in neuronal numbers. J Neurobiol. 23:1159-1171.
26. Finlay BL, Darlington RB. 1995. Linked regularities in the development and evolution of mammalian brains. Science. 268:1578-1584.
27. Finlay BL, Hersman MN, Darlington RB. 1998. Patterns of vertebrate neurogenesis and the paths of vertebrate evolution. Brain Behav Evol. 52:232-242.
28. Finlay BL, Slattery M. 1983. Local differences in the amount of early cell death in neocortex predict adult local specializations. Science. 219:1349-1351.
29. Friede RL. 1963. The relationship of body size, nerve cell size, axon length, and glial density in the cerebellum. Proc Natl Acad Sci USA. 49:187-193.
30. Gabi M, Collins CE, Wong P, Torres LB, Kaas JH, Herculano-Houzel S. 2010. Cellular scaling rules for the brains of an extended number of primate species. Brain Behav Evol. 76:32-44. doi: 10. 1073/ pnas. 0901484106.
31. Giannaris EL, Rosene DL. 2012. A stereological study of the numbers of neurons and glia in the primary visual cortex across the lifespan of male and female rhesus monkeys. J Comp Neurol. 520: 3492-3508.
32. Hanken J, Wake DB. 1993. Miniaturization of body size: organismal consequences and evolutionary significance. Annu Rev Ecol Syst. 24:501-519.
33. Herculano-Houzel S, Collins CE, Wong P, Kaas JH. 2007. Cellular scaling rules for primate brains. Proc Natl Acad Sci USA. 104:3562-3567.
34. Herculano-Houzel S, Lent R. 2005. Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J Neurosci. 25:2518-2521.
35. Herculano-Houzel S, Ribeiro P, Campos L, Valotta da Silva A, Torres LB, Catania KC, Kaas JH. 2011. Updated neuronal scaling rules for the brains of Glires (rodents/lagomorphs). Brain Behav Evol. 78:302-314. doi: 10. 1073/pnas. 0901484106.
36. Hutsler J, Lee D, Porter K. 2005. Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species. Brain Res. 1052:71-81.
37. Kaiser M, Hilgetag CC. 2006. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol. 2:95. doi: 10. 1073/pnas. 0901484106.
38. Kaskan PM, Franco ECS, Yamada ES, de Lima Silveira LC, Darlington RB, Finlay BL. 2005. Peripheral variability and central constancy in mammalian visual system evolution. Proc Biol Sci. 272:91-100.
39. Kennedy H, Dehay C. 1993. Cortical specification of mice and men. Cereb Cortex. 3:171-186.
40. Klyachko VA, Stevens CF. 2003. Connectivity optimization and the positioning of cortical areas. Proc Natl Acad Sci USA. 100: 7937-7941.
41. Lent R, Hedin-Pereira C, Menezes JR, Jhaveri S. 1990. Neurogenesis and development of callosal and intracortical connections in the hamster. Neuroscience. 38:21-37.
42. Lewitus E, Hof PR, Sherwood CC. 2012. Phylogenetic comparison of neuron and glia densities in the primary visual cortex and hippocampus of carnivores and primates. Evolution. 66:2551-2563.doi: 10.1073/pnas. 0901484106
43. Lidow MS, Song Z-M. 2001. Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J Comp Neurol. 435:263-275. doi: 10. 1073/pnas. 0901484106
44. McGowan LD, Alaama RA, Freise AC, Huang JC, Charvet CJ, Striedter GF. 2012. Expansion, folding, and abnormal lamination of the chick optic tectum after intraventricular injections of FGF2. Proc Natl Acad Sci USA. 109:10640-10646.
45. Miyama S, Takahashi T, Nowakowski RS, Caviness VS Jr. 1997. A gradient in the duration of the G1 phase in the murine neocortical proliferative epithelium. Cereb Cortex. 7:678-689.
46. Modha DS, Singh R. 2010. Network architecture of the long-distance pathways in the macaque brain. Proc Natl Acad Sci USA. 107:13485-13490.
47. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ. 2001. Molecular phylogenetics and the origins of placental mammals. Nature. 409:614-618.
48. Murre JMJ, Sturdy DPF. 1995. The connectivity of the brain: multi-level quantitative analysis. Biol Cybern. 73:529-545.
49. O'Kusky J, Colonnier M. 1982. A laminar analysis of the number of neurons, glia, and synapses in the adult cortex (area 17) of adult macaque monkeys. J Comp Neurol. 210:278-290.
50. Rakic P. 2008. Confusing cortical columns. Proc Natl Acad Sci USA. 105:12099-12100.
51. Rakic P. 2009. Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci. 10:724-735.
52. Rakic P. 1974. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science. 183:425-427.
53. Rakic P. 2002. Pre-And post-developmental neurogenesis in primates. Clin Neurosci Res. 2:29-39.
54. Reep RL, Finlay BL, Darlington RB. 2007. The limbic system in mammalian brain evolution. Brain Behav Evol. 70:57-70.
55. Rockel AJ, Hiorns RW, Powell TPS. 1980. The basic uniformity in structure of the neocortex. Brain. 103:221-244.
56. Sherwood CC, Raghanti MA, Stimpson CD, Bonar CJ, de Sousa AA, Preuss TM, Hof PR. 2007. Scaling of inhibitory interneurons in areas v1 and v2 of anthropoid primates as revealed by calcium-binding protein immunohistochemistry. Brain Behav Evol. 69:176-195.
57. Smart IH. 1983. Three dimensional growth of the mouse isocortex. J Anat. 137:683-694.
58. Stephan H, Frahm H, Baron G. 1981. New and revised data on volumes of brain structures on insectivores and primates. Folia Primatol (Basel). 35:1-29.
59. Striedter GF. 2005. Principles of brain evolution. Sunderland (MA): Sinauer.
60. Striedter GF, Charvet CJ. 2008. Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus). J Comp Neurol. 507:1663-1675.doi 10. 1002/ cne. 21640
61. Suner I, Rakic P. 1996. Numerical relationship between neurons in the lateral geniculate nucleus and primary visual cortex in macaque monkeys. Vis Neurosci. 13:585-590.
62. Suter B, Nowakowski RS, Bhide PG, Caviness VS. 2007. Navigating neocortical neurogenesis and neuronal specification: a positional information system encoded by neurogenetic gradients. J Neurosci. 27:0777-10784.
63. Watts DJ, Strogatz SH. 1998. Collective dynamics of 'small-world' networks. Nature. 393:440-442.
64. Williams RW, Rakic P. 1988. Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J Comp Neurol. 278:344-352.
65. Williams RW, von Bartheld CS, Rosen GD. 2003. Counting cells in sectioned material: a suite of techniques, tools, and tips. Curr Protoc Neurosci. 1. 11. 1-1. 11. 29. doi: 10. 1002/cne. 21640.
66. Workman AD, Charvet CJ, Clancy B, Darlington RB, Finlay BL. 2013. Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci. 33:7368-7383. doi: 10. 1523/JNEUROSCI. 5746-12.
67. Young NA, Collins CE, Kaas JH. 2013. Cell and neuron densities in the primary motor cortex of primates. Front Neural Circuits. 7:30. doi:10. 3389/fncir. 2013. 00030.