Effect of temperature and glia in brain size enlargement and origin of allometric body-brain size scaling in vertebrates.

Yuguo Yu, Jan Karbowski, Robert N S Sachdev, Jianfeng Feng
Author Information
  1. Yuguo Yu: Centre for Computational Systems Biology, State Key Laboratory of Medical Neurobiology, Institutes of Brain Science, Department of Physiology and Biophysics, School of Life Sciences, Fudan University, Shanghai 200433, People's Republic of China. yuyuguo@fudan.edu.cn.

Abstract

BACKGROUND: Brain signaling requires energy. The cost of maintaining and supporting energetically demanding neurons is the key constraint on brain size. The dramatic increase in brain size among mammals and birds cannot be understood without solving this conundrum: larger brains, with more neurons, consume more energy.
RESULTS: Here we examined the intrinsic relationships between metabolism, body-brain size ratios and neuronal densities of both endothermic and ectothermic animals. We formulated a general model to elucidate the key factors that correlate with brain enlargement, and the origin of allometric body-brain size scaling. This framework identified temperature as a critical factor in brain enlargement via temperature-regulated changes in metabolism. Our framework predicts that ectothermic animals living in tropical climates should have brain sizes that are several times larger than those of ectothermic animals living in cold climates. This prediction was confirmed by data from experiments in fish brains. Our framework also suggests that a rapid increase in the number of less energy-demanding glial cells may be another important factor contributing to the ten-fold increase in the brain sizes of endotherms compared with ectotherms.
CONCLUSIONS: This study thus provides a quantitative theory that predicts the brain sizes of all the major types of animals and quantifies the contributions of temperature-dependent metabolism, body size and neuronal density.

References

  1. PLoS One. 2011 Apr 06;6(4):e18277 [PMID: 21494328]
  2. PeerJ. 2014 Mar 13;2:e301 [PMID: 24688876]
  3. Front Neuroanat. 2009 Jun 29;3:8 [PMID: 19636383]
  4. J Anim Ecol. 2010 May;79(3):610-9 [PMID: 20180875]
  5. PLoS One. 2010 Mar 10;5(3):e9617 [PMID: 20224776]
  6. J Exp Biol. 1970 Jun;52(3):539-52 [PMID: 5465273]
  7. Brain Behav Evol. 2010;76(1):32-44 [PMID: 20926854]
  8. Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):1051-6 [PMID: 17215372]
  9. J Cereb Blood Flow Metab. 2012 Jul;32(7):1222-32 [PMID: 22434069]
  10. Trends Cogn Sci. 2005 May;9(5):250-7 [PMID: 15866152]
  11. Wiley Interdiscip Rev Cogn Sci. 2013 Jan;4(1):33-45 [PMID: 23529256]
  12. Q Rev Biol. 1983 Dec;58(4):495-512 [PMID: 6665118]
  13. J Comp Neurol. 1995 Mar 6;353(2):213-33 [PMID: 7745132]
  14. Philos Trans R Soc Lond B Biol Sci. 2007 Apr 29;362(1480):587-602 [PMID: 17296597]
  15. Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):12138-43 [PMID: 16880386]
  16. Nature. 2011 Nov 09;480(7375):91-3 [PMID: 22080949]
  17. Proc Natl Acad Sci U S A. 2010 Sep 14;107(37):16216-21 [PMID: 20823252]
  18. Biol Rev Camb Philos Soc. 2005 Nov;80(4):611-62 [PMID: 16221332]
  19. J Comp Neurol. 1954 Aug;101(1):19-51 [PMID: 13211853]
  20. Science. 1997 Apr 4;276(5309):122-6 [PMID: 9082983]
  21. Annu Rev Physiol. 1995;57:69-95 [PMID: 7778882]
  22. Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3549-54 [PMID: 23319606]
  23. J Exp Biol. 2005 May;208(Pt 9):1611-9 [PMID: 15855392]
  24. BMC Biol. 2007 May 09;5:18 [PMID: 17488526]
  25. Science. 2001 Sep 21;293(5538):2248-51 [PMID: 11567137]
  26. Brain Res Bull. 1998 Jun;46(3):175-87 [PMID: 9667810]
  27. Ann Hum Biol. 2009 Sep-Oct;36(5):562-72 [PMID: 19575315]
  28. Nature. 2005 Oct 27;437(7063):1349-52 [PMID: 16251963]
  29. Nat Rev Neurosci. 2005 Feb;6(2):151-9 [PMID: 15685220]
  30. Biol Lett. 2006 Dec 22;2(4):557-60 [PMID: 17148287]
  31. Biol Lett. 2006 Mar 22;2(1):125-7 [PMID: 17148344]
  32. Nature. 1981 Sep 3;293(5827):57-60 [PMID: 7266659]
  33. Am J Phys Anthropol. 2010 Dec;143(4):579-90 [PMID: 20623679]
  34. Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3562-7 [PMID: 17360682]
  35. Curr Opin Neurobiol. 2013 Jun;23(3):443-9 [PMID: 23414685]
  36. Ecology. 2007 Feb;88(2):315-23 [PMID: 17479750]
  37. Science. 1981 Apr 3;212(4490):43-5 [PMID: 17747629]
  38. Biol Rev Camb Philos Soc. 2010 Feb;85(1):111-38 [PMID: 19895606]
  39. Am J Physiol. 1981 Sep;241(3):R203-12 [PMID: 7282965]
  40. Science. 2007 Sep 7;317(5843):1344-7 [PMID: 17823343]
  41. J Comp Neurol. 2009 Apr 10;513(5):532-41 [PMID: 19226510]
  42. Biosci Rep. 2001 Apr;21(2):223-36 [PMID: 11725871]
  43. Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16994-9 [PMID: 18952839]
  44. J Hum Evol. 2009 Oct;57(4):392-400 [PMID: 19732937]
  45. PLoS One. 2011 Mar 01;6(3):e17514 [PMID: 21390261]
  46. Prog Brain Res. 2012;195:413-30 [PMID: 22230639]
  47. Trends Neurosci. 2006 Oct;29(10):547-53 [PMID: 16938356]
  48. Curr Biol. 2007 Jan 9;17(1):R29-35 [PMID: 17208176]
  49. Glia. 2011 Sep;59(9):1215-36 [PMID: 21584869]
  50. Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4046-9 [PMID: 12637681]
  51. J Evol Biol. 2012 May;25(5):981-94 [PMID: 22435703]
  52. J Exp Biol. 2008 Jun;211(Pt 11):1792-804 [PMID: 18490395]

MeSH Term

Animals
Biological Evolution
Body Size
Brain
Energy Metabolism
Neuroglia
Neurons
Organ Size
Temperature
Vertebrates

Word Cloud

Created with Highcharts 10.0.0brainsizeanimalsincreasemetabolismbody-brainectothermicenlargementframeworksizesenergyneuronskeylargerbrainsneuronaloriginallometricscalingtemperaturefactorpredictslivingclimatesBACKGROUND:Brainsignalingrequirescostmaintainingsupportingenergeticallydemandingconstraintdramaticamongmammalsbirdsunderstoodwithoutsolvingconundrum:consumeRESULTS:examinedintrinsicrelationshipsratiosdensitiesendothermicformulatedgeneralmodelelucidatefactorscorrelateidentifiedcriticalviatemperature-regulatedchangestropicalseveraltimescoldpredictionconfirmeddataexperimentsfishalsosuggestsrapidnumberlessenergy-demandingglialcellsmayanotherimportantcontributingten-foldendothermscomparedectothermsCONCLUSIONS:studythusprovidesquantitativetheorymajortypesquantifiescontributionstemperature-dependentbodydensityEffectgliavertebrates

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