Linking brains and brawn: Exercise and the evolution of human neurobiology

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1750, 2013, Pages

  Raichlen, David A ^a   Polk, John D ^b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Brain size; Brain derived neurotrophic factor; Encephalization; Endurance running; Neurotrophins; Physical activity

Indexed keywords

BRAIN; FOOD AVAILABILITY; HUMAN EVOLUTION; HUNTER-GATHERER; LIFESTYLE; NATURAL SELECTION; NEUROLOGY; PROTEIN;

EID: 84869842192     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.2250     Document Type: Review

References (89)

1. Cotman CW, Berchtold NC, Christie LA. 2007 Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 30, 464-472. (doi:10.1016/j.tins.2007.06.011)
2. van Praag H. 2008 Neurogenesis and exercise: past and future directions. Neuromol. Med. 10, 128-140. (doi:10.1007/s12017-008-8028-z)
3. Colcombe SJ, Kramer AF. 2003 Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol. Sci. 14, 125-130. (doi:10.1111/ 1467-9280.t01-1-01430)
4. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD. 2003 VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci 18, 2803-2812.
5. Hillman CH, Erickson KI, Kramer AF. 2008 Be smart, exercise your heart: exercise effects on brain and cognition. Nat. Rev. Neurosci. 9, 58-65. (doi:10. 1038/nrn2298)
6. Raichlen DA, Gordon AD. 2011 Relationship between exercise capacity and brain size in mammals. PLoS ONE 6, e20601. (doi:10.1371/ journal.pone.0020601)
7. Trejo JL, Carro E, Torres-Aleman I. 2001 Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21, 1628-1634.
8. van Praag H, Kempermann G, Gage FH. 1999 Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270. (doi:10.1038/6368)
9. Lieberman DE. 2011 The evolution of the human head. Cambridge, MA: Harvard University Press.
10. Schoenemann PT. 2006 Evolution of the size and functional areas of the human brain. Annu. Rev. Anthropol. 35, 379-406. (doi:10.1146/annurev. anthro.35.081705.123210)
11. Holloway RL. 2008 The human brain evolving: a personal retrospective. Annu. Rev. Anthropol. 37, 1-19. (doi:10.1146/annurev.anthro.37.081407.085211)
12. Holloway RL, Broadfield DC, Yuan MS. 2004 The human fossil record, vol. 3. Brain endocasts: the paleoneurological evidence. Hoboken, NJ: Wiley and Sons.
13. Sherwood CC, Subiaul F, Zawidzki TW. 2008 A natural history of the human mind: tracing evolutionary changes in brain and cognition. J. Anatomy 212, 426-454. (doi:10.1111/j. 1469-7580.2008.00868.x)
14. Dunbar RIM. 2003 The social brain: mind, language, and society in evolutionary perspective. Annu. Rev. Anthropol. 32, 163-181. (doi:10.1146/annurev. anthro.32.061002.093158)
15. Barton RA. 1996 Neocortex size and behavioural ecology in primates. Proc. R. Soc. Lond. B 263, 173-177. (doi:10.1098/rspb.1996.0028)
16. Milton K. 1981 Distribution patterns of tropical plants as an evolutionary stimulus to primate mental development. Am. Anthropol. 83, 534-548. (doi:10.1525/aa.1981.83.3.02a00020)
17. Bramble DM, Lieberman DE. 2004 Endurance running and the evolution of Homo. Nature 432, 345-352. (doi:10.1038/nature03052)
18. Carrier DR. 1984 The energetic paradox of human running and hominid evolution. Curr. Anthropol. 25, 483-495. (doi:10.1086/203165)
19. Lieberman DE, Bramble DM, Raichlen DA, Shea JJ. 2009 Brains versus brawn and the evolution of Homo. In The origin of homo (eds F Grine, REF Leakey), pp. 77-92. New York, NY: Plenum.
20. Lieberman DE, Raichlen DA, Pontzer H, Bramble DM, Cutright-Smith E. 2006 The human gluteus maximus and its role in running. J. Exp. Biol. 209, 2143-2155. (doi:10.1242/jeb.02255)
21. Hilton CE, Meldrum DJ. 2004 Striders, runners, and transporters. In From biped to strider: the emergence of modern human walking, running, and resource transport (eds DJ Meldrum, CE Hilton), pp. 1-8. New York, NY: Kluwer Academic/Plenum Publishers.
22. Kelly RL. 1992 Mobility/sedentism: concepts, archaeological measures, and effects. Annu. Rev. Anthropol. 21, 43-66. (doi:10.1146/annurev.an.21. 100192.000355)
23. Krantz GS. 1968 Brain size and hunting ability in earliest man. Curr. Anthropol. 9, 450-451. (doi:10. 1086/200927)
24. Malina RM, Little BB. 2008 Physical activity: the present in the context of the past. Am. J. Hum. Biol. 20, 373-391. (doi:10.1002/ajhb.20772)
25. Chaddock L, Erickson KI, Prakash RS, VanPatter M, Voss MW, Pontifex MB, Raine LB, Hillman CH, Kramer AF. 2010 Basal ganglia volume is associated with aerobic fitness in preadolescent children. Dev. Neurosci. 32, 249-256. (doi:10.1159/000316648)
26. Chaddock L, Hillman CH, Buck SM, Cohen NJ. 2011 Aerobic fitness and executive control of relational memory in preadolescent children. Med. Sci. Sports Exerc. 43, 344-349. (doi:10.1249/MSS. 0b013e3181e9af48)
27. Colcombe SJ et al. 2006 Aerobic exercise training increases brain volume in aging adults. J. Gerontol. 61A, 1166-1170.
28. Mandyam CD, Wee S, Eisch AJ, Richardson HN, Koob GF. 2007 Methamphetamine self-administration and voluntary exercise have opposing effects on medial prefrontal cortex gliogenesis. J. Neurosci. 27, 11 442-11 450. (doi:10.1523/JNEUROSCI.2505-07.2007)
29. Ehninger D, Kempermann G. 2003 Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb. Cortex 13, 845-851. (doi:10.1093/cercor/13.8.845)
30. Rhyu IJ et al. 2010 Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 167, 1239-1248. (doi:10.1016/j.neuroscience. 2010.03.003)
31. van Praag H, Shubert T, Zhao CM, Gage FH. 2005 Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25, 8680-8685. (doi:10.1523/JNEUROSCI.1731-05.2005)
32. Vaynman S, Ying Z, Gomez-Pinilla F. 2004 Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J. Neurosci. 20, 2580-2590. (doi:10.1111/ j.1460-9568.2004.03720.x)
33. Chaddock L et al. 2010 A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res. 1358, 172-183. (doi:10.1016/j.brainres. 2010.08.049)
34. Erickson KI et al. 2011 Exercise training increases size of hippocampus and improves memory. Proc. Natl Acad. Sci. USA 108, 3017-3022. (doi:10.1073/ pnas.1015950108)
35. Peters J, Dauvermann M, Mette C, Platen P, Franke J, Hinrichs T, Daum I. 2009 Voxel-based morphometry reveals an association between aerobic capacity and grey matter density in the right anterior insula. Neuroscience 163, 1102-1108. (doi:10.1016/j.neuroscience.2009.07.030)
36. Sibley BA, Etnier JL. 2003 The relationship between physical activity and cognition in children: a metaanalysis. Pediatr. Exerc. Sci. 15, 243-256.
37. Griffin EW, Mullally S, Foley C, Warmington SA, Mara SM, Kelly AM. 2011 Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol. Behav. 104, 934-941. (doi:10.1016/j.physbeh. 2011.06.005)
38. Hawkins HL, Kramer AF, Capaldi D. 1992 Aging, exercise, and attention. Psychol. Aging 7, 643-653. (doi:10.1037/0882-7974.7.4.643)
39. Smith PJ, Blumenthal JA, Hoffman BM, Cooper H, Strauman TA, Welsh-Bohmer K, Browndyke JN, Sherwood A. 2010 Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom. Med. 72, 239-252. (doi:10.1097/PSY. 0b013e3181d14633)
40. Cotman CW, Berchtold NC. 2002 Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25, 295-301. (doi:10. 1016/S0166-2236(02)02143-4)
41. Allen SJ, Dawbarn D. 2006 Clinical relevance of the neurotrophins and their receptors. Clin. Sci. 110, 175-191. (doi:10.1042/CS20050161)
42. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW. 1995 Exercise and brain neurotrophins. Nature 373, 109. (doi:10.1038/373109a0)
43. Zoladz JA, Pilc A, Majerczak J, Grandys M, Zapart-Bukowska J, Duda K. 2008 Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J. Physiol. Pharmacol. 59, 119-132.
44. Carro E, Nunez A, Busiguina S, Torres-Aleman I. 2000 Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 20, 2926-2933.
45. Aberg ND, Brywe KG, Isgaard J. 2006 Aspects of growth hormone and insulin-like growth factor-I related to neuroprotection, regeneration, and functional plasticity in the adult brain. Sci. World J. 6, 53-80. (doi:10.1100/tsw.2006.22)
46. Cao L, Jiao XY, Zuzga DS, Liu YH, Fong DM, Young D, During MJ. 2004 VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36, 827-835. (doi:10.1038/ng1395)
47. Gustafsson T, Bodin K, Sylven C, Gordon A, Tyni-Lenne R, Jansson E. 2001 Increased expression of VEGF following exercise training in patients with heart failure. Eur. J. Clini. Invest. 31, 362-366. (doi:10.1046/j.1365-2362.2001.00816.x)
48. Koziris LP, Hickson RC, Chatterton RTJ, Groseth RT, Christie JM, Goldflies DG, Unterman TG. 1999 Serum levels of total and free IGF-I and IGFBP-3 are increased and maintained in long-term training. J. Appl. Physiol. 86, 1436-1442.
49. Cappon J, Brasel JA, Mohan S, Cooper DM. 1994 Effect of brief exercise on circulating insulin-like growth factor I. J. Appl. Physiol. 76, 2490-2496. (doi:10.1063/1.357607)
50. Kraus RM, Stallings HWI, Yeager RC, Gavin TP. 2004 Circulating plasma VEGF response to exercise in sedentary and endurance-trained men. J. Appl. Physiol. 96, 1445-1450. (doi:10.1152/japplphysiol. 01031.2003)
51. Amaral SL, Papanek PE, Greene AS. 2001 Angiotensin II and VEGF are involved in angiogenesis induced by short-term exercise training. Am. J. Physiol. 281, H1163-H1169.
52. Weibel ER, Bacigalupe LD, Schmitt B, Hoppeler H. 2012 Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir. Physiol. Neurobiol. 140, 115-132. (doi:10.1016/j.resp.2004.01.006)
53. Pedersen BK, Pedersen M, Krabbe KS, Bruunsgaard H, Matthews VB, Febbraio MA. 2009 Role of exercise-induced brain-derived neurotrophic factor production in the regulation of energy homeostasis in mammals. Exp. Physiol. 94, 1153-1160. (doi:10. 1113/expphysiol.2009.048561)
54. Coggan AR. 1991 Plasma-glucose metabolism during exercise in humans. Sports Med. 11, 102-124. (doi:10.2165/00007256-199111020-00003)
55. Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, Knudsen GM, Aznar S. 2011 Blood BDNF concentrations reflect brain-tissue BDNF across species. Int. J. Neuropsychopharmacol. 14, 347-353. (doi:10.1017/S1461145710000738)
56. Fabel K, Kempermann G. 2008 Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromol. Med. 10, 59-66. (doi:10. 1007/s12017-008-8031-4)
57. Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, Wolf SA. 2010 Why and how physical activity promotes experience-induced brain plasticity? Front. Neurosci. 4, 1-9. (doi:10.3389/ fnins.2010.00189)
58. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F. 1995 IGF-I disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumincontaining neurons. Neuron 14, 717-730. (doi:10. 1016/0896-6273(95)90216-3)
59. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R. 2006 The disease progression of Mecp2 mutant mice affected by the level of BDNF expression. Neuron 49, 341-348. (doi:10.1016/j.neuron.2005.12.027)
60. Cheng CM, Joncas G, Reinhardt RR, Farrer R, Quarles R, Janssen J. 1998 Biochemical and morphometric analyses show that myelination in the insulin-like growth factor 1 null brain is proportionate to its neuronal composition. J. Neurosci. 18, 5673-5681.
61. Ye P, Xing Y, Dai Z, D'Ercole AJ. 1996 In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-I increases proliferation of granule cell progenitors. Dev. Brain Res. 95, 44-54. (doi:10.1016/0165-3806(96)00492-0)
62. Raab S, Beck H, Gaumann A, Yuce A, Gerber H, Plate K, Hammes H, Ferrara N, Breier G. 2004 Impaired brain angiogenesis and neuronal apoptosis induced by conditional homozygous inactivation of vascular endothelial growth factor. Thromb. Haemost. 91, 595-605.
63. Woods KA, CamachoHubner C, Savage MO, Clark AJL. 1996 Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. New Engl. J. Med. 335, 1363-1367. (doi:10.1056/ NEJM199610313351805)
64. Hansen-Pupp I et al. 2011 Postnatal decrease in circulating insulin-like growth factor-i and low brain volumes in very preterm infants. J. Clin. Endocrinol. Metab. 96, 1129-1135. (doi:10.1210/jc.2010-2440)
65. Rao R, Mashburn CB, Mao J, Wadhwa N, Smith GM, Desai NS. 2009 Brain-derived neurotrophic factor in infants,32 weeks gestational age: correlation with antenatal factors and postnatal outcomes. Pediatr. Res. 65, 548-552. (doi:10.1203/PDR. 0b013e31819d9ea5)
66. Johnson RA, Mitchell GS. 2003 Exercise-induced changes in hippocampal brain-derived neurotrophic factor and neurotrophin-3: effects of rat strain. Brain Res. 983, 108-114. (doi:10.1016/S0006-8993(03)03039-7)
67. Chappell MA, Garland TJ, Robertson GF, Saltzmann W. 2007 Relationships among running performance, aerobic physiology and organ mass in male Mongolian gerbils. J. Exp. Biol. 210, 4179-4197. (doi:10.1242/jeb.006163)
68. Prior SJ, Hagberd JM, Paton CM, Douglass LW, Brown MD, McLenithan JC, Roth SM. 2006 DNA sequence variation in the promoter region of the VEGF gene impacts VEGF gene expression and maximal oxygen consumption. Am. J. Physiol. Heart Circ. Physiol. 290, H1848-H1855. (doi:10.1152/ ajpheart.01033.2005)
69. Tang K, Breen EC, Gerber HP, Ferrara NMA, Wagner PD. 2004 Capillary regression in vascular endothelial growth factor-deficient skeletal muscle. Physiol. Genomics 18, 63-69. (doi:10.1152/ physiolgenomics.00023.2004)
70. Howlett RA, Gonzalez NC, Wagner HE, Fu Z, Britton SL, Koch LG, Wagner PD. 2003 Selected contribution: skeletal muscle capillarity and enzyme activity in rats selectively bred for running endurance. J. Appl. Physiol. 94, 1682-1688.
71. 2, max. Physiol. Genomics 35, 213-221. (doi:10.1152/ physiolgenomics.90282.2008)
72. Wikgren J, Mertikas GG, Raussi P, Tirkkonen R, Ayravainen L, Pelto-Huikko M, Koch LG, Britton SL, Kainulainen H. 2012 Selective breeding for endurance running capacity affects cognitive but not motor learning in rats. Physiol. Behav. 106, 95-100. (doi:10.1016/j.physbeh.2012.01.011)
73. Swallow JG, Carter PA, Garland Jr T. 1998 Artificial selection for increased wheel-running behavior in house mice. Behav. Genet. 28, 227-237. (doi:10. 1023/A:1021479331779)
74. Rezende EL, Garland TJ, Chappell MA, Malisch JL, Gomes FR. 2006 Maximum aerobic performance in lines of Mus selected for high wheel-running activity: effects of selection, oxygen availability, and the mini-muscle phenotype. J. Exp. Biol. 209, 115-127. (doi:10.1242/jeb.01883)
75. Johnson RA, Rhodes JS, Jeffrey SL, Garland Jr T, Mitchell GS. 2003 Hippocampal brain-derived neurotrophic factor but not neurotrophin-3 increases more in mice selected for increased voluntary wheel running. Neuroscience 121, 1-7. (doi:10.1016/ S0306-4522(03)00422-6)
76. Rhodes JS, van Praag H, Jeffrey S, Girard I, Mitchell GS, Garland TJ, Gage FH. 2003 Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav. Neurosci. 117, 1006-1016. (doi:10.1037/0735-7044. 117.5.1006)
77. Audet GN, Meek TH, Garland TJ, Olfert IM. 2011 Expression of angiogenic regulators and skeletal muscle capillarity in slectively bred high aerobic capacity mice. Exp. Physiol. 11, 1138-1150.
78. Kolb EM. 2010 Neurobiological and physiological underpinnings of high voluntary wheel running. Riverside, CA: University of California at Riverside.
79. Kolb EM, Rezende EL, Holness L, Radtke A, Lee SK, Obnaus A, Garland TJ. In press. Mice selectively bred for high voluntary wheel running have larger midbrains: support for the mosaic model or brain evolution. J. Exp. Biol.
80. Perez-Barberia FJ, Shultz S, Dunbar RIM. 2007 Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61, 2811-2821. (doi:10.1111/j.1558-5646.2007. 00229.x)
81. Lieberman DE, Bramble DM, Raichlen DA, Shea JJ. 2007 Endurance running and the tyranny of ethnography: a reply to Pickering and Bunn. J. Hum. Evol. 53, 434-437. (doi:10.1016/j.jhevol.2007.01.012)
82. Spoor F, Wood B, Zonneveld F. 1994 Implications of early hominid labyrinth morphology for the evolution of human bipedal locomotion. Nature 369, 645-648. (doi:10.1038/369645a0)
83. Pontzer H. 2006 Locomotor energetics, ranging ecology, and the emergence of the genus Homo. Cambridge, MA: Harvard University Press.
84. Martin RD. 1981 Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293, 57-60. (doi:10.1038/293057a0)
85. Suwa G, Asfaw B, Kono RT, Kubo D, Lovejoy CO, White TD. 2009 The Ardipithecus ramidus skull and its implications for hominid origins. Science 326, 68e61-68e67.
86. Isler K, Kirk EC, Miller JMA, Albrecht GA, Gelvin BR, Martin RD. 2008 Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J. Hum. Evol. 55, 967-978. (doi:10.1016/j.jhevol.2008.08.004)
87. Spoor F, Garlan TJ, Krovitz G, Ryan TM, Silcox MT, Walker A. 2007 The primate semicircular canal system and locomotion. Proc. Natl Acad. Sci. USA 104, 10 808-10 812. (doi:10.1073/pnas. 0704250104)
88. Spoor F, Hublin JJ, Braun M, Zonneveld F. 2003 The bony labyrinth of Neanderthals. J. Hum. Evol. 44, 141-165. (doi:10.1016/S0047-2484(02)00166-5)
89. Dunbar RIM, Shultz S. 2007 Evolution of the social brain. Science 1344, 1344-1347. (doi:10.1126/ science.1145463)