Abstract
Humans have the largest brain of any primate. While it seems logical to assume that overall size is very important for generating complex behaviours, brain size relative to body size has been considered to be a major factor in predicting overall brain capacity. It turns out, however, that the absolute number of neurons in the cerebral cortex, regardless of body mass, may be a more relevant factor. Here we review the ways in which brains have increased in size, why absolute brain size is sometimes important, and why the size of the human brain allowed us to have cognitive abilities that exceed those of other primates. We suggest that cognitive functions are largely mediated by the neocortex, and because the human brain scales like a typical primate brain, the large neocortex of humans contains more neurons than any other mammal, even those with larger brains such as elephants. Further, as neurons in primary sensory cortex increase in numbers with brain size at a greater rate than the increase in the number of neurons in thalamic relay nuclei, primates with larger brains and more neocortex also have more neurons to analyze these sensory inputs. As numbers of neurons increase, individual neurons are free to specialize in different ways, generating increasing variability in cell size, shape, dendritic arborization and other features. In addition, an expanded cortical sheet contains more cortical areas, thereby increasing the number of computational levels involved in information processing, decision-making, and information storage. Having more cortical areas allows any given area to become more specialized in terms of laminar and sub-laminar organization, modular organization, connectivity and function. Increases in cortical field number also allow for greater variation in the sizes of areas, and thereby different types of functional specializations. Finally, large brains have more areas that are removed from primary sensory inputs and capable of hemispheric specialization. Of course, the costs of a large brain are considerable in terms of gestation time, postnatal vulnerability, and metabolic costs. Thus, it is not surprising that most mammals have relatively small brains that are constrained in their processing capacity, but are more metabolically efficient, and mature rapidly allowing for early reproduction.
References
Allman J, McLaughlin T, Hakeem A (1993) Brain weight and life-span in primate species. Proc Natl Acad Sci U S A 90:118–122
Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Intuition and autism: a possible role for Von Economo neurons. Trends Cogn Sci 9:367–373
Azevedo FAC, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, Leite REP, Jacob Filho W, Lent R, Herculano-Houzel S (2009) Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513:532–541
Balsters JH, Cussans E, Diedrichsen J, Phillips JK, Ramnani N (2010) Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules. NeuroImage 49:2045–2052
Baldwin MKL, Cooke DF, Krubitzer L (2016) Intracortical microstimulation maps of motor, somatosensory, and posterior parietal cortex in tree shrews (tupaia belangeri) reveal complex movement representations. Cereb Cortex 27:1439–1456
Barrickman NL, Bastian ML, Isler K, Van Schaik CP (2008) Life history costs andbenefits of encephalization: a comparative test using data from long-term studies of primates in the wild. J Hum Evol 54:568–590
Barton RA, Harvey PH (2000) Mosaic evolution of brain struture in mammals. Nature 405: 1055–1058
Brodal A (1981) Neurological anatomy, 3rd edn. Oxford University Press, Oxford
Brodmann K (1909) Vergleichende lokalisationslehre der grosshirnride. Barth, Leipzig
Brown AR, Teskey GC (2014) Motor cortex is functionally organized as a set of spatially distinct representations for complex movements. J Neurosci 34:13574–13585
Buxhoeveden DP, Switala AE, Roy E, Litaker M, Casanova MF (2001) Morphological differences between minicolumns in human and nonhuman primate cortex. Am J Phys Anthropol 115:361–371
Byrne RW, Corp N (2004) Neocortex size predicts deception rate in primates. Proc R Soc Lond B 271:1693–1699
Caminiti R, Ghaziri H, Galuske R, Hof PR, Innocenti GM (2009) Evolution amplified processing with temporally dispersed slow neuronal connectivity in primates. Proc Natl Acad Sci U S A 106:19551–19556
Casanova MF, Opris I (2015) Recent advances in the modular organization of the cortex. Springer, New York
Cherniak C (1990) The bounded brain: toward quantitative neuroanatomy. J Cogn Neurosci 2: 58–68
Collins CE, Hendrickson A, Kaas JH (2005) Overview of the visual system of Tarsius. Anat Rec 287A:1013–1025
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 primate brains. Brain Struct Funct 218:805–816
Collins CE, Turner EC, Sawyer EK, Reed JL, Young NA, Flaherty DK, Kaas JH (2016) Cortical cell and neuron density estimates in one chimpanzee hemisphere. Proc Natl Acad Sci U S A 113:740–745
Cooper HM, Herbin M, Nevo E (1993) Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol 328:313–350
Creutzfeldt OD (1993) Cortex Cerebri English edition. Hubent and Co., Gottingen
Cusick CG, Kaas JH (1986) Interhemispheric connections of cortical sensory and motor maps in primates. In: Lepore F, Ptito M, Jasper HH (eds) Two hemispheres- one brain. Alan R Liss, New York, pp 83–102
Deaner RO, Isler K, Burkart J, van Schaik C (2007) Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav Evol 70:115–124
Delacour J (1997) Neurobiology of consciousness: an overview. Behav Brain Res 85:127–141
Desmurget M, Richard N, Harquel S, Baraduc P, Szathmari A, Mottolese C, Sirigu A (2014) Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus. Proc Natl Acad Sci U S A 111:5718–5722
Doty RW (2007) Cortical commissural connections in primates. In: Kaas JH, Preuss TM (eds) Evolution of nervous systems, vol 4. Primates. Elsevier, London, pp 277–279
Dunbar RIM (1998) The social brain hypothesis. Evol Anthropl 6:178–190
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 A Discov Mol Cell Evol Biol 288A:26–35
Fan S, Hansen ME, Lo Y, Tishkoff SA (2016) Going global by adapting local: a review of recent human adaptation. Science 354:54–59
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Felleman DJ, Lim H, Xiao Y, Wang Y, Eriksson A, Parajuli A (2015) The representation of orientation in macaque V2: four stripes not three. Cereb Cortex 25:2354–2369
Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578–1584
Fonseca-Azevedo K, Herculano-Houzel S (2012) Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution. Proc Natl Acad Sci U S A 109:18571–18576
Fournier J, Muller CM, Laurent G (2015) Looking for the roots of cortical sensory computation in three-layered cortex. Current Opin Neurobiol 3l:119–126
Frey SH (2008) Tool use, communicative gesture and cerebral asymmetries in the modern human brain. Philos Trans R Soc Lond Ser B Biol Sci 363:1951–1957
Fries W, Keizer K, Kuypers HG (1985) Large layer VI cells in macaque striate cortex (Meynert cells) project to both superior colliculus and prestriate visual area V5. Exp Brain Res 58:613–616
Gabi M, Neves K, Masseron C, Ribeiro PFM, Ventura-Antunes L, Torres L, Mota B, Kaas JH, Herculano-Houzel S (2016) No relative expansion of the number of prefrontal neurons in primate and human evolution. Proc Natl Acad Sci U S A 113:9617–9622
Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? Brain 123(Pt 7):1293–1326
Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Ugurbil K, Andersson J, Beckmann CF, Jenkinson M, Smith SM, Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536:171–178
Goldman-Rakic PS (1996) Regional and cellular fractionation of working memory. Proc Natl Acad Sci U S A 93:13473–13480
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25
Gould HJ, Cusick CG, Pons TP, Kaas JH (1986) The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys. J Comp Neurol 247(3):297–325
Gould SJ (1981) Mismeasure of man. Norton, New York
Graziano MS (2009) The intelligent movement machine. Oxford University Press, New York
Herculano-Houzel S (2009) The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci 3:31
Herculano-Houzel S (2015) Decreasing sleep requirement with increasing numbers of neurons as a driver for bigger brains and bodies in mammalian evolution. Proc R Soc B 282:20151853
Herculano-Houzel S (2016) The human advantage. MIT Press, Cambridge
Herculano-Houzel S (2017) Numbers of neurons as biological correlates of cognitive capability. Curr Opin Behav Sci 16:1–7
Herculano-Houzel S, Mota B, Lent R (2006) Cellular scaling rules for rodent brains. Proc Natl Acad Sci U S A 103:12138–12143
Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci U S A 104:3562–3567
Herculano-Houzel S (2010) Coordinated scaling of cortical and cerebellar numbers of neurons. Front Neuroanat 4:12. https://doi.org/10.3389/fnana.2010.00012
Herculano-Houzel S, Mota B, Wong P, Kaas JH (2010) Connectivity-driven white matter scaling and folding in primate cerebral cortex. Proc Natl Acad Sci U S A 107:19008–19013
Herculano-Houzel S, Watson C, Paxinos G (2013) Distribution of neurons in functional areas of the mouse cerebral cortex reveals quantitatively different cortical zones. Front Neuroanat 7:35
Herculano-Houzel S, Manger PR, Kaas JH (2014a) Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size. Front Neuroanat 8:77
Herculano-Houzel S, Avelino-de-Souza K, Neves K, PorfÃrio J, Messeder D, Feijó LM, Maldonado J, Manger PR (2014b) The elephant brain in numbers. Front Neuroanat 8:46
Herculano-Houzel S, Kaas JH, de Oliveira-Souza R (2016) Corticalization of motor control in humans is a consequence of brain scaling in primate evolution. J Comp Neurol 524:448–455
Hill J, Inder T, Neil J, Dierker D, Harwell J, Van Essen D (2010) Similar patterns of cortical expansion during human development and evolution. Proc Natl Acad Sci U S A 107: 13135–13140
Jerison H (1973) Evolution of the brain and intelligence. Academic, New York
Kaas JH (2000) Why brain size is so important: design problems and solutions as neocortex gets bigger or smaller. Brain Mind 1:7–23
Kaas JH (2006) Evolution of the neocortex. Curr Biol 16:R910–R914
Kaas JH (2007) Reconstructing the organization of neocortex of the first mammals and subsequent modifications. In: Kaas JH, Krubitzer LA (eds) Evolution of nervous systems, vol. 3, mammals. Elsevier, London, pp 27–48
Kaas JH (2012) Evolution of columns, modules, and domains in the neocortex of primates. Proc Natl Acad Sci U S A 109(Suppl 1):10655–10660
Kaas JH, Preuss TM (2014) Human brain evolution In: Fundamental neuroscience, 4th ed., Larry R Squire (ed), Elsevier, London, pp 901–918
Kaas JH, Balaram P (2015) The types of functional and structural subdivisions of cortical areas. In: Casanova MF, Opris I (eds) Recent advances on the modular organization of the Cortex. Springer, New York, pp 35–62. https://doi.org/10.1007/978-94-37-9900-3_4
Kaas JH, Stepniewska I (2016) Evolution of posterior parietal cortex and parietal-frontal networks for specific actions in primates. J Comp Neurol 524:595–608
Kaas JH (2017) The organization of neocortex in early mammals. In: Herculano-Houzel S (ed) Evolution of nervous systems, Mammals, vol 2, 2nd edn. Elsevier, London, pp 87–101
Krubitzer L, Campi KL, Cooke DF (2011) All rodents are not the same: a modern synthesis of cortical organization. Brain Behav Evol 78:51–93
Krubitzer L, Manger P, Pettigrew J, Calford M (1995) Organization of somatosensory cortex in monotremes: in search of the prototypical plan. J Comp Neurol 351:261–306
Kruska DCT (2007) The effects of domestication on brain size. In: Kaas JH, Krubitzer LA (eds) Evolution of nervous systems, Mammals, vol 3. Elsevier, London, pp 143–153
Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246
Leiner HC, Leiner A, Dow RS (1989) Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? Behav Neurosci 103:998–1008
Liao CC, Reed JL, Kaas JH, Qi HX (2016) Intracortical connections are altered after long-standing deprivation of dorsal column inputs in the hand region of area 3b in squirrel monkeys. J Comp Neurol 524:1494–1526
Livingstone M, Hubel D (1988) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240:740–749
MacLean EL et al (2014) The evolution of self-control. Proc Natl Acad Sci U S A 111:E2141–E2148
McHenry HM (1994) Tempo and mode in human evolution. Proc Natl Acad Sci U S A 91:6780–6786
Mota B, Herculano-Houzel S (2014) All brains are made of this: a fundamental building block of brain matter with matching neuronal and glial masses. Front Neuroanat 8:127
Mota B, Herculano-Houzel S (2015) Cortical folding scales universally with surface area and thickness, not number of neurons. Science 349:74–77
Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434
Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, Hof PR (1999) A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci U S A 96:5268–5273
Opris I, Popa IL, Casanova MF (2015) Prefrontal cortical microcircuits for executive control of behavior. In: Casanova MF, Opris I (eds) Recent advances on the modular organization of cortex. Springer, New York, pp 157–179
Perge JA, Niver JE, Margraini E, Balasubramanian V, Sterling P (2012) Why do axons differ in caliber? J Neurosci 32:626–638
Phillips KA, Stimpson CD, Smaers JB, Raghanti MA, Jacobs B, Popratiloff A, Hof PR, Sherwood CC (2015) The corpus callosum in primates: processing speed of axons and the evolution of hemispheric asymmetry. Proc Biol Sci 282(1818):282. 20151535
Pinker S (2009) How the mind works. W W Norton and Company, New York
Preuss TM, Qi H, Kaas JH (1999) Distinctive compartmental organization of human primary visual cortex. Proc Natl Acad Sci U S A 96:11601–11606
Preuss TM (1995) Do rats have prefrontal cortex? The rose-woolsey-akert program reconsidered. J Cogn Neurosci 7:1–24
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
Radinsky L (1976) Cerebral clues. Nat Hist 85:54–59
Ramnani N (2006) The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci 7:511–522
Ramnani N, Behrens TE, Johansen-Berg H, Richter MC, Pinks MA, Andersoon JL, Rudebeck P, Ciccarelli O, Richter W, Thomson AJ, Gross CG, Robson MD, Kastner S, Matthews PS (2006) The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from macaque monkeys and humans. Cereb Cortex 16:811–818
Rauschecker JP, Scott SK (2009) Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12:718–724
Ringo JL, Doty RW, Demeter S, Simard PY (1994) Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cereb Cortex 4:331–343
Spocter MA, Raghanti MA, Butti C, Hof PR, Sherwood CC (2015) The minicolumns in comparative cortex. In: Casanova MF, Opris I (eds) Recent advances on the modular organization of the cortex. Springer, New York, pp 63–80
Stein JF, Glickstein M (1992) Role of the cerebellum in visual guidance of movement. Physiol Rev 72:967–1017
Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15:403–442
Timmermann A, Friedrich T (2016) Late Pleistocene climate drivers of early human migration. Nature 538:92–95
Tremblay P, Dick AS (2016) Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain Lang 162:60–71
Turner EC, Young NA, Reed JL, Collins CE, Flaherty DK, Gabi M, Kaas JH (2016) Distributions of cells and neurons across the cortical sheet in old world macaques. Brain Behav Evol 88:1–13. https://doi.org/10.11591000446762
Ungerleider LG, Haxby JV (1994) ‘What’ and ‘where’ in the human brain. Curr Opin Neurobiol 4:157–165
Van Essen D (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318
Ventura-Antunes L, Mota B, Herculano-Houzel S (2013) Different scaling of white matter volume, cortical connectivity and gyrification across rodent and primate brains. Front Neuroanat 7:3
Watson C, Provis J, Herculano-Houzel S (2012) What determines motor neuron number? Slow scaling of facial motor neuron numbers with body mass in marsupials and primates. Anat Rec 295:1683–1691
Welker WI (1990) Why does cerebral cortex fissure and fold? In: Jones EG, Peters A (eds) Cerebral cortex, vol 8B. Plenum Press, New York, pp 3–136
Wong P, Kaas JH (2010) Architectonic subdivisions of neocortex in the galago (Otolemur garnetti). Anat Rec 293:1033–1069
Wong P, Peebles JK, Asplund CL, Collins CE, Herculano-Houzel S, Kaas JH (2013) Faster scaling of auditory neurons in cortical areas relative to subcortical structures in primate brains. Brain Behav Evol 81:209–218
Young NA, Szabo CA, Phelix CF, Flaherty DK, Balaram P, Foust-Yeoman KB, Collins CE, Kaas JH (2013) Epileptic baboons have lower numbers of neurons in specific areas of cortex. Proc Natl Acad Sci U S A 110:19107–19112
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Kaas, J.H., Herculano-Houzel, S. (2017). What Makes the Human Brain Special: Key Features of Brain and Neocortex. In: Opris, I., Casanova, M.F. (eds) The Physics of the Mind and Brain Disorders. Springer Series in Cognitive and Neural Systems, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-319-29674-6_1
Download citation
DOI: https://doi.org/10.1007/978-3-319-29674-6_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-29672-2
Online ISBN: 978-3-319-29674-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)