The evolution of distributed association networks in the human brain
2013; Elsevier BV; Volume: 17; Issue: 12 Linguagem: Inglês
10.1016/j.tics.2013.09.017
ISSN1879-307X
AutoresRandy L. Buckner, Fenna M. Krienen,
Tópico(s)Memory and Neural Mechanisms
Resumo•The human brain is triple the size of ancestors that lived 3 million years ago.•Widely distributed cortical association regions are disproportionately expanded in humans compared with other primates.•The separate association regions are connected by multiple large-scale networks that mature late in development.•Cortical expansion may have caused critical properties of association networks to evolve as a spandrel.•Many cortical features may be consequences of expansion in the context of conserved developmental programs. The human cerebral cortex is vastly expanded relative to other primates and disproportionately occupied by distributed association regions. Here we offer a hypothesis about how association networks evolved their prominence and came to possess circuit properties vital to human cognition. The rapid expansion of the cortical mantle may have untethered large portions of the cortex from strong constraints of molecular gradients and early activity cascades that lead to sensory hierarchies. What fill the gaps between these hierarchies are densely interconnected networks that widely span the cortex and mature late into development. Limitations of the tethering hypothesis are discussed as well as its broad implications for understanding critical features of the human brain as a byproduct of size scaling. The human cerebral cortex is vastly expanded relative to other primates and disproportionately occupied by distributed association regions. Here we offer a hypothesis about how association networks evolved their prominence and came to possess circuit properties vital to human cognition. The rapid expansion of the cortical mantle may have untethered large portions of the cortex from strong constraints of molecular gradients and early activity cascades that lead to sensory hierarchies. What fill the gaps between these hierarchies are densely interconnected networks that widely span the cortex and mature late into development. Limitations of the tethering hypothesis are discussed as well as its broad implications for understanding critical features of the human brain as a byproduct of size scaling. Our ancestors advanced tool use, evolved language, and achieved complex social order during the past 3 million years. From one perspective, that is a lot of time for drift and selection to mold a new species. Changes in gene frequencies and adaptive mutations can arise rapidly in isolated populations. From another perspective, it is unexpected given the trajectories of closely related primate species. To anchor this point, consider the divergent evolution of the common chimpanzee and the bonobo over the past 1–2 million years. These two great apes became genetically isolated from one another when the Congo River formed allowing distinct phenotypes to evolve over a short time period [1Prüfer K. et al.The bonobo genome compared with the chimpanzee and human genomes.Nature. 2012; 486: 527-531PubMed Google Scholar]. Bonobos display a matriarchal social order that differs from the aggressive alpha male-dominated society of the chimpanzee [2Boesch C. et al.Behavioural Diversity in Chimpanzees and Bonobos. Cambridge University Press, 2002Crossref Google Scholar, 3Hare B. From hominoid to hominid mind: what changed and why?.Annu. Rev. Anthropol. 2011; 40: 293-309Crossref Scopus (7) Google Scholar]. Chimpanzees use primitive tools to extract food in the wild, whereas bonobos do not [3Hare B. From hominoid to hominid mind: what changed and why?.Annu. Rev. Anthropol. 2011; 40: 293-309Crossref Scopus (7) Google Scholar]. Differences in brain structures exist between the two species that may be important to social behaviors [4Rilling J.K. et al.Differences between chimpanzees and bonobos in neural systems supporting social cognition.Soc. Cogn. Affect. Neurosci. 2012; 7: 369-379Crossref PubMed Scopus (11) Google Scholar], but these differences pale in comparison with the expansion of the life cycle, social organization, and cognitive abilities that emerge in hominins over a slightly longer time frame [5Sherwood C.C. et al.A natural history of the human mind: tracing evolutionary changes in brain and cognition.J. Anat. 2008; 212: 426-454Crossref PubMed Scopus (51) Google Scholar]. Given the quick pace of change observed in the hominin lineage, we are left with a puzzle: how did brain networks that underlie extraordinary human capabilities evolve so rapidly? A large part of the explanation must lie in the brain expansion that separates us from our ape cousins (Box 1). The human brain is more than triple the size of the chimpanzee brain [6Sherwood C.C. et al.Human brain evolution writ large and small.Prog. Brain Res. 2012; 195: 237-254Crossref PubMed Scopus (6) Google Scholar]. Fossil evidence suggests that this increase occurred over roughly the time period when our ancestors advanced their extraordinary abilities [7Holloway R.L. et al.The Human Fossil Record, Brain Endocasts: The Paleoneurological Evidence. John Wiley & Sons, 2004Crossref Google Scholar], but not necessarily in lock step with the exact timing of behavioral and cultural achievements (Box 2). Key genetic events also occurred that may interact with or cause brain expansion in hominins (e.g., [8Enard W. et al.Molecular evolution of FOXP2, a gene involved in speech and language.Nature. 2002; 418: 869-872Crossref PubMed Scopus (561) Google Scholar, 9Ferland R.J. et al.Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome.Nat. Genet. 2004; 36: 1008-1013Crossref PubMed Scopus (196) Google Scholar, 10Mikkelsen T.S. et al.Initial sequence of the chimpanzee genome and comparison with the human genome.Nature. 2005; 437: 69-87Crossref PubMed Scopus (997) Google Scholar, 11Bailey J.A. Eichler E.E. Primate segmental duplications: crucibles of evolution, diversity and disease.Nat. Rev. Genet. 2006; 7: 552-564Crossref PubMed Scopus (241) Google Scholar, 12Vallender E.J. et al.Genetic basis of human brain evolution.Trends Neurosci. 2008; 31: 637-644Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar, 13Dennis M.Y. et al.Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication.Cell. 2012; 149: 912-922Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar, 14McLean C.Y. et al.Human-specific loss of regulatory DNA and the evolution of human-specific traits.Nature. 2011; 471: 216-219Crossref PubMed Scopus (66) Google Scholar, 15Konopka G. et al.Human-specific transcriptional networks in the brain.Neuron. 2012; 75: 601-617Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar]; see [16Somel M. et al.Human brain evolution: transcripts, metabolites and their regulators.Nat. Rev. Neurosci. 2013; 14: 112-127Crossref PubMed Scopus (7) Google Scholar] for discussion).Box 1The evolutionary road to the human brain's expanded cerebral cortexThe hominin brain grew rapidly over the past 3 million years in a primate lineage that had already experienced multiple events that increased brain size (Figure I depicts hominin brain evolution estimated from fossil endocasts, with labels for representative individuals from major species). The most significant determinant of our large brain size is that we are large animals: absolute brain size scales allometrically with body size [148Jerison H.J. Brain to body ratios and the evolution of intelligence.Science. 1955; 121: 447-449Crossref PubMed Google Scholar]. After factoring out body weight, which accounts for as much as 85% of the total variance in brain size across mammalian species, the human brain is about five times larger than one would expect for a typical mammal [149Jerison H.J. Evolution of the brain and intelligence.Curr. Anthropol. 1975; 16: 403-426Crossref Google Scholar, 150Marino L. A comparison of encephalization between odontocete cetaceans and anthropoid primates.Brain Behav. Evol. 1998; 51: 230-238Crossref PubMed Google Scholar]. Primates generally have disproportionately larger brains for their body size than other mammals (quantified as the encephalization quotient). This relative size difference is present at early embryonic stages, suggesting an ancient evolutionary event that shifted a greater proportion of the embryonic precursor cells to commit to a neuronal lineage ([151Count E.W. Brain and body weight in man: their antecedents in growth and evolution: a study in dynamic somatometry.Ann. N. Y. Acad. Sci. 1947; 46: 993-1122Crossref Google Scholar], data interpreted in [152Striedter G.F. Principles of Brain Evolution. Sinauer Associates, 2005Google Scholar]; see also [153Charvet C.J. Finlay B.L. Embracing covariation in brain evolution: large brains, extended development, and flexible primate social systems.Prog. Brain Res. 2012; 195: 71-87Crossref PubMed Scopus (6) Google Scholar]). Differences across primate suborders hint at other major evolutionary events including a step increase in brain size in monkeys (e.g., macaque and squirrel monkey) relative to prosimians (e.g., lemur). The acceleration over the past several million years probably derives from a distinct mechanism. Chimpanzees and humans have roughly the same body size and share a common ancestor about 5–7 million years ago. The early phases of brain development for chimpanzees and humans are conserved, with a similar proportion of the total body size devoted to the brain. At late phases, the brain continues to grow relative to the body in humans but stops earlier in chimpanzees, leading to a relative brain size expansion [152Striedter G.F. Principles of Brain Evolution. Sinauer Associates, 2005Google Scholar] (see also [154Lieberman D.E. The Evolution of the Human Head. Harvard University Press, 2011Google Scholar, 155Sakai T. et al.Fetal brain development in chimpanzees versus humans.Curr. Biol. 2012; 22: R791-R792Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar]). An interesting feature of brain scaling is that brain enlargement disproportionately expands some brain structures more than others. The cerebral cortex in mammals has the most privileged position in brain growth. A key contributor to disproportionate cortical expansion is constraints from embryonic development [135Finlay B.L. Darlington R.B. Linked regularities in the development and evolution of mammalian brains.Science. 1995; 268: 1578-1584Crossref PubMed Google Scholar]. Cerebral cortex progenitor cells are the last to be born among different neuronal pools. Because embryonic development is temporally stretched in large-brained mammals, the cerebral progenitor pool continues to divide for the longest period and forms the largest cell pool. This ‘late equals large’ developmental feature causes the cerebrum to have the greatest relative size increase. The cerebral surface area is ∼120 cm2 in the macaque and a remarkable ∼960 cm2 in the highly gyrified human brain [25Van Essen D.C. Dierker D.L. Surface-based and probabilistic atlases of primate cerebral cortex.Neuron. 2007; 56: 209-225Abstract Full Text Full Text PDF PubMed Google Scholar] (see also [156Rilling J.K. Insel T.R. The primate neocortex in comparative perspective using magnetic resonance imaging.J. Hum. Evol. 1999; 37: 191-223Crossref PubMed Scopus (161) Google Scholar]).Box 2Scaling exceptions and the paradox of Homo floresiensisThe central point of this review is that brain size scaling may have essential, underexplored implications for large-scale circuit organization. However, it is also important to note observations that make clear how brain scaling is not the only factor at work in the evolution of hominin capabilities. For example, a marked increase in brain size was not the initial gateway to stone tool use. The oldest documented stone tools are 2.6 million years old [157Semaw S. et al.2.6-Million-year-old stone tools and associated bones from OGS-6 and OGS-7, Gona, Afar, Ethiopia.J. Hum. Evol. 2003; 45: 169-177Crossref PubMed Scopus (118) Google Scholar] and were made by hominins with moderate encephalization, possibly australopiths. Stone-cut marks are claimed by some to have been made as early as 3.4 million years ago [158McPherron S.P. et al.Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia.Nature. 2010; 466: 857-860Crossref PubMed Scopus (79) Google Scholar]. Living 2.0 million years ago, Australopithecus sediba possessed hand features suggesting stone tool use [159Kivell T.L. et al.Australopithecus sediba hand demonstrates mosaic evolution of locomotor and manipulative abilities.Science. 2011; 333: 1411-1417Crossref PubMed Scopus (41) Google Scholar], but had a brain size small even for australopiths [160Carlson K.J. et al.The endocast of MH1, Australopithecus sediba.Science. 2011; 333: 1402-1407Crossref PubMed Scopus (34) Google Scholar]. Au. sediba's virtual endocast hints toward reorganization of the frontal lobe (see also [7Holloway R.L. et al.The Human Fossil Record, Brain Endocasts: The Paleoneurological Evidence. John Wiley & Sons, 2004Crossref Google Scholar]). As another example, Homo neanderthalensis (Neanderthals) had a brain slightly larger than contemporary humans but similar in size to early modern humans [154Lieberman D.E. The Evolution of the Human Head. Harvard University Press, 2011Google Scholar, 161Ruff C.B. et al.Body mass and encephalization in Pleistocene Homo.Nature. 1997; 387: 173-176Crossref PubMed Scopus (303) Google Scholar]. Neanderthals mastered sophisticated technologies, but whatever neurological differences there were between Neanderthals and modern humans, absolute brain size was not likely to have been a significant contributor. Furthermore, modern brain size evolved long before the Upper Paleolithic and many traces of modern, symbolic behavior such as cave paintings, figurines, and personal ornamentation [162Klein R.G. Archeology and the evolution of human behavior.Evol. Anthropol. 2000; 9: 17-36Crossref Google Scholar]. Hominin brain capacity may have achieved its full functional advantage only with the amplifying effects of accumulated knowledge – sometimes referred to as the ‘cultural ratchet’ [121Tennie C. et al.Ratcheting up the ratchet: on the evolution of cumulative culture.Philos. Trans. R. Soc. B: Biol. Sci. 2009; 364: 2405-2415Crossref PubMed Scopus (100) Google Scholar, 122Boyd R. et al.The cultural niche: why social learning is essential for human adaptation.Proc. Natl. Acad. Sci. U.S.A. 2011; 108: 10918-10925Crossref PubMed Scopus (40) Google Scholar]. Mosaic evolutionary events that reorganized the brain and cultural innovations probably played important roles in hominin advancement.The recently extinct hominin species H. floresiensis provides a striking counterexample to a simplistic model that brain size alone determines capabilities [163Brown P. et al.A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia.Nature. 2004; 431: 1055-1061Crossref PubMed Scopus (280) Google Scholar, 164Morwood M.J. et al.Archaeology and age of a new hominin from Flores in eastern Indonesia.Nature. 2004; 431: 1087-1091Crossref PubMed Scopus (162) Google Scholar]. Living within the past 100,000 years, H. floresiensis stood 3 feet tall with a cranial capacity similar to that of a chimpanzee [165Kubo D. et al.Brain size of Homo floresiensis and its evolutionary implications.Proc. Biol. Sci. 2013; https://doi.org/10.1098/rspb.2013.0338Crossref PubMed Scopus (1) Google Scholar]. Although debate persists regarding H. floresiensis's origins, it seems likely that the species experienced some degree of brain size reduction through insular dwarfism from a larger-brained ancestor that was Homo erectus (or possibly Homo habilis) [166Lieberman D.E. Palaeoanthropology: Homo floresiensis from head to toe.Nature. 2009; 459: 41-42Crossref PubMed Scopus (6) Google Scholar]. Certain archeological discoveries suggest that H. floresiensis may have used sophisticated stone tools requiring multistage construction and hunted juvenile dwarfed elephants [164Morwood M.J. et al.Archaeology and age of a new hominin from Flores in eastern Indonesia.Nature. 2004; 431: 1087-1091Crossref PubMed Scopus (162) Google Scholar]. The exact level of stone tool technology mastered by H. floresiensis is a matter of ongoing debate. A reasonable hypothesis is that brain size reduction did come with a cognitive cost, but evidence that H. floresiensis was able to construct and use sophisticated tool technologies with a brain size comparable to a small Australopithecus emphasizes that the other stuff acquired during hominin evolution beyond brain size scaling is functionally significant.The focus of this review on critical implications of brain scaling should not be taken to imply brain scaling alone accounts for hominin evolution. The hominin brain grew rapidly over the past 3 million years in a primate lineage that had already experienced multiple events that increased brain size (Figure I depicts hominin brain evolution estimated from fossil endocasts, with labels for representative individuals from major species). The most significant determinant of our large brain size is that we are large animals: absolute brain size scales allometrically with body size [148Jerison H.J. Brain to body ratios and the evolution of intelligence.Science. 1955; 121: 447-449Crossref PubMed Google Scholar]. After factoring out body weight, which accounts for as much as 85% of the total variance in brain size across mammalian species, the human brain is about five times larger than one would expect for a typical mammal [149Jerison H.J. Evolution of the brain and intelligence.Curr. Anthropol. 1975; 16: 403-426Crossref Google Scholar, 150Marino L. A comparison of encephalization between odontocete cetaceans and anthropoid primates.Brain Behav. Evol. 1998; 51: 230-238Crossref PubMed Google Scholar]. Primates generally have disproportionately larger brains for their body size than other mammals (quantified as the encephalization quotient). This relative size difference is present at early embryonic stages, suggesting an ancient evolutionary event that shifted a greater proportion of the embryonic precursor cells to commit to a neuronal lineage ([151Count E.W. Brain and body weight in man: their antecedents in growth and evolution: a study in dynamic somatometry.Ann. N. Y. Acad. Sci. 1947; 46: 993-1122Crossref Google Scholar], data interpreted in [152Striedter G.F. Principles of Brain Evolution. Sinauer Associates, 2005Google Scholar]; see also [153Charvet C.J. Finlay B.L. Embracing covariation in brain evolution: large brains, extended development, and flexible primate social systems.Prog. Brain Res. 2012; 195: 71-87Crossref PubMed Scopus (6) Google Scholar]). Differences across primate suborders hint at other major evolutionary events including a step increase in brain size in monkeys (e.g., macaque and squirrel monkey) relative to prosimians (e.g., lemur). The acceleration over the past several million years probably derives from a distinct mechanism. Chimpanzees and humans have roughly the same body size and share a common ancestor about 5–7 million years ago. The early phases of brain development for chimpanzees and humans are conserved, with a similar proportion of the total body size devoted to the brain. At late phases, the brain continues to grow relative to the body in humans but stops earlier in chimpanzees, leading to a relative brain size expansion [152Striedter G.F. Principles of Brain Evolution. Sinauer Associates, 2005Google Scholar] (see also [154Lieberman D.E. The Evolution of the Human Head. Harvard University Press, 2011Google Scholar, 155Sakai T. et al.Fetal brain development in chimpanzees versus humans.Curr. Biol. 2012; 22: R791-R792Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar]). An interesting feature of brain scaling is that brain enlargement disproportionately expands some brain structures more than others. The cerebral cortex in mammals has the most privileged position in brain growth. A key contributor to disproportionate cortical expansion is constraints from embryonic development [135Finlay B.L. Darlington R.B. Linked regularities in the development and evolution of mammalian brains.Science. 1995; 268: 1578-1584Crossref PubMed Google Scholar]. Cerebral cortex progenitor cells are the last to be born among different neuronal pools. Because embryonic development is temporally stretched in large-brained mammals, the cerebral progenitor pool continues to divide for the longest period and forms the largest cell pool. This ‘late equals large’ developmental feature causes the cerebrum to have the greatest relative size increase. The cerebral surface area is ∼120 cm2 in the macaque and a remarkable ∼960 cm2 in the highly gyrified human brain [25Van Essen D.C. Dierker D.L. Surface-based and probabilistic atlases of primate cerebral cortex.Neuron. 2007; 56: 209-225Abstract Full Text Full Text PDF PubMed Google Scholar] (see also [156Rilling J.K. Insel T.R. The primate neocortex in comparative perspective using magnetic resonance imaging.J. Hum. Evol. 1999; 37: 191-223Crossref PubMed Scopus (161) Google Scholar]). The central point of this review is that brain size scaling may have essential, underexplored implications for large-scale circuit organization. However, it is also important to note observations that make clear how brain scaling is not the only factor at work in the evolution of hominin capabilities. For example, a marked increase in brain size was not the initial gateway to stone tool use. The oldest documented stone tools are 2.6 million years old [157Semaw S. et al.2.6-Million-year-old stone tools and associated bones from OGS-6 and OGS-7, Gona, Afar, Ethiopia.J. Hum. Evol. 2003; 45: 169-177Crossref PubMed Scopus (118) Google Scholar] and were made by hominins with moderate encephalization, possibly australopiths. Stone-cut marks are claimed by some to have been made as early as 3.4 million years ago [158McPherron S.P. et al.Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia.Nature. 2010; 466: 857-860Crossref PubMed Scopus (79) Google Scholar]. Living 2.0 million years ago, Australopithecus sediba possessed hand features suggesting stone tool use [159Kivell T.L. et al.Australopithecus sediba hand demonstrates mosaic evolution of locomotor and manipulative abilities.Science. 2011; 333: 1411-1417Crossref PubMed Scopus (41) Google Scholar], but had a brain size small even for australopiths [160Carlson K.J. et al.The endocast of MH1, Australopithecus sediba.Science. 2011; 333: 1402-1407Crossref PubMed Scopus (34) Google Scholar]. Au. sediba's virtual endocast hints toward reorganization of the frontal lobe (see also [7Holloway R.L. et al.The Human Fossil Record, Brain Endocasts: The Paleoneurological Evidence. John Wiley & Sons, 2004Crossref Google Scholar]). As another example, Homo neanderthalensis (Neanderthals) had a brain slightly larger than contemporary humans but similar in size to early modern humans [154Lieberman D.E. The Evolution of the Human Head. Harvard University Press, 2011Google Scholar, 161Ruff C.B. et al.Body mass and encephalization in Pleistocene Homo.Nature. 1997; 387: 173-176Crossref PubMed Scopus (303) Google Scholar]. Neanderthals mastered sophisticated technologies, but whatever neurological differences there were between Neanderthals and modern humans, absolute brain size was not likely to have been a significant contributor. Furthermore, modern brain size evolved long before the Upper Paleolithic and many traces of modern, symbolic behavior such as cave paintings, figurines, and personal ornamentation [162Klein R.G. Archeology and the evolution of human behavior.Evol. Anthropol. 2000; 9: 17-36Crossref Google Scholar]. Hominin brain capacity may have achieved its full functional advantage only with the amplifying effects of accumulated knowledge – sometimes referred to as the ‘cultural ratchet’ [121Tennie C. et al.Ratcheting up the ratchet: on the evolution of cumulative culture.Philos. Trans. R. Soc. B: Biol. Sci. 2009; 364: 2405-2415Crossref PubMed Scopus (100) Google Scholar, 122Boyd R. et al.The cultural niche: why social learning is essential for human adaptation.Proc. Natl. Acad. Sci. U.S.A. 2011; 108: 10918-10925Crossref PubMed Scopus (40) Google Scholar]. Mosaic evolutionary events that reorganized the brain and cultural innovations probably played important roles in hominin advancement. The recently extinct hominin species H. floresiensis provides a striking counterexample to a simplistic model that brain size alone determines capabilities [163Brown P. et al.A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia.Nature. 2004; 431: 1055-1061Crossref PubMed Scopus (280) Google Scholar, 164Morwood M.J. et al.Archaeology and age of a new hominin from Flores in eastern Indonesia.Nature. 2004; 431: 1087-1091Crossref PubMed Scopus (162) Google Scholar]. Living within the past 100,000 years, H. floresiensis stood 3 feet tall with a cranial capacity similar to that of a chimpanzee [165Kubo D. et al.Brain size of Homo floresiensis and its evolutionary implications.Proc. Biol. Sci. 2013; https://doi.org/10.1098/rspb.2013.0338Crossref PubMed Scopus (1) Google Scholar]. Although debate persists regarding H. floresiensis's origins, it seems likely that the species experienced some degree of brain size reduction through insular dwarfism from a larger-brained ancestor that was Homo erectus (or possibly Homo habilis) [166Lieberman D.E. Palaeoanthropology: Homo floresiensis from head to toe.Nature. 2009; 459: 41-42Crossref PubMed Scopus (6) Google Scholar]. Certain archeological discoveries suggest that H. floresiensis may have used sophisticated stone tools requiring multistage construction and hunted juvenile dwarfed elephants [164Morwood M.J. et al.Archaeology and age of a new hominin from Flores in eastern Indonesia.Nature. 2004; 431: 1087-1091Crossref PubMed Scopus (162) Google Scholar]. The exact level of stone tool technology mastered by H. floresiensis is a matter of ongoing debate. A reasonable hypothesis is that brain size reduction did come with a cognitive cost, but evidence that H. floresiensis was able to construct and use sophisticated tool technologies with a brain size comparable to a small Australopithecus emphasizes that the other stuff acquired during hominin evolution beyond brain size scaling is functionally significant. The focus of this review on critical implications of brain scaling should not be taken to imply brain scaling alone accounts for hominin evolution. How might a large brain enable complex cognitive functions? One possibility is that the human brain possesses more computational capacity because it has a large number of neurons – estimated at 86 billion neurons using modern cell-counting techniques [17Herculano-Houzel S. The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost.Proc. Natl. Acad. Sci. U.S.A. 2012; 109: 10661-10668Crossref PubMed Scopus (17) Google Scholar]. Other large-brained mammals, such as whales and elephants, radiate from ancestors that had reduced neuronal densities. The sparser neuronal matrix of a whale brain is expected to have fewer neurons than that of a chimpanzee although it is more than double the size of a human brain [17Herculano-Houzel S. The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost.Proc. Natl. Acad. Sci. U.S.A. 2012; 109: 10661-10668Crossref PubMed Scopus (17) Google Scholar]. Neuronal number and the connectional properties that go along with differences in neuronal density [18Changizi M.A. Scaling the brain and its connections.in: Kaas J. Evolution of Nervous Systems. Elsevier, 2007: 167-180Crossref Scopus (6) Google Scholar] are likely to explain much about human cognitive capabilities. However, what has captured our interest is a peculiar feature of brain scaling that might prove critical. The feature concerns how brain scaling shifts the predominant circuit organization from one primarily linked to sensory–motor hierarchies to a noncanonical form vital to human thought. The emergent circuit organization may be a side effect, perhaps even to be considered a spandrel [19Gould S.J. Lewontin R.C. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme.Proc. R. Soc. B: Biol. Sci. 1979; 205: 581-598Crossref PubMed Google Scholar], of developmental rules and an organization inherited from our simpler mammalian ancestors but now expressed in a massively scaled cerebral cortex. The rapid expansion of the cortical mantle may have untethered large portions of the cortex from strong constraints of molecular gradients and early activity cascades that lead to local sensory hierarchies. What fill the gaps between these hierarchies are distributed, interconnected association networks that widely span the cortex, develop late, and are preferentially more dependent on protracted activity-dependent influences. A striking feature of the human cerebral cortex is that it follows an ancient mammalian prototype but also displays relative enlargement of regions distributed throughout association cortex (Figure 1). The proportion of cortical surface occupied by sensory and motor areas decreases as the overall size of the cortex expands [20Diamond I.T. Hall W.C. Evolution of neocortex.Science. 1969; 164: 251-262Crossref PubMed Google Scholar]. This observation can be made in several ways. Certain cortical areas (Box 3) are conserved across mammals, suggesting that they were present in an ancient mammalian ancestor (e.g., primary visual cortex [V1] [21Kaas J.H. The organization of neocortex in mammals: implications for theories
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