Brain Plasticity and Human Evolution

Human behavior is shaped by social learning to an extent that is unrivaled in the natural world. What neurobiological changes have occurred in human evolutionary history that have enabled this remarkable cultural capacity? Human brain anatomy and function have evolved to be highly responsive to experience from the environment, especially the milieu of social interactions. Numerous aspects of human brain development show evidence of specialization leading to increased plasticity. These include the timing of brain growth relative to birth, rates of synaptogenesis and myelination, and shifts in gene expression and epigenetic modifications. Some of these evolutionary changes in human brain plasticity are also evident in fossil hominins and from analyses of ancient DNA.

[1]  Margaret A. Sheridan,et al.  Neglect as a Violation of Species-Expectant Experience: Neurodevelopmental Consequences , 2017, Biological Psychiatry.

[2]  C. Sherwood,et al.  Human brain evolution , 2017, Current Opinion in Behavioral Sciences.

[3]  A. Gómez‐Robles,et al.  Exceptional Evolutionary Expansion of Prefrontal Cortex in Great Apes and Humans , 2017, Current Biology.

[4]  A. Halley Minimal variation in eutherian brain growth rates during fetal neurogenesis , 2017, Proceedings of the Royal Society B: Biological Sciences.

[5]  R. Gur,et al.  Patterns of coordinated cortical remodeling during adolescence and their associations with functional specialization and evolutionary expansion , 2017, Proceedings of the National Academy of Sciences.

[6]  Chet C. Sherwood,et al.  Exceptional Evolutionary Expansion of Prefrontal Cortex in Great Apes and Humans , 2017, Current Biology.

[7]  William D Hopkins,et al.  The heritability of chimpanzee and human brain asymmetry , 2016, Proceedings of the Royal Society B: Biological Sciences.

[8]  M. Robbins,et al.  Behavioral Variation in Gorillas: Evidence of Potential Cultural Traits , 2016, PloS one.

[9]  P. Hof,et al.  Combining diffusion magnetic resonance tractography with stereology highlights increased cross‐cortical integration in primates , 2016, The Journal of comparative neurology.

[10]  S. Pääbo,et al.  Disruption of an Evolutionarily Novel Synaptic Expression Pattern in Autism , 2016, PLoS biology.

[11]  Todd M. Preuss,et al.  Comparative Methylome Analyses Identify Epigenetic Regulatory Loci of Human Brain Evolution , 2016, Molecular biology and evolution.

[12]  C. Zollikofer,et al.  Brain development is similar in Neanderthals and modern humans , 2016, Current Biology.

[13]  S. Suomi,et al.  Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys , 2016, Nature Communications.

[14]  B. Hare,et al.  Metabolic acceleration and the evolution of human brain size and life history , 2016, Nature.

[15]  Janet Kelso,et al.  Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins , 2016, Nature.

[16]  Michael L Platt,et al.  Adaptations for social cognition in the primate brain , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  R. Douglas Fields,et al.  A new mechanism of nervous system plasticity: activity-dependent myelination , 2015, Nature Reviews Neuroscience.

[18]  C. Sherwood,et al.  Relaxed genetic control of cortical organization in human brains compared with chimpanzees , 2015, Proceedings of the National Academy of Sciences.

[19]  S. Sawyer,et al.  Nuclear and mitochondrial DNA sequences from two Denisovan individuals , 2015, Proceedings of the National Academy of Sciences.

[20]  Shihui Han,et al.  A Culture–Behavior–Brain Loop Model of Human Development , 2015, Trends in Cognitive Sciences.

[21]  Michelle L. Reyzer,et al.  High spatial resolution proteomic comparison of the brain in humans and chimpanzees , 2015, The Journal of comparative neurology.

[22]  Alan C. Evans,et al.  Changes in thickness and surface area of the human cortex and their relationship with intelligence. , 2015, Cerebral cortex.

[23]  P. Hof,et al.  Analysis of synaptic gene expression in the neocortex of primates reveals evolutionary changes in glutamatergic neurotransmission. , 2015, Cerebral cortex.

[24]  H. Roche,et al.  3.3-million-year-old stone tools from Lomekwi 3, West Turkana, Kenya , 2015, Nature.

[25]  J. DeSilva,et al.  A neonatal perspective on Homo erectus brain growth. , 2015, Journal of human evolution.

[26]  Christopher J. Campisano,et al.  Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia , 2015, Science.

[27]  P. Gunz,et al.  Brain ontogeny and life history in Pleistocene hominins , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  Erin E. Hecht,et al.  Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans , 2015, NeuroImage.

[29]  Barbara L. Finlay,et al.  Developmental mechanisms channeling cortical evolution , 2015, Trends in Neurosciences.

[30]  H. D. Steklis,et al.  Personality dimensions and their behavioral correlates in wild Virunga mountain gorillas (Gorilla beringei beringei). , 2015, Journal of comparative psychology.

[31]  Peter Richerson,et al.  Cultural group selection plays an essential role in explaining human cooperation: A sketch of the evidence , 2014, Behavioral and Brain Sciences.

[32]  Richard E. Passingham,et al.  Is the Prefrontal Cortex Especially Enlarged in the Human Brain? Allometric Relations and Remapping Factors , 2014, Brain, Behavior and Evolution.

[33]  Judith M Burkart,et al.  The evolutionary origin of human hyper-cooperation , 2014, Nature Communications.

[34]  P. Hof,et al.  Metabolic costs and evolutionary implications of human brain development , 2014, Proceedings of the National Academy of Sciences.

[35]  L. Orlando,et al.  An epigenetic window into the past? , 2014, Science.

[36]  William D. Hopkins,et al.  Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans , 2014, Nature Communications.

[37]  S. Pääbo,et al.  Reconstructing the DNA Methylation Maps of the Neandertal and the Denisovan , 2014, Science.

[38]  C. V. van Schaik,et al.  How humans evolved large brains: Comparative evidence , 2014, Evolutionary anthropology.

[39]  Philip L. F. Johnson,et al.  The complete genome sequence of a Neandertal from the Altai Mountains , 2013, Nature.

[40]  E. Birney,et al.  Archaic humans: Four makes a party , 2013, Nature.

[41]  Qiaomei Fu,et al.  A mitochondrial genome sequence of a hominin from Sima de los Huesos , 2013, Nature.

[42]  Randy L. Buckner,et al.  The evolution of distributed association networks in the human brain , 2013, Trends in Cognitive Sciences.

[43]  L. Stefanacci,et al.  Evolution, development, and plasticity of the human brain: from molecules to bones , 2013, Front. Hum. Neurosci..

[44]  A. Gnirke,et al.  Charting a dynamic DNA methylation landscape of the human genome , 2013, Nature.

[45]  J. DeSilva,et al.  Mojokerto revisited: evidence for an intermediate pattern of brain growth in Homo erectus. , 2013, Journal of human evolution.

[46]  C. Sherwood,et al.  Increased morphological asymmetry, evolvability and plasticity in human brain evolution , 2013, Proceedings of the Royal Society B: Biological Sciences.

[47]  P. Hof,et al.  Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans , 2013, Proceedings of the National Academy of Sciences.

[48]  Chris Venditti,et al.  Human frontal lobes are not relatively large , 2013, Proceedings of the National Academy of Sciences.

[49]  P. Hof,et al.  Early Brain Growth Cessation in Wild Virunga Mountain Gorillas (Gorilla beringei beringei) , 2013, American journal of primatology.

[50]  B. Finlay,et al.  Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species , 2013, The Journal of Neuroscience.

[51]  H. Burbano,et al.  A recent evolutionary change affects a regulatory element in the human FOXP2 gene. , 2013, Molecular biology and evolution.

[52]  Karl Zilles,et al.  A volumetric comparison of the insular cortex and its subregions in primates. , 2013, Journal of human evolution.

[53]  A. Mikami,et al.  Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain , 2013, Proceedings of the Royal Society B: Biological Sciences.

[54]  P. Khaitovich,et al.  Human brain evolution: transcripts, metabolites and their regulators , 2013, Nature Reviews Neuroscience.

[55]  C. V. van Schaik,et al.  How to explain the unusually late age at skill competence among humans. , 2012, Journal of human evolution.

[56]  J. Sikela,et al.  Evolution of genetic and genomic features unique to the human lineage , 2012, Nature Reviews Genetics.

[57]  Adrian W. Briggs,et al.  A High-Coverage Genome Sequence from an Archaic Denisovan Individual , 2012, Science.

[58]  J. Call,et al.  The evolution of primate societies , 2012 .

[59]  Daniel J. Miller,et al.  Prolonged myelination in human neocortical evolution , 2012, Proceedings of the National Academy of Sciences.

[60]  D. Geschwind,et al.  Divergent whole-genome methylation maps of human and chimpanzee brains reveal epigenetic basis of human regulatory evolution. , 2012, American journal of human genetics.

[61]  T. Deacon,et al.  Metabolic hypothesis for human altriciality , 2012, Proceedings of the National Academy of Sciences.

[62]  S. Herculano‐Houzel The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost , 2012, Proceedings of the National Academy of Sciences.

[63]  P. Hof,et al.  Dynamic Gene Expression in the Human Cerebral Cortex Distinguishes Children from Adults , 2012, PloS one.

[64]  Peter A. Jones Functions of DNA methylation: islands, start sites, gene bodies and beyond , 2012, Nature Reviews Genetics.

[65]  Peter H. Sudmant,et al.  Evolution of Human-Specific Neural SRGAP2 Genes by Incomplete Segmental Duplication , 2012, Cell.

[66]  Anirvan Ghosh,et al.  Inhibition of SRGAP2 Function by Its Human-Specific Paralogs Induces Neoteny during Spine Maturation , 2012, Cell.

[67]  S. Pääbo,et al.  Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. , 2012, Genome research.

[68]  P. Gunz,et al.  A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya. , 2012, Journal of human evolution.

[69]  R. Blesa,et al.  Human neoteny revisited: The case of synaptic plasticity , 2011, American journal of human biology : the official journal of the Human Biology Council.

[70]  Jamie L. Russell,et al.  The role of socio-communicative rearing environments in the development of social and physical cognition in apes. , 2011, Developmental science.

[71]  B. Hare,et al.  From Hominoid to Hominid Mind: What Changed and Why?* , 2011 .

[72]  José Manuel de la Cuétara,et al.  A Bivariate Approach to the Variation of the Parietal Curvature in the Genus Homo , 2011, Anatomical record.

[73]  John S. Allen,et al.  Aging of the cerebral cortex differs between humans and chimpanzees , 2011, Proceedings of the National Academy of Sciences.

[74]  G. Šimić,et al.  Extraordinary neoteny of synaptic spines in the human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[75]  J. Henrich,et al.  The cultural niche: Why social learning is essential for human adaptation , 2011, Proceedings of the National Academy of Sciences.

[76]  W. Enard FOXP2 and the role of cortico-basal ganglia circuits in speech and language evolution , 2011, Current Opinion in Neurobiology.

[77]  T. Preuss The human brain: rewired and running hot , 2011, Annals of the New York Academy of Sciences.

[78]  S. Pääbo,et al.  Rapid metabolic evolution in human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[79]  J. DeSilva A shift toward birthing relatively large infants early in human evolution , 2011, Proceedings of the National Academy of Sciences.

[80]  Philip L. F. Johnson,et al.  Genetic history of an archaic hominin group from Denisova Cave in Siberia , 2010, Nature.

[81]  Tanya M. Smith,et al.  Dental evidence for ontogenetic differences between modern humans and Neanderthals , 2010, Proceedings of the National Academy of Sciences.

[82]  P. Gunz,et al.  Brain development after birth differs between Neanderthals and modern humans , 2010, Current Biology.

[83]  Peter H. Sudmant,et al.  Diversity of Human Copy Number Variation and Multicopy Genes , 2010, Science.

[84]  John W. Harwell,et al.  Similar patterns of cortical expansion during human development and evolution , 2010, Proceedings of the National Academy of Sciences.

[85]  G. Sapiro,et al.  The development of gyrification in childhood and adolescence , 2010, Brain and Cognition.

[86]  Jörn Diedrichsen,et al.  Evolution of the cerebellar cortex: The selective expansion of prefrontal-projecting cerebellar lobules , 2010, NeuroImage.

[87]  Terrence S. Furey,et al.  Both Noncoding and Protein-Coding RNAs Contribute to Gene Expression Evolution in the Primate Brain , 2010, Genome biology and evolution.

[88]  C. V. van Schaik,et al.  The Expensive Brain: a framework for explaining evolutionary changes in brain size. , 2009, Journal of human evolution.

[89]  Evan E. Eichler,et al.  Sequencing primate genomes: what have we learned? , 2009, Annual review of genomics and human genetics.

[90]  Johannes Schwarz,et al.  A Humanized Version of Foxp2 Affects Cortico-Basal Ganglia Circuits in Mice , 2009, Cell.

[91]  B. Nickel,et al.  Transcriptional neoteny in the human brain , 2009, Proceedings of the National Academy of Sciences.

[92]  Constance Scharff,et al.  FOXP2 as a molecular window into speech and language. , 2009, Trends in genetics : TIG.

[93]  Nitzan Mekel-Bobrov,et al.  Genetic basis of human brain evolution , 2008, Trends in Neurosciences.

[94]  Chet C. Sherwood,et al.  Cortical development in brown capuchin monkeys: A structural MRI study , 2008, NeuroImage.

[95]  F. Lazeyras,et al.  Mapping the early cortical folding process in the preterm newborn brain. , 2008, Cerebral cortex.

[96]  Timothy E. J. Behrens,et al.  The evolution of the arcuate fasciculus revealed with comparative DTI , 2008, Nature Neuroscience.

[97]  C. Sherwood,et al.  A natural history of the human mind: tracing evolutionary changes in brain and cognition , 2008, Journal of anatomy.

[98]  H. Burbano,et al.  The Derived FOXP2 Variant of Modern Humans Was Shared with Neandertals , 2007, Current Biology.

[99]  M. Cáceres,et al.  Increased cortical expression of two synaptogenic thrombospondins in human brain evolution. , 2007, Cerebral cortex.

[100]  S. Dongen,et al.  Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future , 2006, Journal of evolutionary biology.

[101]  P. Schoenemann Evolution of the Size and Functional Areas of the Human Brain , 2006 .

[102]  B. Bogin,et al.  Language and life history: a new perspective on the development and evolution of human language. , 2006, The Behavioral and brain sciences.

[103]  J. de Vos,et al.  Relocation of the 1936 Mojokerto skull discovery site near Perning, East Java. , 2006, Journal of human evolution.

[104]  Mijna Hadders-Algra,et al.  Ontogeny of the human central nervous system: what is happening when? , 2006, Early human development.

[105]  Alan C. Evans,et al.  Intellectual ability and cortical development in children and adolescents , 2006, Nature.

[106]  J. Rilling Human and nonhuman primate brains: Are they allometrically scaled versions of the same design? , 2006 .

[107]  W. Kimbel The Human Fossil Record, Vol. 3. Brain Endocasts: The Paleoneurological Evidence. Ralph L. Holloway , Douglas C. Broadfield , Michael S. Yuan , Jeffrey H. Schwartz , Ian Tattersall , 2005 .

[108]  S. Pääbo,et al.  Parallel Patterns of Evolution in the Genomes and Transcriptomes of Humans and Chimpanzees , 2005, Science.

[109]  Bob Jacobs,et al.  Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study , 2005, Developmental Neuroscience.

[110]  Massimo Pigliucci,et al.  Evolution of phenotypic plasticity: where are we going now? , 2005, Trends in ecology & evolution.

[111]  P. Schoenemann,et al.  Prefrontal white matter volume is disproportionately larger in humans than in other primates , 2005, Nature Neuroscience.

[112]  Susan Bowsfield The Symbolic Species: The Co-Evolution of Language and the Brain , 2004 .

[113]  D. Geschwind,et al.  Human brain evolution: insights from microarrays , 2004, Nature Reviews Genetics.

[114]  J. Hublin,et al.  Early brain growth in Homo erectus and implications for cognitive ability , 2004, Nature.

[115]  Ralph L. Holloway,et al.  The Human Fossil Record , 2004 .

[116]  Wenbo Xu,et al.  Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[117]  Matthew A. Zapala,et al.  Elevated gene expression levels distinguish human from non-human primate brains , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[118]  P. Levitt Structural and functional maturation of the developing primate brain. , 2003, The Journal of pediatrics.

[119]  K. Hawkes,et al.  Grandmothers and the evolution of human longevity , 2003, American journal of human biology : the official journal of the Human Biology Council.

[120]  L. Lossi,et al.  In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS , 2003, Progress in Neurobiology.

[121]  Michelle Y. Merrill,et al.  Orangutan Cultures and the Evolution of Material Culture , 2003, Science.

[122]  P. O’Sullivan,et al.  Revised age for Mojokerto 1, an early Homo erectus cranium from East Java, Indonesia , 2003 .

[123]  S. Antón Evolutionary significance of cranial variation in Asian Homo erectus. , 2002, American journal of physical anthropology.

[124]  Adoum H. Mahamat,et al.  A new hominid from the Upper Miocene of Chad, Central Africa , 2002, Nature.

[125]  James K Rilling,et al.  A quantitative morphometric comparative analysis of the primate temporal lobe. , 2002, Journal of human evolution.

[126]  Milos Judas,et al.  Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. , 2002, Cerebral cortex.

[127]  H. Damasio,et al.  Humans and great apes share a large frontal cortex , 2002, Nature Neuroscience.

[128]  J. Stevenson The cultural origins of human cognition , 2001 .

[129]  Christopher S. Monk,et al.  Mechanisms of Postnatal Neurobiological Development: Implications for Human Development , 2001, Developmental neuropsychology.

[130]  Y. Coppens,et al.  First hominid from the Miocene (Lukeino Formation, Kenya) , 2001 .

[131]  A. Whiten,et al.  Cultures in chimpanzees , 1999, Nature.

[132]  R. Kikinis,et al.  Quantitative magnetic resonance imaging of brain development in premature and mature newborns , 1998, Annals of neurology.

[133]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[134]  S. Antón,et al.  Developmental age and taxonomic affinity of the Mojokerto child, Java, Indonesia. , 1997, American journal of physical anthropology.

[135]  L. Aiello,et al.  The Expensive-Tissue Hypothesis: The Brain and the Digestive System in Human and Primate Evolution , 1995, Current Anthropology.

[136]  C. Swisher,et al.  Age of the earliest known hominids in Java, Indonesia. , 1994, Science.

[137]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[138]  H. Loos,et al.  Synaptogenesis in human visual cortex — evidence for synapse elimination during normal development , 1982, Neuroscience Letters.

[139]  S. Gould,et al.  Ontogeny and Phylogeny , 1978 .

[140]  G. Sacher,et al.  Relation of Gestation Time to Brain Weight for Placental Mammals: Implications for the Theory of Vertebrate Growth , 1974, The American Naturalist.

[141]  R. Holloway, The evolution of the primate brain: some aspects of quantitative relations. , 1968, Brain research.

[142]  C. Sherwood,et al.  The evolution of human altriciality and brain plasticity in comparative context , 2017 .

[143]  Lennart Verhagen,et al.  Evolutionary specializations of human association cortex , 2017 .

[144]  Kerstin M. Mueller Neural Darwinism The Theory Of Neuronal Group Selection , 2016 .

[145]  A. Lundervold,et al.  High-expanding cortical regions in human development and evolution are related to higher intellectual abilities. , 2015, Cerebral cortex.

[146]  Julius Maximilian Epigenetic Information from Ancient DNA Provides New Insights into Human Evolution , 2014 .

[147]  R. Blesa,et al.  Alzheimer's disease: an evolutionary approach. , 2013, Journal of anthropological sciences = Rivista di antropologia : JASS.

[148]  K. Semendeferi,et al.  Human prefrontal cortex: evolution, development, and pathology. , 2012, Progress in brain research.

[149]  B. Peterson,et al.  Normal Development of Brain Circuits , 2010, Neuropsychopharmacology.

[150]  J. Rilling,et al.  Neuroscientific approaches and applications within anthropology. , 2008, American journal of physical anthropology.

[151]  S. Leigh Brain ontogeny and life history in Homo erectus. , 2006, Journal of human evolution.

[152]  J. Kaas,et al.  Specializations of the granular prefrontal cortex of primates: implications for cognitive processing. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[153]  J. Adams Nuclear and Mitochondrial DNA in the Courtroom , 2005 .

[154]  S. Antón Natural history of Homo erectus. , 2003, American journal of physical anthropology.

[155]  Tim D. White,et al.  Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia , 1995, Nature.

[156]  M. L. Robertson,et al.  Evolutionary perspectives on human nutrition: The influence of brain and body size on diet and metabolism , 1994, American journal of human biology : the official journal of the Human Biology Council.

[157]  Karen R. Rosenberg,et al.  The evolution of modern human childbirth , 1992 .