Skip to main content

Advertisement

Log in

Cultural Exaptation and Cultural Neural Reuse: A Mechanism for the Emergence of Modern Culture and Behavior

  • Original Article
  • Published:
Biological Theory Aims and scope Submit manuscript

Abstract

On the basis of recent advancements in both neuroscience and archaeology, we propose a plausible biocultural mechanism at the basis of cultural evolution. The proposed mechanism, which relies on the notions of cultural exaptation and cultural neural reuse, may account for the asynchronous, discontinuous, and patchy emergence of innovations around the globe. Cultural exaptation refers to the reuse of previously devised cultural features for new purposes. Cultural neural reuse refers to cases in which exposure to cultural practices induces the formation, activation, and stabilization of new functional and/or structural brain networks during the individual lifespan. The invention of writing is interpreted as a case of cultural exaptation of previous devices to record information, in use since at least the Early Later Stone Age and the beginning of the Upper Paleolithic (44,000 years before present). The measurable changes in brain structure and functioning caused by learning to read are proposed as an exemplar case of cultural neural reuse. It is argued that repeated cycles of cultural exaptation, development of appropriate strategies of cultural transmission, and ensuing cultural neural reuse represent the fundamental mechanism that has regulated the cultural evolution of our lineage. A general predictive model of when and under which circumstances the proposed mechanism should be expected to occur is proposed, and the relationship of our mechanism with gene-culture coevolutionary models is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

(Modified after d’Errico 1995, 1998; d’Errico et al. 2012; d’Errico and Cacho 1994)

Fig. 2

Similar content being viewed by others

References

  • Amunts K, Lenzen M, Friederici AD et al (2010) Broca’s region: novel organizational principles and multiple receptor mapping. PLoS Biol 8:e1000489

    Google Scholar 

  • Anderson ML (2007) Massive redeployment, exaptation, and the functional integration of cognitive operations. Synthese 159:329–345

    Google Scholar 

  • Anderson ML (2010) Neural reuse: a fundamental organizational principle of the brain. Behav Brain Sci 33:245–313

    Google Scholar 

  • Anderson ML (2014) After phrenology: neural reuse and the interactive brain. MIT Press, Cambridge

    Google Scholar 

  • Baker CI, Liu J, Wald LI et al (2007) Visual word processing and experiential origins of functional selectivity in human extrastriate cortex. Proc Natl Acad Sci USA 104:9087–9092

    Google Scholar 

  • Barham L, Mitchell P (2008) The first Africans: African archaeology from the earliest toolmakers to most recent foragers. Cambridge University Press, Cambridge

    Google Scholar 

  • Bar-Yosef O (1998) On the nature of transitions: the Middle to Upper Palaeolithic and the Neolithic revolution. Camb Archaeol J 8:141–163

    Google Scholar 

  • Boyd R, Richerson PJ, Henrich J (2011) The cultural niche: why social learning is essential for human adaptation. Proc Natl Acad Sci USA 108:10918–10925

    Google Scholar 

  • Brem S, Bach S, Kucian K et al (2010) Brain sensitivity to print emerges when children learn letter-speech sound correspondences. Proc Natl Acad Sci USA 107:7939–7944

    Google Scholar 

  • Burdett ERR, Dean LG, Ronfard S (2017) A diverse and flexible teaching toolkit facilitates the human capacity for cumulative culture. Rev Philos Psychol. https://doi.org/10.1007/s13164-017-0345-4

    Article  Google Scholar 

  • Cantlon JF, Pinel P, Dehaene S, Pelphrey KA (2011) Cortical representations of symbols, objects, and faces are pruned back during early childhood. Cereb Cortex 21:191–199

    Google Scholar 

  • Carreiras M, Seghier ML, Baquero S et al (2009) An anatomical signature for literacy. Nature 461:983–986

    Google Scholar 

  • Caspers J, Zilles K, Eickhoff SB et al (2013) Cytoarchitectonical analysis and probabilistic mapping of two extrastriate areas of the human posterior fusiform gyrus. Brain Struct Funct 218:511–526

    Google Scholar 

  • Caspers J, Zilles K, Amunts K et al (2014) Functional characterization and differential coactivation patterns of two cytoarchitectonic visual areas on the human posterior fusiform gyrus. Hum Brain Mapp 35:2754–2767

    Google Scholar 

  • Cohen L, Dehaene S, Naccache L et al (2000) The visual word form area. Spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain 123:291–307

    Google Scholar 

  • Colagè I (2013) Human specificity: recent neuro-scientific advances and new perspectives. ESSSAT New Rev 23:5–19

    Google Scholar 

  • Colagè I (2015) The human being shaping and transcending itself: Written language, brain, and culture. Zygon 50:1002–1021

    Google Scholar 

  • Colagè I, D’Ambrosio P (2014) Exaptation and neural reuse: a research perspective into the human specificity. Antonianum 89:333–358

    Google Scholar 

  • Colagè I, d’Errico F (2018) Culture: the driving force of human cognition. Top Cognit Sci. https://doi.org/10.1111/tops.12372

    Article  Google Scholar 

  • Collard M, Vaesen K, Cosgrove R, Roebroeks W (2016) The empirical case against the ‘demographic turn’ in Palaeolithic archaeology. Phil Trans R Soc B 371:20150242

    Google Scholar 

  • Coltheart M, Rastle K (1994) Serial processing in reading aloud: evidence for dual route models of reading. J Exp Psychol 6:1197–1211

    Google Scholar 

  • D’Ambrosio P, Colagè I (2017) Extending epigenesis: from phenotypic plasticity to the bio-cultural feedback. Biol Philos 32:705–728

    Google Scholar 

  • d’Errico F (1993) La vie sociale de l’art mobilier paléolithique. Manipulation, transport, suspension des objets on os, bois de cervidés, ivoire. Oxf J Archaeol 12(2):145–174

    Google Scholar 

  • d’Errico F (1995) A new model and its implications for the origins of writing: the La Marche antler revisited. Camb Archaeol J 5:163–206

    Google Scholar 

  • d’Errico F (1998) Palaeolithic origins of artificial memory systems: an evolutionary perspective. In: Renfrew C, Scarre C C (ed) Cognition and material culture: the archaeology of symbolic storage. The McDonald Institute Monographs, Cambridge, pp 19–50

    Google Scholar 

  • d’Errico F (2002) Memories out of mind: the archaeology of the oldest artificial memory systems. In: Nowell A (ed) In the mind’s eye, International Monographs in Prehistory Archaeological Series, Ann Arbor, pp 33–49

    Google Scholar 

  • d’Errico F, Backwell L (2016) Earliest evidence of personal ornaments associated with burial: the Conus shells from Border Cave. J Hum Evol 93:91e108

    Google Scholar 

  • d’Errico F, Banks WE (2013) Identifying mechanisms behind Middle Paleolithic and Middle Stone Age cultural trajectories. Curr Anthropol 54:S371–S387

    Google Scholar 

  • d’Errico F, Banks WE (2015) The archaeology of teaching: a conceptual framework. Camb Archaeol J 25:859–866

    Google Scholar 

  • d’Errico F, Cacho C (1994) Notation versus decoration in the Upper Paleolithic: a case-study from Tossal de la Roca, Alicante, Spain. J Archaeol Sci 21:185–200

    Google Scholar 

  • d’Errico F, Stringer CB (2011) Evolution, revolution or saltation scenario for the emergence of modern cultures? Phil Trans R Soc B 366:1060–1069

    Google Scholar 

  • d’Errico F, Henshilwood C, Lawson G et al (2003) Archaeological evidence for the emergence of language, symbolism, and music—an alternative multidisciplinary perspective. J World Prehist 17:1–70

    Google Scholar 

  • d’Errico F, Vanhaeren M, Barton N et al (2009) Additional evidence on the use of personal ornaments in the Middle Paleolithic of North Africa. Proc Natl Acad Sci USA 106:16051–16056

    Google Scholar 

  • d’Errico F, Backwell L, Villa P et al (2012) Early evidence of San material culture represented by organic artifacts from Border Cave, South Africa. Proc Natl Acad Sci USA 109:13214–13219

    Google Scholar 

  • d’Errico F, Doyon L, Colagè I et al (2017) From number sense to number symbols. An archaeological perspective. Phil Trans R Soc B 373:20160518

    Google Scholar 

  • Dean LG, Kendal RL, Schapiro SJ et al (2012) Identification of the social and cognitive processes underlying human cumulative culture. Science 335:1114–1118

    Google Scholar 

  • Dehaene S, Cohen L (2007) Cultural recycling of cortical maps. Neuron 56:384–398

    Google Scholar 

  • Dehaene S, Cohen L (2011) The unique role of the visual word form area in reading. Trends Cogn Sci 15:254–262

    Google Scholar 

  • Dehaene S, Pegado F, Braga LW et al (2010) How learning to read changes the cortical networks for vision and language. Science 330:1359–1364

    Google Scholar 

  • Dehaene S, Cohen L, Morais J, Kolinsky R (2015) Illiterate to literate: Behavioural and cerebral changes induced by reading acquisition. Nat Rev Neurosci 16:234–244

    Google Scholar 

  • Dirks PH, Berger LR, Roberts EM et al (2015) Geological and taphonomic context for the new hominin species Homo naledi from the Dinaledi Chamber, South Africa. eLife 4:e09561

    Google Scholar 

  • Dirks PH, Roberts EM, Hilbert-Wolf H et al (2017) The age of Homo naledi and associated sediments in the Rising Star Cave, South Africa. eLife 6:e24231

    Google Scholar 

  • Donald M (1991) Origins of the modern mind: three stages in the evolution of culture and cognition. Harvard University Press, Cambridge

    Google Scholar 

  • Dor D, Jablonka E (2014) Why we need to move from gene-culture co-evolution to culturally-driven co-evolution. In: Dor D, Knight K, Lewis J (eds) Social origins of language. Oxford University Press, Oxford, pp 15–30

    Google Scholar 

  • Fu Q, Posth C, Hajdinjak M et al (2016) The genetic history of ice age Europe. Nature 534:200–205

    Google Scholar 

  • Gaillard R, Naccache L, Pinel P et al (2006) Direct intracranial, fMRI, and lesion evidence for the causal role of left inferotemporal cortex in reading. Neuron 50:191–204

    Google Scholar 

  • Gomez J, Barnett MA, Natu V et al (2017) Microstructural proliferation in human cortex is coupled with the development of face processing. Science 355:aag0311

    Google Scholar 

  • Goody J (1977) The domestication of the savage mind. Cambridge University Press, Cambridge

    Google Scholar 

  • Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of for. Paleobiology 8:4–15

    Google Scholar 

  • Hagmann P, Cammoun L, Gigandet X et al (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159

    Google Scholar 

  • Hammer M, Woerner AE, Mendez FL et al (2011) Genetic evidence for archaic admixture in Africa. Proc Natl Acad Sci USA 108:15123–15128

    Google Scholar 

  • Hannagan T, Amedi A, Cohen L et al (2015) Origins of the specialization for letters and numbers in ventral occipitotemporal cortex. Trends Cognit Sci 19:374–382

    Google Scholar 

  • Hashimoto R, Sakai KL (2004) Learning letters in adulthood: direct visualization of cortical plasticity for forming a new link between orthography and phonology. Neuron 42:311–322

    Google Scholar 

  • Hecht EE, Gutman DA, Khreisheh N et al (2014) Acquisition of paleolithic toolmaking abilities involves structural remodeling to inferior frontoparietal regions. Brain Struct Funct 220:2315–2331

    Google Scholar 

  • Henrich J (2004) Demography and cultural evolution: how adaptive cultural processes can produce maladaptive losses: the Tasmanian case. Am Antiq 69:197–214

    Google Scholar 

  • Heyes C (2012) Grist and mills: on the cultural origins of cultural learning. Phil Trans R Soc B 367(1599):2181–2191

    Google Scholar 

  • Heyes C (2017) When does social learning become cultural learning? Dev Sci. https://doi.org/10.1111/desc.12350

    Article  Google Scholar 

  • Heyes C (2018) Cognitive gadgets: the cultural evolution of thinking. Harvard University Press, Cambridge

    Google Scholar 

  • Hihara S, Notoya T, Tanaka M et al (2006) Extension of corticocortical afferents into the anterior bank of the intraparietal sulcus by tool-use training in adult monkeys. Neuropsychologia 44:2636–2646

    Google Scholar 

  • Hoffmann DL, Standish CD, García-Diez M et al (2018) U-Th dating of carbonate crusts reveals Neandertal origin of Iberian cave art. Science 359:912–915

    Google Scholar 

  • Högberg A, Gärdenfors P, Larsson L (2015) Knowing, learning and teaching—how Homo became docens. Camb Archaeol J 25:847–858

    Google Scholar 

  • Horwitz B, Tagamets MA, McIntosh AR (1999) Neural modeling, functional brain imaging, and cognition. Trends Cogn Sci 3:91–98

    Google Scholar 

  • Horwitz B, Friston KT, Taylor JC (2000) Neural modeling and functional brain imaging: an overview. Neural Netw 13:829–846

    Google Scholar 

  • Ishibashi H, Hihara S, Takahashi M et al (2002) Tool-use learning selectively induces expression of brain-derived neurotrophic factor, its receptor trkB, and neurotrophin 3 in the intraparietal multisensorycortex of monkeys. Cogn Brain Res 14:3–9

    Google Scholar 

  • Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge

    Google Scholar 

  • Jobard G, Crivello F, Tzourio-Mazoyer N (2003) Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. NeuroImage 20:693–712

    Google Scholar 

  • Johansson S (2014) The thinking Neanderthals: what do we know about Neanderthal cognition? Wiley Interdiscip Rev 5:613–20

    Google Scholar 

  • Joordens JCA, d’Errico F, Wesselingh FP et al (2015) Homo erectus at Trinil on Java used shells for tool production and engraving. Nature 518:228–231

    Google Scholar 

  • Klein RG (1989) The human career. University of Chicago Press, Chicago

    Google Scholar 

  • Klein RG (2000) Archeology and the evolution of human behavior. Evol Anthropol 9:17–36

    Google Scholar 

  • Klingberg T, Hedehus M, Temple E et al (2000) Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging. Neuron 25:493–500

    Google Scholar 

  • Kolodny O, Creanza N, Feldman MW (2015) Evolution in leaps: the punctuated accumulation and loss of cultural innovations. Proc Natl Acad Sci USA 112(49):E6762–E6769

    Google Scholar 

  • Laland KE, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. Proc Natl Acad Sci USA 96:10242–10247

    Google Scholar 

  • Laland KE, Odling-Smee FJ, Myles S (2010) How culture shaped the human genome: bringing genetics and the human sciences together. Nat Rev Genet 11:137–148

    Google Scholar 

  • Legare CH, Nielsen M (2015) Imitation and innovation: the dual engines of cultural learning. Trends Cogn Sci 19:688–699

    Google Scholar 

  • Majkić A, d’Errico F, Milošević S et al (2017) Sequential incisions on a cave bear bone from the Middle Paleolithic of Pešturina Cave, Serbia. J Archaeol Method Theory 25:69–116

    Google Scholar 

  • Mania D, Mania U (1988) Deliberate engravings on bone artefacts of homo erectus. Rock Art Res 5:91–97

    Google Scholar 

  • Marshack A (1964) Lunar notation of Upper Paleolithic remains. Science 184:28–46

    Google Scholar 

  • Marshack A (1972a) Upper Paleolithic notation and symbol. Science 178:817–828

    Google Scholar 

  • Marshack A (1972b) The root of civilization: the cognitive beginnings of man’s first art, symbol and notations. Weidenfeld and Nicolson, London

    Google Scholar 

  • McBrearty S, Brooks AS (2000) The revolution that wasn’t: a new interpretation of the origin of modern human behavior. J Hum Evol 39:453–563

    Google Scholar 

  • Mellars PA, Stringer CB (eds) (1989) The human revolution: behavioral and biological perspectives on the origins of modern humans. Edinburgh University Press, Edinburgh

    Google Scholar 

  • Morgan TJH, Uomini NT, Rendell LE et al (2015) Experimental evidence for the co-evolution of hominin tool-making, teaching and language. Nat Commun 6:1–8

    Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton

    Google Scholar 

  • Ong W (2002) Orality and literacy: the technologizing of the world. Routledge, New York

    Google Scholar 

  • Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401

    Google Scholar 

  • Pettitt P (2011) The palaeolithic origins of human burial. Routledge, New York

    Google Scholar 

  • Powell A, Shennan S, Thomas MG (2009) Late pleistocene demography and the appearance of modern human behavior. Science 324:1298–1301

    Google Scholar 

  • Premo LS, Hublin JJ (2009) Culture, population structure, and low genetic diversity in Pleistocene hominins. Proc Natl Acad Sci 106:33–37

    Google Scholar 

  • Price CJ, Devlin JT (2003) The myth of the visual word form area. NeuroImage 19:473–481

    Google Scholar 

  • Reich L, Szwed M, Cohen L, Amedi A (2011) A ventral visual stream reading center independent of visual experience. Curr Biol 21:363–368

    Google Scholar 

  • Richerson PJ, Boyd R (2005) Not by genes alone: how culture transformed human evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Rifkin RF, Dayet L, Queffelec A et al (2015) Evaluating the photoprotective effects of ochre on human skin by in vivo SPF assessment: Implications for human evolution, adaptation and dispersal. PLoS ONE 10:e0136090

    Google Scholar 

  • Rilling JK, Glasser MP, Preuss TM et al (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:425–428

    Google Scholar 

  • Rodríguez-Vidal J, d’Errico F, Pacheco FG et al (2014) A rock engraving made by Neanderthals in Gibraltar. Proc Natl Acad Sci USA 111:13301–13306

    Google Scholar 

  • Saygin ZM, Osher DE, Norton ES et al (2016) Connectivity precedes function in the development of the visual word form area. Nat Neurosci 19:1250–1255

    Google Scholar 

  • Scerri EM (2017) The North African middle stone age and its place in recent human evolution. Evol Anthropol 26:119–135

    Google Scholar 

  • Schlebusch CM, Malmström H, Günther T et al (2017) Ancient genomes from southern Africa pushes modern human divergence beyond 260,000 years ago. bioRxiv. https://doi.org/10.1101/145409

    Article  Google Scholar 

  • Shennan S (2001) Demography and cultural innovation: a model and its implications for the emergence of modern human culture. Camb Archaeol J 11:5–16

    Google Scholar 

  • Soressi M, McPherron SP, Lenoir M et al (2013) Neandertals made the first specialized bone tools in Europe. Proc Natl Acad Sci USA 110:14186–14190

    Google Scholar 

  • Sporns O, Tononi G, Kötter G (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:e42

    Google Scholar 

  • Stiner MC (2017) Love and death in the stone age: what constitutes first evidence of mortuary treatment of the human body? Biol Theory 12:248–261

    Google Scholar 

  • Stout D, Khreisheh N (2015) Skill learning and human brain evolution: an experimental approach. Camb Archaeol J 25:867–875

    Google Scholar 

  • Szwed M, Qiao E, Jobert A et al (2014) Effects of literacy in early visual and occipitotemporal areas of Chinese and French readers. J Cogn Neurosci 26:45–75

    Google Scholar 

  • Tan LH, Laird A, Li K, Fox PT (2005) Neuroantomical correlates of phonological processing of Chinese characters and alphabetic words: a meta-analysis. Hum Brain Mapp 25:83–91

    Google Scholar 

  • Tattersall I (1995) The fossil trail: how we know what we think we know about human evolution. Oxford University Press, New York

    Google Scholar 

  • Tennie C, Call J, Tomasello M (2009) Ratcheting up the ratchet: on the evolution of cumulative culture. Phil Trans R Soc B 364:2405–2415

    Google Scholar 

  • Thiebaut de Schotten M, Cohen L, Amemiya E et al (2012) Learning to read improves the structure of the arcuate fasciculus. Cereb Cortex 24:989–995

    Google Scholar 

  • Tomasello M (2001) Cultural transmission: a view from chimpanzees and human infants. J Cross-Cult Psychol 32(2):135–146

    Google Scholar 

  • Varki A, Geschwind DH, Eichler EE (2008) Explaining human uniqueness: genome interactions with environment, behaviour and culture. Nat Rev Genet 9:749–763

    Google Scholar 

  • Vigneau M, Jobard G, Mazoyer B, Tzourio-Mazoyer N (2005) Word and non-word reading: what role for the visual word. Form Area? NeuroImage 27:694–705

    Google Scholar 

  • Villa P, Roebroek W (2014) Neandertal demise: an archaeological analysis of the modern human superiority complex. PLoS ONE 9:e96424

    Google Scholar 

  • Vinckier F, Dehaene S, Jobert A et al (2007) Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron 55:143–156

    Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Google Scholar 

  • Waddington CH (1953) Genetic assimilation of an acquired character. Evolution 7:118–126

    Google Scholar 

  • Warrington EK, Shallice T (1980) Word-form dyslexia. Brain 103:99–112

    Google Scholar 

  • Woollett K, Maguire EA (2011) Acquiring ‘the Knowledge’ of London’s layout drives structural brain changes. Curr Biol 21:2109–2114

    Google Scholar 

  • Yeatman JD, Dougherty RF, Ben-Shachar M, Wandell BA (2012) Development of white matter and reading skills. Proc Natl Acad Sci USA 109:E3045–E3053

    Google Scholar 

  • Zilhão J (2016) Lower and middle Palaeolithic mortuary behaviours and the origins of ritual burial. In: Renfrew C, Boyd MJ, Morley I (eds) Death rituals, social order and the archaeology of immortality in the ancient world. Cambridge University Press, Cambridge, pp 27–44

    Google Scholar 

Download references

Acknowledgements

We thank William Banks, Karl Zilles, and Paolo D’Ambrosio for helpful discussions; Laura Comoglio and Luc Doyon for critical reading of the manuscript; and Gauthier Devilder for help with Fig. 2. We also thank two anonymous reviewers for their helpful comments. This research was partially supported by the Research Council of Norway through its Centres of Excellence funding scheme, SFF Centre for Early Sapiens Behaviour (SapienCE), project number 262618, and by the Agence Nationale de la Recherche (ANR-10-LABX-52), LaScArBx Cluster of Excellence.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francesco d’Errico.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

d’Errico, F., Colagè, I. Cultural Exaptation and Cultural Neural Reuse: A Mechanism for the Emergence of Modern Culture and Behavior. Biol Theory 13, 213–227 (2018). https://doi.org/10.1007/s13752-018-0306-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13752-018-0306-x

Keywords

Navigation