Abstract
Archaeological and palaeontological evidence from the Early Stone Age (ESA) documents parallel trends of brain expansion and technological elaboration in human evolution over a period of more than 2 Myr. However, the relationship between these defining trends remains controversial and poorly understood. Here, we present results from a positron emission tomography study of functional brain activation during experimental ESA (Oldowan and Acheulean) toolmaking by expert subjects. Together with a previous study of Oldowan toolmaking by novices, these results document increased demands for effective visuomotor coordination and hierarchical action organization in more advanced toolmaking. This includes an increased activation of ventral premotor and inferior parietal elements of the parietofrontal praxis circuits in both the hemispheres and of the right hemisphere homologue of Broca's area. The observed patterns of activation and of overlap with language circuits suggest that toolmaking and language share a basis in more general human capacities for complex, goal-directed action. The results are consistent with coevolutionary hypotheses linking the emergence of language, toolmaking, population-level functional lateralization and association cortex expansion in human evolution.
References
Ambrose S . 2001Paleolithic technology and human evolution. Science 291, 1748–1753.doi:10.1126/science.1059487. Crossref, PubMed, ISI, Google ScholarAron A.A, Robbins T.W& Poldrack R.A . 2004Inhibition and the right inferior frontal cortex. Trends Cogn. Sci 8, 170–177.doi:10.1016/j.tics.2004.02.010. Crossref, PubMed, ISI, Google ScholarBookheimer S . 2002Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annu. Rev. Neurosci 25, 151–188.doi:10.1146/annurev.neuro.25.112701.142946. Crossref, PubMed, ISI, Google ScholarBuxbaum L.J, Johnson-Frey S.H& Bartlett-Williams M . 2005Deficient internal models for planning hand–object interactions in apraxia. Neuropsychologica 43, 917–929.doi:10.1016/j.neuropsychologia.2004.09.006. Crossref, PubMed, ISI, Google ScholarChaminade T, Meltzoff A& Decety J . 2005An fMRI study of imitation: action representation and body schema. Neuropsychologica 43, 115–127.doi:10.1016/j.neuropsychologia.2004.04.026. Crossref, PubMed, ISI, Google ScholarCorballis M.C . 2003From mouth to hand: gesture, speech, and the evolution of right handedness. Behav. Brain. Sci 26, 199–260.doi:10.1017/S0140525X03000062. Crossref, PubMed, ISI, Google ScholarDagher A, Owen A.M, Boecker H& Brooks D.J . 1999Mapping the network for planning: a correlational PET activation study with the Tower of London task. Brain 122, 1973–1987.doi:10.1093/brain/122.10.1973. Crossref, PubMed, ISI, Google ScholarDelagnes A& Roche H . 2005Late Pliocene hominid knapping skills: the case of Lokalalei 2C, West Turkana, Kenya. J. Hum. Evol 48, 435–472.doi:10.1016/j.jhevol.2004.12.005. Crossref, PubMed, ISI, Google ScholarEdwards S.W . 2001A modern knapper's assessment of the technical skills of the Late Acheulean biface workers at Kalambo Falls. Kalambo Falls prehistoric site.& Clark J.D . The earlier cultures: Middle and Earlier Stone Age, 605–611.Cambridge, UK:Cambridge University Press. Google ScholarFrey S.H, Vinton D, Norlund R& Grafton S.T . 2005Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Cogn. Brain Res 23, 397–405.doi:10.1016/j.cogbrainres.2004.11.010. Crossref, PubMed, Google ScholarGazzaniga M.S . 2000Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition?. Brain 123, 1293–1326.doi:10.1093/brain/123.7.1293. Crossref, PubMed, ISI, Google ScholarGibson K.R& Ingold T . 1993Tools, language and cognition in human evolution. Cambridge, UK:Cambridge University Press. Google ScholarGoel V, Tierney M, Sheesley L, Bartolo A, Vartanian O& Grafman J . 2007Hemispheric specialization in human prefrontal cortex for resolving certain and uncertain inferences. Cereb. Cortex 17, 2245–2250.doi:10.1093/cercor/bhl132. Crossref, PubMed, ISI, Google ScholarGreenfield P.M . 1991Language, tools, and brain: the development and evolution of hierarchically organized sequential behavior. Behav. Brain Sci 14, 531–595. Crossref, ISI, Google ScholarGrezes J& Decety J . 2001Functional anatomy of execution, mental simulation, observation, and verb generation of action: a meta-analysis. Hum. Brain Mapp 12, 1–19.doi:10.1002/1097-0193(200101)12:1<1::AID-HBM10>3.0.CO;2-V. Crossref, PubMed, ISI, Google ScholarGuiard Y . 1987Asymmetric division of labor in human skilled bimanual action: the kinematic chain as a model. J. Motor Behav 19, 486–517. Crossref, PubMed, ISI, Google ScholarHagoort P . 2005On Broca, brain, and binding: a new framework. Trends Cogn. Sci 9, 416–423.doi:10.1016/j.tics.2005.07.004. Crossref, PubMed, ISI, Google ScholarHamzei F, Rijntjes M, Dettmers C, Glauche V, Weiller C& Buchel C . 2003The human action recognition system and its relationship to Broca's area: an fMRI study. Neuroimage 19, 637–644.doi:10.1016/S1053-8119(03)00087-9. Crossref, PubMed, ISI, Google ScholarHartmann K, Goldenberg G, Daumuller M& Hermsdorfer J . 2005It takes the whole brain to make a cup of coffee: the neuropsychology of naturalistic actions involving technical devices. Neuropsychologia 43, 625–637.doi:10.1016/j.neuropsychologia.2004.07.015. Crossref, PubMed, ISI, Google ScholarHolloway R, Broadfield D& Yuan M . 2004The human fossil record. Brain endocasts—the paleoneurological evidence vol. 3Hoboken, NJ:Wiley-Liss. Crossref, Google ScholarInizan M.-L, Reduron-Ballinger M, Roche H& Tixier J . 1999Technology and terminology of knapped stone. Nanterre, France:C.R.E.P. Google ScholarIriki A . 2005A prototype of Homo faber: a silent precursor of human intelligence in the tool-using monkey brain., Dehaene S, Duhamel J.-R, Hauser M.D& Rizzolatti G In From monkey brain to human brain: a Fyssen foundation symposiumCambridge, MA:MIT Press253–271. Google ScholarJohnson-Frey S.H . 2003What's so special about human tool use?. Neuron 39, 201–204.doi:10.1016/S0896-6273(03)00424-0. Crossref, PubMed, ISI, Google ScholarJohnson-Frey S.H . 2004The neural bases of complex tool use in humans. Trends Cogn. Sci 8, 71–78.doi:10.1016/j.tics.2003.12.002. Crossref, PubMed, ISI, Google ScholarJohnson-Frey S.H, Newman-Norlund R& Grafton S.T . 2005A distributed left hemisphere network active during planning of everyday tool use skills. Cereb. Cortex 15, 681–695.doi:10.1093/cercor/bhh169. Crossref, PubMed, ISI, Google ScholarKellenbach M.L, Brett M& Patterson K . 2003Actions speak louder than functions: the importance of manipulability and action in tool representation. J. Cogn. Neurosci 15, 30–45.doi:10.1162/089892903321107800. Crossref, PubMed, ISI, Google ScholarKelly A.M& Garavan H . 2005Human functional neuroimaging of brain changes associated with practice. Cereb. Cortex 15, 1089–1102.doi:10.1093/cercor/bhi005. Crossref, PubMed, ISI, Google ScholarKimura D . 1979Neuromotor mechanisms in the evolution of human communication. Neurobiology of social communication in primates, Steklis L.H.D& Raleigh M.J 179–219New York, NY:Academic Press. Google ScholarKoechlin E& Jubault T . 2006Broca's Area and the hierarchical organization of human behavior. Neuron 50, 963–974.doi:10.1016/j.neuron.2006.05.017. Crossref, PubMed, ISI, Google ScholarLeakey M.D . 1971Olduvai Gorge. Excavations in Beds I and II, 1960–1963 vol. 3New York, NY:Cambridge University Press. Google ScholarLewis J.W . 2006Cortical networks related to human use of tools. Neuroscientist 12, 211–231.doi:10.1177/1073858406288327. Crossref, PubMed, ISI, Google ScholarLieberman P . 2002On the nature and evolution of the neural bases of human language. Am. J. Phys. Anthropol 45, 36–62.doi:10.1002/ajpa.10171. Crossref, ISI, Google ScholarMacNeilage P.F, Studdert-Kennedy M.G& Lindblom B . 1984Functional precursors to language and its lateralization. Am. J. Physiol. Regul. Integr. Comp. Physiol 246, R912–R914. Crossref, Google ScholarMaravita A& Iriki A . 2004Tools for the body (schema). Trends Cogn. Sci 8, 79–86.doi:10.1016/j.tics.2003.12.008. Crossref, PubMed, ISI, Google ScholarOrban G.A, Claeys K, Nelissen K, Smans R, Sunaert S, Todd J.T, Wardak C, Durand J.-B& Vanduffel W . 2006Mapping the parietal cortex of human and non-human primates. Neuropsychologia 44, 2647–2667.doi:10.1016/j.neuropsychologia.2005.11.001. Crossref, PubMed, ISI, Google ScholarPassingham R.E . 1998The specializations of the human neocortex. Comparative neuropsychology& Milner A.D 271–298New York, NY:Oxford University Press. Crossref, Google ScholarPassingham R.E& Sakai K . 2004The prefrontal cortex and working memory: physiology and brain imaging. Curr. Opin. Neurobiol 14, 163–168.doi:10.1016/j.conb.2004.03.003. Crossref, PubMed, ISI, Google ScholarPassingham R.E, Toni I& Rushworth M.F.S . 2000Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning. Exp. Brain Res 133, 103–113.doi:10.1007/s002210000405. Crossref, PubMed, ISI, Google ScholarPetrides M . 2005The rostral-caudal axis of cognitive control within lateral frontal cortex. From monkey brain to human brain: a Fyssen Foundation symposium, Dehaene S, Duhamel J.-R, Hauser M.D& Rizzolatti G 293–314Cambridge, MA:MIT Press. Google ScholarRidderinkhof K.R, van den Wildenberg W.P.M, Segalowitz S.J& Carter C.S . 2004Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward based learning. Brain Cogn 56, 129–140.doi:10.1016/j.bandc.2004.09.016. Crossref, PubMed, ISI, Google ScholarRijntjes M, Dettmers C, Buchel C, Kiebel S, Frackowiak R.S.J& Weiller C . 1999A blueprint for movement: functional and anatomical representations in the human motor system. J. Neurosci 19, 8043–8048. Crossref, PubMed, ISI, Google ScholarRilling J.K . 2006Human and nonhuman primate brains: are they allometrically scaled versions of the same design. Evol. Anthropol 15, 65–77.doi:10.1002/evan.20095. Crossref, ISI, Google ScholarRizzolatti G& Arbib M.A . 1998Language within our grasp. Trends Cogn. Sci 21, 188–194. Google ScholarRizzolatti G& Craighero L . 2004The mirror–neuron system. Annu. Rev. Neurosci 27, 169–192.doi:10.1146/annurev.neuro.27.070203.144230. Crossref, PubMed, ISI, Google ScholarRizzolatti G, Luppino G& Matelli M . 1998The organization of the cortical motor system: new concepts. Electroencephalogr. Clin. Neurophysiol 106, 283–296.doi:10.1016/S0013-4694(98)00022-4. Crossref, PubMed, Google ScholarRose D . 2006A systematic functional approach to language evolution. Camb. Archaeol. J 16, 73–96.doi:10.1017/S0959774306000059. Crossref, ISI, Google ScholarRoux V& David E . 2005Planning abilities as a dynamic perceptual–motor skill: an actualistic study of different levels of expertise involved in stone knapping. Stone knapping: the necessary conditions for a uniquely hominin behaviour, Roux V& Bril B 91–108Cambridge, UK:McDonald Institute for Archaeological Research. Google ScholarSchick K.D& Toth N . 1993Making silent stones speak: human evolution and the dawn of technology. New York, NY:Simon & Schuster. Google ScholarSemaw S . 2000The world's oldest stone artefacts from Gona, Ethiopia: their implications for understanding stone technology and patterns of human evolution 2.6–1.5 million years ago. J. Archaeol. Sci 27, 1197–1214.doi:10.1006/jasc.1999.0592. Crossref, ISI, Google ScholarSemaw S, Renne P, Harris J.W.K, Feibel C.S, Bernor R.L, Fesseha N& Mowbray K . 19972.5-million-year-old stone tools from Gona, Ethiopia. Nature 385, 333–336.doi:10.1038/385333a0. Crossref, PubMed, ISI, Google ScholarSteele J& Uomini N . 2005Humans, tools and handedness. Stone knapping: the necessary conditions for a uniquely hominin behaviour, Roux V& Bril B 217–239Cambridge, UK:McDonald Institute for Archaeological Research. Google ScholarStephan K.E, Marshall J.C, Friston K.J, Rowe J.B, Ritzl A, Zilles K& Fink G.R . 2003Lateralized cognitive processes and lateralized task control in the human brain. Science 301, 384–386.doi:10.1126/science.1086025. Crossref, PubMed, ISI, Google ScholarStout D . 2002Skill and cognition in stone tool production: an ethnographic case study from Irian Jaya. Curr. Anthropol 45, 693–722.doi:10.1086/342638. Crossref, ISI, Google ScholarStout D . 2006Oldowan toolmaking and hominin brain evolution: theory and research using positron emission tomography (PET). The Oldowan: case studies into the earliest Stone Age, Toth N& Schick K 267–305Gosport, IN:Stone Age Institute Press. Google ScholarStout D& Chaminade T . 2007The evolutionary neuroscience of tool making. Neuropsychologia 45, 1091–1100.doi:10.1016/j.neuropsychologia.2006.09.014. Crossref, PubMed, ISI, Google ScholarStout D, Toth N& Schick K . 2006Acheulean toolmaking and hominin brain evolution: a pilot study using positron emission tomography. The Oldowan: case studies into the earliest Stone Age, Toth N& Schick K 321–331Gosport, IN:Stone Age Institute Press. Google ScholarStuddert-Kennedy M& Goldstein L . 2003Launching language: the gestural origins of discrete infinity. Language evolution, Christiansen M.H& Kirby S 235–254Oxford, UK:Oxford University Press. Crossref, Google ScholarToth N . 2001Experiments in quarrying large flake blanks at Kalambo Falls. Kalambo Falls prehistoric site. The earlier cultures: Middle and Earlier Stone Age& Clark J.D 600–604 vol. IIICambridge, UK:Cambridge University Press. Google ScholarWing A.M . 2000Motor control: mechanisms of motor equivalence in handwriting. Curr. Biol 10, R245–R248.doi:10.1016/S0960-9822(00)00375-4. Crossref, PubMed, ISI, Google ScholarWynn T . 2002Archaeology and cognitive evolution. Behav. Brain. Sci 25, 389–438.doi:10.1017/S0140525X02530120. Crossref, PubMed, ISI, Google Scholar


