Volume 19, Issue 1-2
  • ISSN 1572-0373
  • E-ISSN: 1572-0381
Buy:$35.00 + Taxes



We used optical neuroimaging to explore the extent of functional overlap between working memory (WM) networks involved in language and Early Stone Age toolmaking behaviors. Oldowan tool production activates two verbal WM areas, but the functions of these areas are indistinguishable from general auditory WM, suggesting that the first hominin toolmakers relied on early precursors of verbal WM to make simple flake tools. Early Acheulian toolmaking elicits activity in a region bordering on Broca’s area that is involved in both visual and verbal WM tasks. The sensorimotor and mirror neurons in this area, along with enhancement of general WM capabilities around 1.8 million years ago, may have provided the scaffolding upon which a WM network dedicated to processing exclusively linguistic information could evolve. In the road map going forward, neuro-archaeologists should investigate the trajectory of WM over the course of human evolution to better understand its contribution to language origins.


Article metrics loading...

Loading full text...

Full text loading...


  1. Acheson, D. J., MacDonald, M. C.
    (2009) Verbal working memory and language production: Common approaches to the serial ordering of verbal information. Psychological Bulletin, 134, 50–68.10.1037/a0014411
    https://doi.org/10.1037/a0014411 [Google Scholar]
  2. Arbib, M. A.
    (2011) From mirror neurons to complex imitation in the evolution of language and tool use. Annual Review of Anthropology, 40, 257–273.10.1146/annurev‑anthro‑081309‑145722
    https://doi.org/10.1146/annurev-anthro-081309-145722 [Google Scholar]
  3. (2016) Towards a computational comparative neuroprimatology: Framing the language-ready brain. Physics of Life Reviews, 16, 1–54.10.1016/j.plrev.2015.09.003
    https://doi.org/10.1016/j.plrev.2015.09.003 [Google Scholar]
  4. Baddeley, A.
    (2000) The episodic buffer: A new component of working memory?Trends in Cognitive Sciences, 4, 417–423.10.1016/S1364‑6613(00)01538‑2
    https://doi.org/10.1016/S1364-6613(00)01538-2 [Google Scholar]
  5. (2012) Working memory: Theories, models, and controversies. Annual Review of Psychology, 63, 1–29.10.1146/annurev‑psych‑120710‑100422
    https://doi.org/10.1146/annurev-psych-120710-100422 [Google Scholar]
  6. Baddeley, A., Hitch, G.
    (1974) Working memory. New York: Academic Press.10.1016/S0079‑7421(08)60452‑1
    https://doi.org/10.1016/S0079-7421(08)60452-1 [Google Scholar]
  7. Bangert, M., Peschel, T., Schlaug, G., Rotte, M., Drescher, D., Hinrichs, H., Heinze, H-J., Altenmüller, E.
    (2006) Shared networks for auditory and motor processing in professional pianists: Evidence from fMRI conjunction. NeuroImage, 30, 917–926.10.1016/j.neuroimage.2005.10.044
    https://doi.org/10.1016/j.neuroimage.2005.10.044 [Google Scholar]
  8. Beyene, Y., Katoh, S., WoldeGabriel, G., Hart, W. K., Uto, K., Sudo, M., Kondo, M., Hyodo, M., Renne, P. R., Suwa, G., Asfaw, B.
    (2013) The characteristics and chronology of the earliest Acheulean at Konso, Ethiopia. Proceedings of the National Academy of Sciences, 110, 1584–1591.10.1073/pnas.1221285110
    https://doi.org/10.1073/pnas.1221285110 [Google Scholar]
  9. Constantinidis, C., Procyk, E.
    (2004) The primate working memory networks. Cognitive, Affective, & Behavioral Neuroscience, 4, 444–465.10.3758/CABN.4.4.444
    https://doi.org/10.3758/CABN.4.4.444 [Google Scholar]
  10. Coolidge, F. L., Wynn, T.
    (2005) Working memory, its executive functions, and the emergence of modern thinking. Cambridge Archaeological Journal, 15, 5–26.10.1017/S0959774305000016
    https://doi.org/10.1017/S0959774305000016 [Google Scholar]
  11. Corbetta, M., Schulman, G. L.
    (2002) Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201–215.10.1038/nrn755
    https://doi.org/10.1038/nrn755 [Google Scholar]
  12. Courtney, S. M., Ungerleider, L. G., Keil, K., Haxby, J. V.
    (1996) Object and spatial visual working memory activate separate neural systems in human cortex. Cerebral Cortex, 6, 39–49.10.1093/cercor/6.1.39
    https://doi.org/10.1093/cercor/6.1.39 [Google Scholar]
  13. Coutlee, C. G., Huettel, S. A.
    (2012) The functional neuroanatomy of decision making: Prefrontal control of thought and action. Brain Research, 1428C, 3–12.10.1016/j.brainres.2011.05.053
    https://doi.org/10.1016/j.brainres.2011.05.053 [Google Scholar]
  14. De Benni, R., Pazzaglia, F., Gyselinck, V., Meneghetti, C.
    (2005) Visuospatial working memory and mental representation of spatial descriptions. European Journal of Cognitive Psychology, 17, 77–95.10.1080/09541440340000529
    https://doi.org/10.1080/09541440340000529 [Google Scholar]
  15. Fadiga, L., Craighero, L., D’Ausilio, A.
    (2009) Broca’s area in language, action, and music. Annual New York Academy of Sciences, 1169, 448–458.10.1111/j.1749‑6632.2009.04582.x
    https://doi.org/10.1111/j.1749-6632.2009.04582.x [Google Scholar]
  16. Fassihi, A., Akrami, A., Esmaeili, V., Diamond, M. E.
    (2014) Tactile perception and working memory in rats and humans. Proceedings of the National Academy of Sciences, 111, 2331–2336.10.1073/pnas.1315171111
    https://doi.org/10.1073/pnas.1315171111 [Google Scholar]
  17. Fiebach, C. J., Schubotz, R. I.
    (2006) Dynamic anticipatory processing of hierarchical sequential events: A common role for Broca’s area and ventral premotor cortex across domains?Cortex, 42, 499–502.10.1016/S0010‑9452(08)70386‑1
    https://doi.org/10.1016/S0010-9452(08)70386-1 [Google Scholar]
  18. Gathercole, S. E., Baddeley, A. D.
    (2014) Working Memory and Language: Essays in Cognitive Psychology. New York: Psychology Press.
    [Google Scholar]
  19. Goldman-Rakic, P. S.
    (1996) Regional and cellular fractionation of working memory. Proceedings of the National Academy of Sciences, 93, 13473–13480.10.1073/pnas.93.24.13473
    https://doi.org/10.1073/pnas.93.24.13473 [Google Scholar]
  20. Greenfield, P. M.
    (1991) Language, tools and brain: The ontogeny and phylogeny of hierarchically organized sequential behavior. Behavioral and Brain Sciences, 14, 531–595.10.1017/S0140525X00071235
    https://doi.org/10.1017/S0140525X00071235 [Google Scholar]
  21. Grèzes, J., Armony, J. L., Rowe, J., Passingham, R. E.
    (2003) Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study. NeuroImage, 18, 928–937.10.1016/S1053‑8119(03)00042‑9
    https://doi.org/10.1016/S1053-8119(03)00042-9 [Google Scholar]
  22. Heekeren, H. R., Marrett, S., Ruff, D. A., Bandettini, P. A., Ungerledier, L. G.
    (2006) Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality. Proceedings of the National Academy of Sciences, 103, 10023–10028.10.1073/pnas.0603949103
    https://doi.org/10.1073/pnas.0603949103 [Google Scholar]
  23. Jessen, F., Erb, M., Klose, U., Lotze, M., Grodd, W., Heun, R.
    (1999) Activation of human language processing brain regions after the presentation of random letter strings demonstrated with event-related functional magnetic resonance imaging. Neuroscience Letters, 270, 13–16.10.1016/S0304‑3940(99)00453‑X
    https://doi.org/10.1016/S0304-3940(99)00453-X [Google Scholar]
  24. Jönsson, F. U., Møller, P., Olsson, M. J.
    (2011) Olfactory working memory: Effects of verbalization on the 2-back test. Memory & Cognition, 39, 1023–1032.10.3758/s13421‑011‑0080‑5
    https://doi.org/10.3758/s13421-011-0080-5 [Google Scholar]
  25. Just, M. A., Carpenter, P. A.
    (1992) A capacity theory of comprehension: Individual differences in working memory. Psychological Review, 99, 122–149.10.1037/0033‑295X.99.1.122
    https://doi.org/10.1037/0033-295X.99.1.122 [Google Scholar]
  26. Kaller, C. P., Rahm, B., Spreer, J., Weiller, C., Unterrainer, J. M.
    (2011) Dissociable contributions of left and right dorsolateral prefrontal cortex in planning. Cerebral Cortex, 21, 307–317.10.1093/cercor/bhq096
    https://doi.org/10.1093/cercor/bhq096 [Google Scholar]
  27. Kumar, S., Joseph, S., Gander, P. E., Barascud, N., Halpern, A. R., Griffiths, T. D.
    (2016) A brain system for auditory working memory. Journal of Neuroscience, 36, 4492–4505. Quantity, not quality: The relationship between fluid intelligence and working memory capacity. Psychonomic Bulletin & Review, 17, 673–679.
    [Google Scholar]
  28. Lara, A. H., Kennerley, S. W., Wallis, J. D.
    (2009) Encoding of gustatory working memory by orbitofrontal neurons. The Journal of Neuroscience, 29, 765–774.10.1523/JNEUROSCI.4637‑08.2009
    https://doi.org/10.1523/JNEUROSCI.4637-08.2009 [Google Scholar]
  29. Lehnert, G., Zimmer, H. D.
    (2008) Modality and domain specific components in auditory and visual working memory tasks. Cognitive Process, 9, 53–61.10.1007/s10339‑007‑0187‑6
    https://doi.org/10.1007/s10339-007-0187-6 [Google Scholar]
  30. Mahaney, R. A.
    (2014) Exploring the complexity and structure of Acheulean in relation to natural language. PaleoAnthropology2014, 586–606.
    [Google Scholar]
  31. McGuire, P. K., Silbersweig, D. A., Murray, R. M., David, A. S., Frackowiak, R. S. J., Frith, C. D.
    (1996) Functional anatomy of inner speech and auditory verbal imagery. Psychological Medicine, 26, 29–38.10.1017/S0033291700033699
    https://doi.org/10.1017/S0033291700033699 [Google Scholar]
  32. Nie, Q. -Y., Müller, H. J., Conci, M.
    (2017) Hierarchical organization in visual working memory: From global ensemble to individual object structure. Cognition159, 85–96.10.1016/j.cognition.2016.11.009
    https://doi.org/10.1016/j.cognition.2016.11.009 [Google Scholar]
  33. Pardo-Vazquez, J. L., Padron, I., Fernadez-Rey, J., Acuña, C.
    (2011) Decision-making in the ventral premotor cortex harbinger of action. Frontiers in Integrative Neuroscience, 5, 1–14.10.3389/fnint.2011.00054
    https://doi.org/10.3389/fnint.2011.00054 [Google Scholar]
  34. Petit, L., Simon, G., Joliot, M., Andersson, F., Bertin, T., Zago, L., Mellet, E., Tzourio-Mazoyer, N.
    (2007) Right hemisphere dominance for auditory attention and its modulation by eye position: An event related fMRI study. Restorative Neurology and Neuroscience, 25, 211–225.
    [Google Scholar]
  35. Putt, S. S., Wijeakumar, S., Franciscus, R. G., Spencer, J. P.
    (2017) The functional brain networks that underlie Early Stone Age tool manufacture. Nature Human Behaviour, 1, 1–8.10.1038/s41562‑017‑0102
    https://doi.org/10.1038/s41562-017-0102 [Google Scholar]
  36. Rämä, P., Sala, J. B., Gillen, J. S., Pekar, J. J., Courtney, S. M.
    (2001) Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information. Cognitive, Affective, & Behavioral Neuroscience, 1, 161–171.10.3758/CABN.1.2.161
    https://doi.org/10.3758/CABN.1.2.161 [Google Scholar]
  37. Romanski, L. M., Goldman-Rakic, P. S.
    (2002) An auditory domain in primate prefrontal cortex. Nature Neuroscience, 5, 15–16.10.1038/nn781
    https://doi.org/10.1038/nn781 [Google Scholar]
  38. Rothmayr, C., Baumann, O., Endestad, T., Rutschmann, R. M., Magnussen, S., Greenlee, M. W.
    (2007) Dissociation of neural correlates of verbal and non-verbal visual working memory with different delays. Behavioral and Brain Functions, 3(56), 1–11.
    [Google Scholar]
  39. Schulze, K., Mueller, K., Koelsch, S.
    (2010) Neural correlates of strategy use during auditory working memory in musicians and non-musicians. European Journal of Neuroscience, 33, 189–196.10.1111/j.1460‑9568.2010.07470.x
    https://doi.org/10.1111/j.1460-9568.2010.07470.x [Google Scholar]
  40. Semaw, S., Renne, P., Harris, J. W. K., Feibel, C. S., Bernor, R. L., Fesseha, N., et al.
    (1997) 2.5-million-year-old stone tools from Gona, Ethiopia. Nature, 385, 333–336.10.1038/385333a0
    https://doi.org/10.1038/385333a0 [Google Scholar]
  41. Shipton, C.
    (2010) Imitation and shared intentionality in the Acheulean. Cambridge Archaeologicial Journal, 20, 197–210.10.1017/S0959774310000235
    https://doi.org/10.1017/S0959774310000235 [Google Scholar]
  42. Stout, D.
    (2018) Archaeology and language evolution: From skilled action to meaningful interaction. Interaction Studies.
    [Google Scholar]
  43. Stout, D., Hecht, E.
    (2015) Neuroarchaeology. InE. Bruner (Ed.), vol.3: Human Paleoneurology (pp.145–175). New York: Springer International Publishing.
    [Google Scholar]
  44. Stout, D. Hecht, E., Khreisheh, N., Bradley, B., Chaminade, T.
    (2015) Cognitive demands of Lower Paleolithic toolmaking. PloS ONE, 10, e0121804.10.1371/journal.pone.0121804
    https://doi.org/10.1371/journal.pone.0121804 [Google Scholar]
  45. Stout, D., Toth, N., Schick, K. D., Chaminade, T.
    (2008) Neural correlates of Early Stone Age tool-making: Technology, language and cognition in human evolution. Philosophical Transactions of the Royal Society B, 363, 1939–1949.10.1098/rstb.2008.0001
    https://doi.org/10.1098/rstb.2008.0001 [Google Scholar]
  46. Toth, N.
    (1985) The Oldowan reassessed: A close look at early stone artifacts. Journal of Archaeological Science, 12, 101–120.10.1016/0305‑4403(85)90056‑1
    https://doi.org/10.1016/0305-4403(85)90056-1 [Google Scholar]
  47. Toth, N., Schick, K. D., Savage-Rumbaugh, E. S., Sevcik, R. A., Rumbaugh, D. M.
    (1993) Pan the tool-maker: Investigations into the stone tool-making and stone tool-using capabilities of a bonobo (Pan paniscus). Journal of Archaeological Science, 20(1):81–91.10.1006/jasc.1993.1006
    https://doi.org/10.1006/jasc.1993.1006 [Google Scholar]
  48. Vigneau, M., Beaucousin, V., Hervé, P-Y., Jobard, G., Petit, L. Crivello, F., Mellet, E., Zago, L., Mazoyer, B., Tzourio-Mazoyer, N.
    (2011) What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis. NeuroImage, 54, 577–593.10.1016/j.neuroimage.2010.07.036
    https://doi.org/10.1016/j.neuroimage.2010.07.036 [Google Scholar]
  49. Wadley, L.
    (2010) Compound-adhesive manufacture as a behavioral proxy for complex cognition in the Middle Stone Age. Current Anthropology, 51, S111–S119.10.1086/649836
    https://doi.org/10.1086/649836 [Google Scholar]
  50. Warburton, E. A., Wise, R. J. S., Price, C. J., Weiller, C., Hadar, U., Ramsay, S., Fackowiak, R. S. J.
    (1996) Noun and verb retrieval by normal subjects. Studies with PET. Brain, 119, 159–179.10.1093/brain/119.1.159
    https://doi.org/10.1093/brain/119.1.159 [Google Scholar]
  51. Wijeakumar, S., Huppert, T. J., Magnotta, V. A., Buss, A. T., Spencer, J. P.
    (2017) Validating an image-based fNIRS approach with fMRI and a working memory task. NeuroImage, 147, 204–218.10.1016/j.neuroimage.2016.12.007
    https://doi.org/10.1016/j.neuroimage.2016.12.007 [Google Scholar]
  52. Wijeakumar, S., Spencer, J. P., Bohache, K., Boas, D. A., Magnotta, V. A.
    (2015) Validating a new methodology for optical probe design and image registration in fNIRS studies. NeuroImage, 106, 86–100.10.1016/j.neuroimage.2014.11.022
    https://doi.org/10.1016/j.neuroimage.2014.11.022 [Google Scholar]
  53. Whittaker, J. C.
    (1994) Flintknapping: Making and Understanding Stone Tools. Austin: University of Texas Press.
    [Google Scholar]
  54. Williams, V. M. E., Burke, A., Lombard, M.
    (2014) Throwing spears and shooting arrows: Preliminary results of a pilot neuroarchaeological study. The South African Archaeological Bulletin, 69, 199–207.
    [Google Scholar]
  55. Wright, R. V. S.
    (1972) Imitative learning of a flaked stone technology–The case of an orangutan. The Australian Journal of Anthropology, 8, 296–306.10.1111/j.1835‑9310.1972.tb00451.x
    https://doi.org/10.1111/j.1835-9310.1972.tb00451.x [Google Scholar]
  56. Wynn, T.
    (1979) The intelligence of later Acheulean hominids. Man, 14, 371–391.10.2307/2801865
    https://doi.org/10.2307/2801865 [Google Scholar]
  57. Wynn, T., Coolidge, F. L.
    (2010) Beyond symbolism and language: An introduction to Supplement 1, Working Memory. Current Anthropology, 51(S1), S5–S16.10.1086/650526
    https://doi.org/10.1086/650526 [Google Scholar]

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was successful
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error