Article published in:
How the Brain Got Language: Towards a New Road Map
Edited by Michael A. Arbib
[Interaction Studies 19:1/2] 2018
► pp. 272–288

Tracing the evolutionary trajectory of verbal working memory with neuro-archaeology

| The Stone Age Institute | Indiana University
| University of Stirling
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.
Keywords: visual working memory, auditory working memory, ventral premotor cortex, protolanguage, stone tools
Article outline
  • Introduction
  • Neuro-archaeological insights into the evolution of working memory
    • Working memory centers activated during stone tool production
  • Discussion
  • Towards a new road map
  • Acknowledgements
  • References
Published online: 17 September 2018
https://doi.org/10.1075/is.17042.put
References
Acheson, D. J., MacDonald, M. C.
(2009) Verbal working memory and language production: Common approaches to the serial ordering of verbal information. Psychological Bulletin, 1341, 50–68. CrossrefGoogle Scholar
Arbib, M. A.
(2011) From mirror neurons to complex imitation in the evolution of language and tool use. Annual Review of Anthropology, 401, 257–273. CrossrefGoogle Scholar
(2016) Towards a computational comparative neuroprimatology: Framing the language-ready brain. Physics of Life Reviews, 161, 1–54. CrossrefGoogle Scholar
Baddeley, A.
(2000) The episodic buffer: A new component of working memory? Trends in Cognitive Sciences, 41, 417–423. CrossrefGoogle Scholar
(2012) Working memory: Theories, models, and controversies. Annual Review of Psychology, 631, 1–29. CrossrefGoogle Scholar
Baddeley, A., Hitch, G.
(1974) Working memory. New York: Academic Press. CrossrefGoogle Scholar
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, 301, 917–926. CrossrefGoogle Scholar
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, 1101, 1584–1591. CrossrefGoogle Scholar
Constantinidis, C., Procyk, E.
(2004) The primate working memory networks. Cognitive, Affective, & Behavioral Neuroscience, 41, 444–465. CrossrefGoogle Scholar
Coolidge, F. L., Wynn, T.
(2005) Working memory, its executive functions, and the emergence of modern thinking. Cambridge Archaeological Journal, 151, 5–26. CrossrefGoogle Scholar
Corbetta, M., Schulman, G. L.
(2002) Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 31, 201–215. CrossrefGoogle Scholar
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, 61, 39–49. CrossrefGoogle Scholar
Coutlee, C. G., Huettel, S. A.
(2012) The functional neuroanatomy of decision making: Prefrontal control of thought and action. Brain Research, 1428C1, 3–12. CrossrefGoogle Scholar
De Benni, R., Pazzaglia, F., Gyselinck, V., Meneghetti, C.
(2005) Visuospatial working memory and mental representation of spatial descriptions. European Journal of Cognitive Psychology, 171, 77–95. CrossrefGoogle Scholar
Fadiga, L., Craighero, L., D’Ausilio, A.
(2009) Broca’s area in language, action, and music. Annual New York Academy of Sciences, 11691, 448–458. CrossrefGoogle Scholar
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, 1111, 2331–2336. CrossrefGoogle Scholar
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, 421, 499–502. CrossrefGoogle Scholar
Gathercole, S. E., Baddeley, A. D.
(2014) Working Memory and Language: Essays in Cognitive Psychology. New York: Psychology Press. CrossrefGoogle Scholar
Goldman-Rakic, P. S.
(1996) Regional and cellular fractionation of working memory. Proceedings of the National Academy of Sciences, 931, 13473–13480. CrossrefGoogle Scholar
Greenfield, P. M.
(1991) Language, tools and brain: The ontogeny and phylogeny of hierarchically organized sequential behavior. Behavioral and Brain Sciences, 141, 531–595. CrossrefGoogle Scholar
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, 181, 928–937. CrossrefGoogle Scholar
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, 1031, 10023–10028. CrossrefGoogle Scholar
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, 2701, 13–16. CrossrefGoogle Scholar
Jönsson, F. U., Møller, P., Olsson, M. J.
(2011) Olfactory working memory: Effects of verbalization on the 2-back test. Memory & Cognition, 391, 1023–1032. CrossrefGoogle Scholar
Just, M. A., Carpenter, P. A.
(1992) A capacity theory of comprehension: Individual differences in working memory. Psychological Review, 991, 122–149. CrossrefGoogle Scholar
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, 211, 307–317. CrossrefGoogle Scholar
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, 361, 4492–4505. Quantity, not quality: The relationship between fluid intelligence and working memory capacity. Psychonomic Bulletin & Review, 171, 673–679.Google Scholar
Lara, A. H., Kennerley, S. W., Wallis, J. D.
(2009) Encoding of gustatory working memory by orbitofrontal neurons. The Journal of Neuroscience, 291, 765–774. CrossrefGoogle Scholar
Lehnert, G., Zimmer, H. D.
(2008) Modality and domain specific components in auditory and visual working memory tasks. Cognitive Process, 91, 53–61. CrossrefGoogle Scholar
Mahaney, R. A.
(2014) Exploring the complexity and structure of Acheulean in relation to natural language. PaleoAnthropology 20141, 586–606.Google Scholar
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, 261, 29–38. CrossrefGoogle Scholar
Nie, Q. -Y., Müller, H. J., Conci, M.
(2017) Hierarchical organization in visual working memory: From global ensemble to individual object structure. Cognition 1591, 85–96. CrossrefGoogle Scholar
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, 51, 1–14. CrossrefGoogle Scholar
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, 251, 211–225.Google Scholar
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, 11, 1–8. CrossrefGoogle Scholar
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, 11, 161–171. CrossrefGoogle Scholar
Romanski, L. M., Goldman-Rakic, P. S.
(2002) An auditory domain in primate prefrontal cortex. Nature Neuroscience, 51, 15–16. CrossrefGoogle Scholar
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
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, 331, 189–196. CrossrefGoogle Scholar
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, 3851, 333–336. CrossrefGoogle Scholar
Shipton, C.
(2010) Imitation and shared intentionality in the Acheulean. Cambridge Archaeologicial Journal, 201, 197–210. CrossrefGoogle Scholar
Stout, D.
(2018) Archaeology and language evolution: From skilled action to meaningful interaction. Interaction Studies.Google Scholar
Stout, D., Hecht, E.
(2015) Neuroarchaeology. In E. Bruner (Ed.), vol. 31: Human Paleoneurology (pp. 145–175). New York: Springer International Publishing.Google Scholar
Stout, D. Hecht, E., Khreisheh, N., Bradley, B., Chaminade, T.
(2015) Cognitive demands of Lower Paleolithic toolmaking. PloS ONE, 101, e0121804. CrossrefGoogle Scholar
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, 3631, 1939–1949. CrossrefGoogle Scholar
Toth, N.
(1985) The Oldowan reassessed: A close look at early stone artifacts. Journal of Archaeological Science, 121, 101–120. CrossrefGoogle Scholar
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. CrossrefGoogle Scholar
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, 541, 577–593. CrossrefGoogle Scholar
Wadley, L.
(2010) Compound-adhesive manufacture as a behavioral proxy for complex cognition in the Middle Stone Age. Current Anthropology, 511, S111–S119. CrossrefGoogle Scholar
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, 1191, 159–179. CrossrefGoogle Scholar
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, 1471, 204–218. CrossrefGoogle Scholar
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, 1061, 86–100. CrossrefGoogle Scholar
Whittaker, J. C.
(1994) Flintknapping: Making and Understanding Stone Tools. Austin: University of Texas Press.Google Scholar
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, 691, 199–207.Google Scholar
Wright, R. V. S.
(1972) Imitative learning of a flaked stone technology–The case of an orangutan. The Australian Journal of Anthropology, 81, 296–306. CrossrefGoogle Scholar
Wynn, T.
(1979) The intelligence of later Acheulean hominids. Man, 141, 371–391. CrossrefGoogle Scholar
Wynn, T., Coolidge, F. L.
(2010) Beyond symbolism and language: An introduction to Supplement 1, Working Memory. Current Anthropology, 51(S1), S5–S16. CrossrefGoogle Scholar
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