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Article published In: Evolutionary Linguistic Theory
Vol. 1:2 (2019) ► pp.162–174

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The anatomical foundations of language dominance

A selective review of the available data

 | University School for Advanced Studies IUSS | IRCCS Mondino Foundation
Published online: 24 January 2020
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https://doi.org/10.1075/elt.00009.cap
Abstract
The evidence about asymmetries between the two hemispheres in human and non-human species may contribute to the current debate about language evolution. Here I present a selective review of the available data, limited to the macroscopic and microscopic anatomy of the main language areas. Both post-mortem and imaging studies confirm the presence of a leftward asymmetry in the Planum Temporale (PT) region in humans; in the case of Broca’s area the evidence is less consistent. The data about non-human primates also support the presence of a leftward asymmetry of the PT area in apes and monkeys. Studies on large populations, combining quantitative structural imaging of cortex and white matter, functional imaging measures during language tasks, and detailed assessments of handedness are needed to assess the relevance of comparative brain anatomy data to the investigation of language evolution.
Article outline
  • 1.Introduction
  • 2.Hemispheric asymmetries in humans: Planum Temporale
  • 3.Broca’s area
  • 4.White matter asymmetries and connectomics
  • 5.Conclusions
  • References
References (46)
References
Aboitiz, F. (2012). Gestures, vocalizations, and memory in language origins. Frontiers in Evolutionary Neuroscience, 41, Article 2. Google Scholar logo with link to Google Scholar
Allendorfer, J. B., Hernando, K. A., Hossain, S., Nenert, R., Holland, S. K., Szaflarski, J. P. (2016). Arcuate fasciculus asymmetry has a hand in language function but not handedness. Human brain mapping, 37(9), 3297–3309. Google Scholar logo with link to Google Scholar
Amunts, K., Lenzen, M., Friederici, A. D., Schleicher, A., Morosan, P., Palomero-Gallagher, N., Zilles, K. (2010). Broca’s region: novel organizational principles and multiple receptor mapping. PLoS Biol, 8(9). Google Scholar logo with link to Google Scholar
Amunts, K., Schleicher, A., Burgel, U., Mohlberg, H., Uylings, H. B., Zilles, K. (1999). Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol, 412(2), 319–341. Google Scholar logo with link to Google Scholar
Amunts, K., Schleicher, A., Ditterich, A., Zilles, K. (2003). Broca’s region: cytoarchitectonic asymmetry and developmental changes. J Comp Neurol, 465(1), 72–89. Google Scholar logo with link to Google Scholar
Bernard, F., Zemmoura, I., Ter Minassian, A., Lemée, J.-M., Menei, P. (2019). Anatomical variability of the arcuate fasciculus: a systematical review. Surgical and Radiologic Anatomy, 1–12.Google Scholar logo with link to Google Scholar
Berwick, R. C., Chomsky, N. (2016). Why only us: Language and evolution: MIT press. Google Scholar logo with link to Google Scholar
Broca, P. (1865). Sur la siège de la faculté de langage articulé. Bulletin de la Societè de Anthropologie, 61, 337–398.Google Scholar logo with link to Google Scholar
Cantalupo, C., Hopkins, W. D. (2001). Asymmetric Broca’s area in great apes. Nature, 414(6863), 505. Google Scholar logo with link to Google Scholar
Cappa, S. F. (2015). Disorders of Language. In A. W. Toga (Ed.), Brain Mapping: An Encyclopedic Reference. Vol. 3. Amsterdam: Elsevier, 1089–1093. Google Scholar logo with link to Google Scholar
Catani, M., Jones, D. K., ffytche, D. H. (2005). Perisylvian language networks of the human brain. Ann Neurol, 57(1), 8–16. Google Scholar logo with link to Google Scholar
Chance, S. A., Casanova, M. F., Switala, A. E., Crow, T. J. (2006). Minicolumnar structure in Heschl’s gyrus and planum temporale: Asymmetries in relation to sex and callosal fiber number. Neuroscience, 143(4), 1041–1050. Google Scholar logo with link to Google Scholar
de Schotten, M. T., Dell’Acqua, F., Valabregue, R., Catani, M. (2012). Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex, 48(1), 82–96. Google Scholar logo with link to Google Scholar
Dick, A. S., & Tremblay, P. (2012). Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain, 135(12), 3529–3550. Google Scholar logo with link to Google Scholar
Economo, C. von, Horn, L. (1930). Über Windungsrelief, Maße und Rindenarchitektonik der Supratemporalfläche, ihre individuellen und ihre Seitenunterschiede. Zeitschrift für die gesamte Neurologie und Psychiatrie, 1301, 678–757. Google Scholar logo with link to Google Scholar
Eichert, N., Verhagen, L., Folloni, D., Jbabdi, S., Khrapitchev, A. A., Sibson, N. R., Mars, R. B. (2019). What is special about the human arcuate fasciculus? Lateralization, projections, and expansion. Cortex, 1181, 107–115. Google Scholar logo with link to Google Scholar
Falzi, G., Perrone, P., Vignolo, L. A. (1982). Right-left asymmetry in anterior speech region. Arch Neurol, 39(4), 239–240. Google Scholar logo with link to Google Scholar
Frey, S., Campbell, J. S. W., Pike, G. B., Petrides, M. (2008). Dissociating the human language pathways with high angular resolution diffusion fiber tractography. J. Neurosci. 281, 11435–11444. Google Scholar logo with link to Google Scholar
Geschwind, N., Levitsky, W. (1968). Human brain: left-right asymmetries in temporal speech region. Science, 161(3837), 186–187. Google Scholar logo with link to Google Scholar
Gough, P. M., Connally, E. L., Howell, P., Ward, D., Chesters, J., & Watkins, K. E. (2018). Planum temporale asymmetry in people who stutter. Journal of fluency disorders, 551, 94–105. Google Scholar logo with link to Google Scholar
Hauser, M. D., Yang, C., Berwick, R. C., Tattersall, I., Ryan, M. J., Watumull, J., Lewontin, R. C. (2014). The mystery of language evolution. Front Psychol, 51, 401. Google Scholar logo with link to Google Scholar
Hecht, E. E., Gutman, D. A., Bradley, B. A., Preuss, T. M., Stout, D. (2015). Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans. Neuroimage, 1081, 124–137. Google Scholar logo with link to Google Scholar
Hopkins, W. D., Nir, T. M. (2010). Planum temporale surface area and grey matter asymmetries in chimpanzees (Pan troglodytes): the effect of handedness and comparison with findings in humans. Behav Brain Res, 208(2), 436–443. Google Scholar logo with link to Google Scholar
Keller, S. S., Crow, T., Foundas, A., Amunts, K., Roberts, N. (2009). Broca’s area: nomenclature, anatomy, typology and asymmetry. Brain Lang, 109(1), 29–48. Google Scholar logo with link to Google Scholar
Kelly, K., Uddin, L. Q., Shehzad, Z., Margulies, D. S., Castellanos, F. X., Milham, M. P., Petrides, M. (2010). Broca’s region: linking human brain functional connectivity data and nonhuman primate tracing anatomy studies. Eur. J. Neurosci. 321, 383–398. Google Scholar logo with link to Google Scholar
Kong, X.-Z., Mathias, S. R., Guadalupe, T., Glahn, D. C., Franke, B., Crivello, F., Francks, C. (2018). Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium. Proceedings of the National Academy of Sciences, 115(22), E5154–E5163. Google Scholar logo with link to Google Scholar
Mantini, D., Corbetta, M., Romani, G. L., Orban, G. A., Vanduffel, W. (2013). Evolutionarily novel functional networks in the human brain? Journal of Neuroscience, 33(8), 3259–3275. Google Scholar logo with link to Google Scholar
Marie, D., Roth, M., Lacoste, R., Nazarian, B., Bertello, A., Anton, J.-L., Meguerditchian, A. (2017). Left brain asymmetry of the planum temporale in a nonhominid primate: Redefining the origin of brain specialization for language. Cerebral Cortex, 28(5), 1808–1815. Google Scholar logo with link to Google Scholar
Mars, R. B., Eichert, N., Jbabdi, S., Verhagen, L., & Rushworth, M. F. (2018). Connectivity and the search for specializations in the language-capable brain. Current Opinion in Behavioral Sciences, 211, 19–26. Google Scholar logo with link to Google Scholar
Martino, J., Hamer, P. C. D. W., Berger, M. S., Lawton, M. T., Arnold, C. M., de Lucas, E. M., Duffau, H. (2013). Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Structure and Function, 218(1), 105–121. Google Scholar logo with link to Google Scholar
Neubert, F.-X., Mars, R. B., Thomas, A. G., Sallet, J., Rushworth, M. F. (2014). Comparison of human ventral frontal cortex areas for cognitive control and language with areas in monkey frontal cortex. Neuron, 81(3), 700–713. Google Scholar logo with link to Google Scholar
Ocklenburg, S., Friedrich, P., Fraenz, C., Schluter, C., Beste, C., Gunturkun, O., Genc, E. (2018). Neurite architecture of the planum temporale predicts neurophysiological processing of auditory speech. Sci Adv, 4(7), eaar6830. Google Scholar logo with link to Google Scholar
Parker, G. J., Luzzi, S., Alexander, D. C., Wheeler-Kingshott, C. A., Ciccarelli, O., Lambon Ralph, M. A. (2005). Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage, 24(3), 656–666. Google Scholar logo with link to Google Scholar
Petrides, M., Pandya, D. N. (2009). Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol. 7, e1000170. Google Scholar logo with link to Google Scholar
Plessen, K. J., Hugdahl, K., Bansal, R., Hao, X., Peterson, B. S. (2014). Sex, age, and cognitive correlates of asymmetries in thickness of the cortical mantle across the life span. Journal of Neuroscience, 34(18), 6294–6302. Google Scholar logo with link to Google Scholar
Poldrack, R. A. (2011). Inferring mental states from neuroimaging data: from reverse inference to large-scale decoding. Neuron, 72(5), 692–697. Google Scholar logo with link to Google Scholar
Rilling, J. K., Glasser, M. F., Preuss, T. M., Ma, X., Zhao, T., Hu, X., Behrens, T. E. (2008). The evolution of the arcuate fasciculus revealed with comparative DTI. Nature neuroscience, 11(4), 426. Google Scholar logo with link to Google Scholar
Schenker, N. M., Buxhoeveden, D. P., Blackmon, W. L., Amunts, K., Zilles, K., Semendeferi, K. (2008). A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca’s area in humans and great apes. J Comp Neurol, 510(1), 117–128. Google Scholar logo with link to Google Scholar
Schenker, N. M., Hopkins, W. D., Spocter, M. A., Garrison, A. R., Stimpson, C. D., Erwin, J. M., Sherwood, C. C. (2010). Broca’s area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb Cortex, 20(3), 730–742. Google Scholar logo with link to Google Scholar
Schmitz, J., Gunturkun, O., Ocklenburg, S. (2019). Building an asymmetrical brain-the molecular perspective. Frontiers in psychology, 101, 982. Google Scholar logo with link to Google Scholar
Shapleske, J., Rossell, S. L., Woodruff, P. W., David, A. S. (1999). The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Brain Res Rev, 29(1), 26–49. Google Scholar logo with link to Google Scholar
Taglialatela, J. P., Russell, J. L., Schaeffer, J. A., Hopkins, W. D. (2008). Communicative signaling activates ‘Broca’s’ homolog in chimpanzees. Curr Biol, 18(5), 343–348. Google Scholar logo with link to Google Scholar
Toga, A. W., Thompson, P. M. (2003). Mapping brain asymmetry. Nature Reviews Neuroscience, 41, 37. Google Scholar logo with link to Google Scholar
Tzourio-Mazoyer, N., Mazoyer, B. (2017). Variations of planum temporale asymmetries with Heschl’s Gyri duplications and association with cognitive abilities: MRI investigation of 428 healthy volunteers. Brain Struct Funct, 222(6), 2711–2726. Google Scholar logo with link to Google Scholar
Uylings, H. B., Jacobsen, A. M., Zilles, K., Amunts, K. (2006). Left-right asymmetry in volume and number of neurons in adult Broca’s area. Cortex, 42(4), 652–658. Google Scholar logo with link to Google Scholar
Zilles, K., & Amunts, K. (2018). Cytoarchitectonic and receptorarchitectonic organization in Broca’s region and surrounding cortex. Current opinion in behavioral sciences, 211, 93–105. Google Scholar logo with link to Google Scholar
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