Letter | Published:

Fluid intelligence is supported by the multiple-demand system not the language system

Nature Human Behaviourvolume 2pages200204 (2018) | Download Citation

Abstract

A set of frontoparietal brain regions—the multiple-demand (MD) system1,2—has been linked to fluid intelligence in brain imaging3,4 and in studies of patients with brain damage5,6,7. For example, the amount of damage to frontal or parietal, but not temporal, cortices predicts fluid intelligence deficit5. However, frontal and parietal lobes are structurally8 and functionally9,10 heterogeneous. They contain domain-general regions that respond across diverse tasks11,12, but also specialized regions that respond selectively during language processing13. Since language may be critical for complex thought14,15,16,17,18,19,20,21,22,23,24 (compare with refs 25,26), intelligence loss following damage to the frontoparietal cortex could have important contributions from damage to language-selective regions. To evaluate the relative contributions of MD versus language-selective regions, we employed large functional magnetic resonance imaging datasets to construct probabilistic maps of the two systems. We used these maps to weigh the volume of lesion (in each of 80 patients) falling within each system. MD-weighted, but not language-weighted, lesion volumes predicted fluid intelligence deficit (with the opposite pattern observed for verbal fluency), indicating that fluid intelligence is specifically tied to the MD system, and undermining claims that language is at the core of complex thought.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.

References

  1. 1.

    Duncan, J. The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn. Sci. 14, 172–179 (2010).

  2. 2.

    Duncan, J. The structure of cognition: attentional episodes in mind and brain. Neuron 80, 35–50 (2013).

  3. 3.

    Gray, J. R., Chabris, C. F. & Braver, T. S. Neural mechanisms of general fluid intelligence. Nat. Neurosci. 6, 316–322 (2003).

  4. 4.

    Duncan, J. et al. A neural basis for general intelligence. Science 289, 457–460 (2000).

  5. 5.

    Woolgar, A. et al. Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex. Proc. Natl Acad. Sci. USA 107, 14899–14902 (2010).

  6. 6.

    Duncan, J., Burgess, P. & Emslie, H. Fluid intelligence after frontal lobe lesions. Neuropsychologia 33, 261–268 (1995).

  7. 7.

    Glascher, J. et al. Distributed neural system for general intelligence revealed by lesion mapping. Proc. Natl Acad. Sci. USA 107, 4705–4709 (2010).

  8. 8.

    Amunts, K. et al. Brocaas region: novel organizational principles and multiple receptor mapping. PLoS Biol. 8, e1000489 (2010).

  9. 9.

    Fedorenko, E., Duncan, J. & Kanwisher, N. Language-selective and domain-general regions lie side by side within Broca’s area. Curr. Biol. 22, 2059–2062 (2012).

  10. 10.

    Wise, R. J. et al. Separate neural subsystems within ‘Wernicke’s area’. Brain 124, 83–95 (2001).

  11. 11.

    Duncan, J. & Owen, A. M. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 23, 475–483 (2000).

  12. 12.

    Fedorenko, E., Duncan, J. & Kanwisher, N. Broad domain generality in focal regions of frontal and parietal cortex. Proc. Natl Acad. Sci. USA 110, 16616–16621 (2013).

  13. 13.

    Fedorenko, E., Behr, M. K. & Kanwisher, N. Functional specificity for high-level linguistic processing in the human brain. Proc. Natl Acad. Sci. USA 108, 16428–16433 (2011).

  14. 14.

    Carruthers, P. The cognitive functions of language. Behav. Brain Sci. 25, 657–674 (2002).

  15. 15.

    Hinzen, W. The philosophical significance of Universal Grammar. Lang. Sci. 34, 635–649 (2012).

  16. 16.

    Hinzen, W. Narrow syntax and the language of thought. Philos. Psychol. 26, 1–23 (2013).

  17. 17.

    Dennett, D. C. in Language and Thought (ed. Burri, A.) Ch. 3 (de Gruyter, Berlin, 1997).

  18. 18.

    Bickerton, D. Language and Human Behavior (Univ. Washington Press, Seattle, WA, 1995).

  19. 19.

    Gentner, D. in Language in Mind: Advances in the Study of Language and Thought (eds Gentner, D. & Goldin-Meadow, S.) Ch. 8 (MIT Press, Cambridge, MA, 2003).

  20. 20.

    Kuczaj, S. A. & Hendry, J. L. in Language in Mind: Advances in the Study of Language and Thought (eds Gentner, D. & Goldin-Meadow, S.) Ch. 9 (MIT Press, Cambridge, MA, 2003).

  21. 21.

    Bermúdez, J. L. Thinking without Words (Oxford Univ. Press, Oxford, 2003).

  22. 22.

    Baldo, J. V., Bunge, S. A., Wilson, S. M. & Dronkers, N. F. Is relational reasoning dependent on language? A voxel-based lesion symptom mapping study. Brain Lang. 113, 59–64 (2010).

  23. 23.

    Baldo, J. V., Dronkers, N. F., Wilkins, D., Ludy, C., Raskin, P. & Kim, J. Is problem solving dependent on language? Brain Lang. 92, 240–250 (2005).

  24. 24.

    Baldo, J. V., Paulraj, S. R., Curran, B. C. & Dronkers, N. F. Impaired reasoning and problem-solving in individuals with language impairment due to aphasia or language delay. Front. Psychol. 6, 1523 (2015).

  25. 25.

    Fedorenko, E. & Varley, R. Language and thought are not the same thing: evidence from neuroimaging and neurological patients. Ann. NY Acad. Sci. 1369, 132–153 (2016).

  26. 26.

    Varley, R. Reason without much language. Lang. Sci. 46, 232–244 (2014).

  27. 27.

    Tomasello, M. & Herrmann, E. Ape and human cognition: what’s the difference? Curr. Dir. Psychol. Sci. 19, 3–8 (2010).

  28. 28.

    Sherwood, C. C., Subiaul, F. & Zawidzki, T. W. A natural history of the human mind: tracing evolutionary changes in brain and cognition. J. Anat. 212, 426–454 (2008).

  29. 29.

    Premack, D. Human and animal cognition: continuity and discontinuity. Proc. Natl Acad. Sci. USA 104, 13861–13867 (2007).

  30. 30.

    Penn, D. C., Holyoak, K. J. & Povinelli, D. J. Darwin’s mistake: explaining the discontinuity between human and nonhuman minds. Behav. Brain Sci. 31, 109–130 (2008).

  31. 31.

    Broca, P. Remarks on the seat of the faculty of articulated language, following an observation of aphemia (loss of speech). Bull. De. la Société Anat. 6, 330–357 (1861).

  32. 32.

    Monti, M. M., Parsons, L. M. & Osherson, D. N. Thought beyond language: neural dissociation of algebra and natural language. Psychol. Sci. 23, 914–922 (2012).

  33. 33.

    Woolgar, A., Jackson, J. & Duncan, J. Coding of visual, auditory, rule, and response information in the brain: 10 years of multivoxel pattern analysis. J. Cogn. Neurosci. 28, 1433–1454 (2016).

  34. 34.

    Yeo, B.T. et al. Functional specialization and flexibility in human association cortex. Cereb. Cortex 25, 3654–3672 (2014).

  35. 35.

    Niendam, T. A. et al. Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn. Affect Behav. Neurosci 12, 241–268 (2012).

  36. 36.

    Dosenbach, N. U. et al. A core system for the implementation of task sets. Neuron 50, 799–812 (2006).

  37. 37.

    Naghavi, H. R. & Nyberg, L. Common fronto-parietal activity in attention, memory, and consciousness: shared demands on integration? Conscious. Cogn. 14, 390–425 (2005).

  38. 38.

    Owen, A. M., McMillan, K. M., Laird, A. R. & Bullmore, E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum. Brain Mapp. 25, 46–59 (2005).

  39. 39.

    Cole, M. W. & Schneider, W. The cognitive control network: integrated cortical regions with dissociable functions. NeuroImage 37, 343–360 (2007).

  40. 40.

    Dosenbach, N. U., Fair, D. A., Cohen, A. L., Schlaggar, B. L. & Petersen, S. E. A dual-networks architecture of top-down control. Trends Cogn. Sci. 12, 99–105 (2008).

  41. 41.

    Power, J. D. & Petersen, S. E. Control-related systems in the human brain. Curr. Opin. Neurobiol. 23, 223–228 (2013).

  42. 42.

    Corbetta, M. & Shulman, G. L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).

  43. 43.

    Miller, E. K. & Cohen, J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

  44. 44.

    Gray, J. R. & Thompson, P. M. Neurobiology of intelligence: science and ethics. Nat. Rev. 5, 471–482 (2004).

  45. 45.

    Fedorenko, E., Hsieh, P. J., Nieto-Castanon, A., Whitfield-Gabrieli, S. & Kanwisher, N. New method for fMRI investigations of language: defining ROIs functionally in individual subjects. J. Neurophysiol. 104, 1177–1194 (2010).

  46. 46.

    Blank, I., Kanwisher, N. & Fedorenko, E. A functional dissociation between language and multiple-demand systems revealed in patterns of BOLD signal fluctuations. J. Neurophysiol. 112, 1105–1118 (2014).

  47. 47.

    Mahowald, K. & Fedorenko, E. Reliable individual-level neural markers of high-level language processing: a necessary precursor for relating neural variability to behavioral and genetic variability. NeuroImage 139, 74–93 (2016).

  48. 48.

    Measuring Intelligence with the Culture Fair Tests (Institute for Personality and Ability Testing, Champaign, IL, 1973).

  49. 49.

    Ekstrom, R. B., French, J. W., Harmon, H. H. & Derman, D. ETS Kit of Factor-Referenced Cognitive Tests (Educational Testing Service, Princeton, NJ, 1976).

  50. 50.

    Nelson, H. E. & Willison, J. R. The Revised National Adult Reading Test–Test Manual. (NFER-Nelson: Windsor, 1991).

  51. 51.

    Burin, D. I., Jorge, R. E., Arizaga, R. A. & Paulsen, J. S. Estimation of premorbid intelligence: the word accentuation test—Buenos Aires version. J. Clin. Exp. Neuropsychol. 22, 677–685 (2000).

  52. 52.

    Benton, A. L. & Hamsher, K. Multilingual Aphasia Examination. (Univ. Iowa Press: Iowa City, IA, 1976).

  53. 53.

    Roca, M. et al. Executive function and fluid intelligence after frontal lobe lesions. Brain 133, 234–247 (2010).

  54. 54.

    Hartshorne, J. K. & Germine, L. T. When does cognitive functioning peak? The asynchronous rise and fall of different cognitive abilities across the life span. Psychol. Sci. 26, 433–443 (2015).

  55. 55.

    Vernon, M. Relationship of language to the thinking process. Arch. Gen. Psychiatry 16, 325–333 (1967).

  56. 56.

    Monti, M. M., Parsons, L. M. & Osherson, D. N. The boundaries of language and thought in deductive inference. Proc. Natl Acad. Sci. USA 106, 12554–12559 (2009).

  57. 57.

    de Villiers, J. in Understanding Other Minds: Perspectives from Developmental Cognitive Neuroscience 2nd edn (eds Baron-Cohen, S. et al.) 83–123 (2000).

  58. 58.

    Piaget, J. The Language and Thought of the Child (Harcourt Brace, Oxford, 1926).

  59. 59.

    Vygotskiĭ, L. S. Thought and Language (MIT Press, Cambridge, MA, 2012).

  60. 60.

    Gentner, D. & Loewenstein, J. in Language, Literacy, and Cognitive Development: the Development and Consequences of Symbolic Communication (eds Amsel, E. & Byrnes, J. P.) Ch. 4 (Lawrence Erlbaum Associates, London, 2002).

  61. 61.

    Winsler, A. & Naglieri, J. Overt and covert verbal problem-solving strategies: developmental trends in use, awareness, and relations with task performance in children aged 5 to 17. Child. Dev. 74, 659–678 (2003).

  62. 62.

    Hulley, S. B., Cummings, S. R., Browner, W. S., Grady, D. G. & Newman, T. B. Designing Clinical Research (Lippincott Williams and Wilkins, Philadelphia, PA, 2013).

  63. 63.

    Fedorenko, E. The role of domain-general cognitive control in language comprehension. Front. Psychol. 5, 335 (2014).

Download references

Acknowledgements

A.W. was supported by Australian Research Council Fellowships (Discovery Early Career Researcher Award grant no. DE120100898 and Future Fellowship grant no. FT170100105) and an Australian Research Council Discovery Project research grant (DP12102835). J.D. was supported by the Medical Research Council (United Kingdom) intramural programme (grant no. SUAG/002/RG91365). E.F. was supported by an R00 award HD 057522 from National Institute of Child Health and Human Development, and by grants ANR-11-LABX-0036 (Brain and Language Research Institute) and ANR-11-IDEX-0001-02 (A*MIDEX: Initiative d'excellence Aix-Marseille). We thank N. Dermody for help with analysis. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Affiliations

  1. Perception in Action Research Centre (PARC), Department of Cognitive Science, Faculty of Human Sciences, Macquarie University, Sydney, New South Wales, Australia

    • Alexandra Woolgar
  2. Australian Research Council Centre of Excellence in Cognition and its Disorders (CCD), Macquarie University, Sydney, New South Wales, Australia

    • Alexandra Woolgar
    •  & Facundo Manes
  3. Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK

    • John Duncan
  4. Department of Psychology, University of Oxford, Oxford, UK

    • John Duncan
  5. Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCyT), INECO Foundation, Favaloro University, Buenos Aires, Argentina

    • Facundo Manes
  6. National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina

    • Facundo Manes
  7. Department of Psychiatry, Harvard Medical School, Boston, MA, USA

    • Evelina Fedorenko
  8. Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, USA

    • Evelina Fedorenko

Authors

  1. Search for Alexandra Woolgar in:

  2. Search for John Duncan in:

  3. Search for Facundo Manes in:

  4. Search for Evelina Fedorenko in:

Contributions

E.F did the conceptualization, E.F. and A.W. did the methodology, A.W. did the formal analysis, E.F. and A.W. wrote the original draft of the paper, J.D., E.F. and A.W reviewed and edited the paper, A.W. did the visualization and E.F. and J.D. supervised. F.M. traced the patient lesions.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Alexandra Woolgar or Evelina Fedorenko.

Supplementary information

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41562-017-0282-3