Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Hierarchical cognitive control deficits following damage to the human frontal lobe

Nature Neuroscience volume 12, pages 515–522 (2009)Cite this article

Abstract

Cognitive control permits us to make decisions about abstract actions, such as whether to e-mail versus call a friend, and to select the concrete motor programs required to produce those actions, based on our goals and knowledge. The frontal lobes are necessary for cognitive control at all levels of abstraction. Recent neuroimaging data have motivated the hypothesis that the frontal lobes are organized hierarchically, such that control is supported in progressively caudal regions as decisions are made at more concrete levels of action. We found that frontal damage impaired action decisions at a level of abstraction that was dependent on lesion location (rostral lesions affected more abstract tasks, whereas caudal lesions affected more concrete tasks), in addition to impairing tasks requiring more, but not less, abstract action control. Moreover, two adjacent regions were distinguished on the basis of the level of control, consistent with previous functional magnetic resonance imaging results. These results provide direct evidence for a rostro-caudal hierarchical organization of the frontal lobes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Trial events and task analysis of the four response-selection tasks.
Figure 2: Overall performance across the four tasks.
Figure 3: Observer-independent overlap analysis.
Figure 4: Performance of dimension and feature patient groups.

Similar content being viewed by others

References

  1. Badre, D. & Wagner, A.D. Selection, integration and conflict monitoring; assessing the nature and generality of prefrontal cognitive control mechanisms. Neuron 41, 473–487 (2004).

    Article  CAS  Google Scholar 

  2. D'Esposito, M. et al. The neural basis of the central executive system of working memory. Nature 378, 279–281 (1995).

    Article  CAS  Google Scholar 

  3. D'Esposito, M., Postle, B.R. & Rypma, B. Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp. Brain Res. 133, 3–11 (2000).

    Article  CAS  Google Scholar 

  4. Duncan, J. An adaptive coding model of neural function in prefrontal cortex. Nat. Rev. Neurosci. 2, 820–829 (2001).

    Article  CAS  Google Scholar 

  5. Fuster, J.M. The Prefrontal Cortex: Anatomy, Physiology and Neuropsychology of the Frontal Lobe (Lippincott-Raven Publishers, Philadelphia, Pennsylvania, 1997).

    Google Scholar 

  6. Goldman-Rakic, P.S. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Phil. Trans. R. Soc. Lond. B 351, 1445–1453 (1996).

    Article  CAS  Google Scholar 

  7. Koechlin, E. & Summerfield, C. An information theoretical approach to prefrontal executive function. Trends Cogn. Sci. 11, 229–235 (2007).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Passingham, R.E. The Frontal Lobes and Voluntary Action. (Oxford University Press, Oxford, 1993).

    Google Scholar 

  10. Passingham, R.E. & Rowe, J.B. Dorsal prefrontal cortex: maintenance in memory or attentional selection? in Principles of Frontal Lobe Function (eds. Stuss, D.T. & Knight, RT.) 221–232 (Oxford University Press, Oxford, 2002).

    Chapter  Google Scholar 

  11. Petrides, M. Lateral prefrontal cortex: architectonic and functional organization. Phil. Trans. R. Soc. Lond. B. 360, 781–795 (2005).

    Article  Google Scholar 

  12. Shallice, T. & Burgess, P.W. Deficits in strategy application following frontal lobe damage in man. Brain 114, 727–741 (1991).

    Article  Google Scholar 

  13. Smith, E.E. & Jonides, J. Storage and executive processes in the frontal lobes. Science 283, 1657–1661 (1999).

    Article  CAS  Google Scholar 

  14. Stuss, D.T. & Benson, D.F. The frontal lobes and control of cognition and memory. in The Frontal Lobes Revisited (ed. Perecman, E.) 141–158 (The IRBN Press, New York, 1987).

    Google Scholar 

  15. Bunge, S.A. How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn. Affect. Behav. Neurosci. 4, 564–579 (2004).

    Article  Google Scholar 

  16. Carter, C.S. et al. Anterior cingulate cortex, error detection and the on-line monitoring of performance. Science 280, 747–749 (1998).

    Article  CAS  Google Scholar 

  17. O'Reilly, R.C. & Frank, M.J. Making working memory work: a computational model of learning in the prefrontal cortex and basal ganglia. Neural Comput. 18, 283–328 (2006).

    Article  Google Scholar 

  18. Courtney, S.M., Roth, J.K. & Sala, J.B. A hierarchical biased-competition model of domain-dependent working memory maintenance and executive control. in The Cognitive Neuroscience of Working Memory (eds. Osaka, N., Logie, R. & D'Esposito, M.) 369–383 (Oxford University Press, Oxford, 2007).

    Chapter  Google Scholar 

  19. Cohen, J.D., Dunbar, K. & McClelland, J.L. On the control of automatic processes: a parallel distributed processing account of the Stroop effect. Psychol. Rev. 97, 332–361 (1990).

    Article  CAS  Google Scholar 

  20. Cohen, J.D. & Servan-Schreiber, D. Context, cortex and dopamine: a connectionist approach to behavior and biology in schizophrenia. Psychol. Rev. 99, 45–77 (1992).

    Article  CAS  Google Scholar 

  21. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  Google Scholar 

  22. MacDonald, A.W. III, Cohen, J.D., Stenger, V.A. & Carter, C.S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288, 1835–1838 (2000).

    Article  CAS  Google Scholar 

  23. Wallis, J.D., Anderson, K.C. & Miller, E.K. Single neurons in prefrontal cortex encode abstract rules. Nature 411, 953–956 (2001).

    Article  CAS  Google Scholar 

  24. Botvinick, M.M. Multilevel structure in behaviour and in the brain: a model of Fuster's hierarchy. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1615–1626 (2007).

    Article  Google Scholar 

  25. Botvinick, M.M. Hierarchical models of behavior and prefrontal function. Trends Cogn. Sci. 12, 201–208 (2008).

    Article  Google Scholar 

  26. O'Reilly, R.C., Noelle, D.C., Braver, T.S. & Cohen, J.D. Prefrontal cortex and dynamic categorization tasks: representational organization and neuromodulatory control. Cereb. Cortex 12, 246–257 (2002).

    Article  Google Scholar 

  27. Hazy, T.E., Frank, M.J. & O'Reilly, R.C. Towards an executive without a homunculus: computational models of the prefrontal cortex/basal ganglia system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1601–1613 (2007).

    Article  Google Scholar 

  28. Badre, D. & D'Esposito, M. Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J. Cogn. Neurosci. 19, 2082–2099 (2007).

    Article  Google Scholar 

  29. Christoff, K. & Keramatian, K. Abstraction of mental representations: theoretical considerations and neuroscientific evidence. in Perspectives on Rule-Guided Behavior (eds. Bunge, S.A. & Wallis, J.D.) (Oxford University Press, New York, 2007).

    Google Scholar 

  30. Koechlin, E. & Jubault, T. Broca's area and the hierarchical organization of human behavior. Neuron 50, 963–974 (2006).

    Article  CAS  Google Scholar 

  31. Koechlin, E., Ody, C. & Kouneiher, F. The architecture of cognitive control in the human prefrontal cortex. Science 302, 1181–1185 (2003).

    Article  CAS  Google Scholar 

  32. Badre, D. Cognitive control, hierarchy and the rostro-caudal organization of the frontal lobes. Trends Cogn. Sci. 12, 193–200 (2008).

    Article  Google Scholar 

  33. Buckner, R.L. Functional-anatomic correlates of control processes in memory. J. Neurosci. 23, 3999–4004 (2003).

    Article  CAS  Google Scholar 

  34. Fuster, J.M. The prefrontal cortex—an update: time is of the essence. Neuron 30, 319–333 (2001).

    Article  CAS  Google Scholar 

  35. Rowe, J.B. et al. Is the prefrontal cortex necessary for establishing cognitive sets? J. Neurosci. 27, 13303–13310 (2007).

    Article  CAS  Google Scholar 

  36. Sakai, K. & Passingham, R.E. Prefrontal interactions reflect future task operations. Nat. Neurosci. 6, 75–81 (2003).

    Article  CAS  Google Scholar 

  37. Sakai, K. & Passingham, R.E. Prefrontal set activity predicts rule-specific neural processing during subsequent cognitive performance. J. Neurosci. 26, 1211–1218 (2006).

    Article  CAS  Google Scholar 

  38. Barbas, H. & Pandya, D.N. Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J. Comp. Neurol. 256, 211–228 (1987).

    Article  CAS  Google Scholar 

  39. Petrides, M. & Pandya, D.N. Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. J. Neurosci. 27, 11573–11586 (2007).

    Article  CAS  Google Scholar 

  40. Christoff, K. & Gabrieli, J.D.E. The frontopolar cortex and human cognition: evidence for a rostrocaudal hierarchal organization within the human prefrontal cortex. Psychobiology 28, 168–186 (2000).

    Google Scholar 

  41. Christoff, K., Ream, J.M., Geddes, L.P.T. & Gabrieli, J.D.E. Evaluating self-generated information: anterior prefrontal contributions to human cognition. Behav. Neurosci. 117, 1161–1168 (2003).

    Article  Google Scholar 

  42. Halsband, U. & Passingham, R.E. Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis). Behav. Brain Res. 18, 269–277 (1985).

    Article  CAS  Google Scholar 

  43. Hampshire, A., Duncan, J. & Owen, A.M. Selective tuning of the blood oxygenation level-dependent response during simple target detection dissociates human frontoparietal subregions. J. Neurosci. 27, 6219–6223 (2007).

    Article  CAS  Google Scholar 

  44. Hampshire, A., Thompson, R., Duncan, J. & Owen, A.M. The target selective neural response–similarity, ambiguity, and learning effects. PLoS ONE 3, e2520 (2008).

    Article  Google Scholar 

  45. Heekeren, H.R., Marrett, S., Bandettini, P.A. & Ungerleider, L.G. A general mechanism for perceptual decision-making in the human brain. Nature 431, 859–862 (2004).

    Article  CAS  Google Scholar 

  46. Petrides, M., Alivisatos, B., Evans, A.C. & Meyer, E. Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proc. Natl. Acad. Sci. USA 90, 873–877 (1993).

    Article  CAS  Google Scholar 

  47. Rushworth, M.F. et al. Attentional selection and action selection in the ventral and orbital prefrontal cortex. J. Neurosci. 25, 11628–11636 (2005).

    Article  CAS  Google Scholar 

  48. Dreher, J.C., Koechlin, E., Tierney, M. & Grafman, J. Damage to the fronto-polar cortex is associated with impaired multitasking. PLoS ONE 3, e3227 (2008).

    Article  Google Scholar 

  49. Thompson-Schill, S.L. et al. Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proc. Natl. Acad. Sci. USA 95, 15855–15860 (1998).

    Article  CAS  Google Scholar 

  50. Jeffreys, H. Theory of Probability (Clarendon Press, Oxford, 1961).

    Google Scholar 

Download references

Acknowledgements

We are grateful to R.T. Knight and D. Scabini for their help with patient recruitment and lesion characterization. We also would like to thank W. Heindel and A. Kayser for their input on revisions of this manuscript. This work was supported by the US National Institutes of Health (grants MH63901 and NS40813), the Veterans Administration Research Service and a National Research Service Award (F32 NS053337).

Author information

Authors and Affiliations

  1. Department of Cognitive and Linguistic Sciences, Brown University, Providence, Rhode Island, USA

    David Badre

  2. Department of Psychology, Brown University, Providence, Rhode Island, USA

    David Badre

  3. Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California, USA

    Joshua Hoffman, Jeffrey W Cooney & Mark D'Esposito

  4. Department of Psychology, University of California, Berkeley, Berkeley, California, USA

    Mark D'Esposito

Authors
  1. David Badre
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joshua Hoffman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey W Cooney
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark D'Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David Badre.

Supplementary information

Supplementary Text and Figures

Supplementary Figure 1 and Supplementary Table 1 (PDF 240 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Badre, D., Hoffman, J., Cooney, J. et al. Hierarchical cognitive control deficits following damage to the human frontal lobe. Nat Neurosci 12, 515–522 (2009). https://doi.org/10.1038/nn.2277

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2277

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing