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.

  • Letter
  • Published:

Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation

Nature volume 488, pages 218–221 (2012)Cite this article

Abstract

The ability to optimize behavioural performance when confronted with continuously evolving environmental demands is a key element of human cognition. The dorsal anterior cingulate cortex (dACC), which lies on the medial surface of the frontal lobes, is important in regulating cognitive control. Hypotheses about its function include guiding reward-based decision making1, monitoring for conflict between competing responses2 and predicting task difficulty3. Precise mechanisms of dACC function remain unknown, however, because of the limited number of human neurophysiological studies. Here we use functional imaging and human single-neuron recordings to show that the firing of individual dACC neurons encodes current and recent cognitive load. We demonstrate that the modulation of current dACC activity by previous activity produces a behavioural adaptation that accelerates reactions to cues of similar difficulty to previous ones, and retards reactions to cues of different difficulty. Furthermore, this conflict adaptation, or Gratton effect2,4, is abolished after surgically targeted ablation of the dACC. Our results demonstrate that the dACC provides a continuously updated prediction of expected cognitive demand to optimize future behavioural responses. In situations with stable cognitive demands, this signal promotes efficiency by hastening responses, but in situations with changing demands it engenders accuracy by delaying responses.

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: Behavioural task, fMRI and subject performance.
Figure 2: Individual and population neuronal responses.
Figure 3: Effect of previous trial on dACC firing and RT.
Figure 4: Abolition of behavioural adaptation after a targeted dACC lesion.

Similar content being viewed by others

References

  1. Williams, Z. M., Bush, G., Rauch, S. L., Cosgrove, G. R. & Eskandar, E. N. Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nature Neurosci. 7, 1370–1375 (2004)

    Article  CAS  Google Scholar 

  2. Botvinick, M., Nystrom, L. E., Fissell, K., Carter, C. S. & Cohen, J. D. Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402, 179–181 (1999)

    Article  ADS  CAS  Google Scholar 

  3. Brown, J. W. & Braver, T. S. Learned predictions of error likelihood in the anterior cingulate cortex. Science 307, 1118–1121 (2005)

    Article  ADS  CAS  Google Scholar 

  4. Gratton, G., Coles, M. G. & Donchin, E. Optimizing the use of information: strategic control of activation of responses. J. Exp. Psychol. Gen. 121, 480–506 (1992)

    Article  CAS  Google Scholar 

  5. Hayden, B. Y. & Platt, M. L. Neurons in anterior cingulate cortex multiplex information about reward and action. J. Neurosci. 30, 3339–3346 (2010)

    Article  CAS  Google Scholar 

  6. Narayanan, N. S. & Laubach, M. Neuronal correlates of post-error slowing in the rat dorsomedial prefrontal cortex. J. Neurophysiol. 100, 520–525 (2008)

    Article  Google Scholar 

  7. Botvinick, M. M., Cohen, J. D. & Carter, C. S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci. 8, 539–546 (2004)

    Article  Google Scholar 

  8. Carter, C. S. & van Veen, V. Anterior cingulate cortex and conflict detection: an update of theory and data. Cogn. Affect. Behav. Neurosci. 7, 367–379 (2007)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  10. Nieuwenhuis, S., Schweizer, T. S., Mars, R. B., Botvinick, M. M. & Hajcak, G. Error-likelihood prediction in the medial frontal cortex: a critical evaluation. Cereb. Cortex 17, 1570–1581 (2007)

    Article  Google Scholar 

  11. Davis, K. D., Hutchison, W. D., Lozano, A. M., Tasker, R. R. & Dostrovsky, J. O. Human anterior cingulate cortex neurons modulated by attention-demanding tasks. J. Neurophysiol. 83, 3575–3577 (2000)

    Article  CAS  Google Scholar 

  12. Davis, K. D. et al. Human anterior cingulate cortex neurons encode cognitive and emotional demands. J. Neurosci. 25, 8402–8406 (2005)

    Article  CAS  Google Scholar 

  13. Bush, G. & Shin, L. M. The Multi-Source Interference Task: an fMRI task that reliably activates the cingulo-frontal-parietal cognitive/attention network. Nature Protocols 1, 308–313 (2006)

    Article  Google Scholar 

  14. Bush, G., Shin, L. M., Holmes, J., Rosen, B. R. & Vogt, B. A. The Multi-Source Interference Task: validation study with fMRI in individual subjects. Mol. Psychiatry 8, 60–70 (2003)

    Article  CAS  Google Scholar 

  15. Bush, G. et al. Functional magnetic resonance imaging of methylphenidate and placebo in attention-deficit/hyperactivity disorder during the multi-source interference task. Arch. Gen. Psychiatry 65, 102–114 (2008)

    Article  CAS  Google Scholar 

  16. Fellows, L. K. & Farah, M. J. Is anterior cingulate cortex necessary for cognitive control? Brain 128, 788–796 (2005)

    Article  Google Scholar 

  17. Kerns, J. G. et al. Anterior cingulate conflict monitoring and adjustments in control. Science 303, 1023–1026 (2004)

    Article  ADS  CAS  Google Scholar 

  18. Nakamura, K., Roesch, M. R. & Olson, C. R. Neuronal activity in macaque SEF and ACC during performance of tasks involving conflict. J. Neurophysiol. 93, 884–908 (2005)

    Article  Google Scholar 

  19. Holroyd, C. B. & Coles, M. G. The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol. Rev. 109, 679–709 (2002)

    Article  Google Scholar 

  20. Botvinick, M. M. Conflict monitoring and decision making: reconciling two perspectives on anterior cingulate function. Cogn. Affect. Behav. Neurosci. 7, 356–366 (2007)

    Article  Google Scholar 

  21. Ito, S., Stuphorn, V., Brown, J. W. & Schall, J. D. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120–122 (2003)

    Article  ADS  CAS  Google Scholar 

  22. Mayr, U., Awh, E. & Laurey, P. Conflict adaptation effects in the absence of executive control. Nature Neurosci. 6, 450–452 (2003)

    Article  CAS  Google Scholar 

  23. Ridderinkhof, K. R. Micro- and macro-adjustments of task set: activation and suppression in conflict tasks. Psychol. Res. 66, 312–323 (2002)

    Article  Google Scholar 

  24. Mansouri, F. A., Buckley, M. J. & Tanaka, K. Mnemonic function of the dorsolateral prefrontal cortex in conflict-induced behavioral adjustment. Science 318, 987–990 (2007)

    Article  ADS  CAS  Google Scholar 

  25. Gehring, W. J. & Fencsik, D. E. Functions of the medial frontal cortex in the processing of conflict and errors. J. Neurosci. 21, 9430–9437 (2001)

    Article  CAS  Google Scholar 

  26. di Pellegrino, G., Ciaramelli, E. & Ladavas, E. The regulation of cognitive control following rostral anterior cingulate cortex lesion in humans. J. Cogn. Neurosci. 19, 275–286 (2007)

    Article  Google Scholar 

  27. Cole, M. W., Yeung, N., Freiwald, W. A. & Botvinick, M. Cingulate cortex: diverging data from humans and monkeys. Trends Neurosci. 32, 566–574 (2009)

    Article  CAS  Google Scholar 

  28. Rauch, S. L. et al. Volume reduction in the caudate nucleus following stereotactic placement of lesions in the anterior cingulate cortex in humans: a morphometric magnetic resonance imaging study. J. Neurosurg. 93, 1019–1025 (2000)

    Article  CAS  Google Scholar 

  29. Asaad, W. F. & Eskandar, E. N. A flexible software tool for temporally-precise behavioral control in Matlab. J. Neurosci. Methods 174, 245–258 (2008)

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Science Foundation (IOB 0645886), the National Institutes of Health (NEI 1R01EY017658-01A1, NIDA 1R01NS063249, NIMH Conte Award MH086400 and R25 NS065743), the Klingenstein Foundation, the Howard Hughes Medical Institute, the Sackler Scholar Programme in Psychobiology, the Centers for Disease Control (5 R01 DP000339), the Benson-Henry Institute at Massachusetts General Hospital for Mind–Body Medicine, the David Judah Fund, the McIngvale Fund, and the Center for Functional Neuroimaging Technologies (P41RR14075).

Author information

Author notes

  1. Sameer A. Sheth and Matthew K. Mian: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Nayef Al-Rodhan Laboratories, Massachusetts General Hospital, Boston, 02114, Massachusetts, USA

    Sameer A. Sheth, Matthew K. Mian, Shaun R. Patel, Ziv M. Williams & Emad N. Eskandar

  2. Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, 02118, Massachusetts, USA

    Shaun R. Patel

  3. Department of Neurosurgery, Alpert Medical School, Brown University and Rhode Island Hospital, Providence, 02912, Rhode Island, USA

    Wael F. Asaad

  4. Department of Psychiatry, Massachusetts General Hospital, Boston, 02114, Massachusetts, USA

    Darin D. Dougherty & George Bush

Authors
  1. Sameer A. Sheth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew K. Mian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaun R. Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wael F. Asaad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ziv M. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Darin D. Dougherty
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. George Bush
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Emad N. Eskandar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.N.E., W.F.A., Z.M.W. and D.D.D. designed the study. G.B. administered and interpreted the fMRI scans. E.N.E. performed the surgical procedures, and S.A.S., M.K.M., S.R.P. and W.F.A. obtained the neuronal recordings. S.A.S. and M.K.M. analysed the data and wrote the manuscript. All authors edited the manuscript.

Corresponding author

Correspondence to Emad N. Eskandar.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-9, Supplementary Methods, Supplementary Table 1, a Supplementary Discussion and Supplementary Notes 1-4. (PDF 1942 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sheth, S., Mian, M., Patel, S. et al. Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature 488, 218–221 (2012). https://doi.org/10.1038/nature11239

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11239

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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