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:

Neural encoding of competitive effort in the anterior cingulate cortex

Abstract

In social environments, animals often compete to obtain limited resources. Strategically electing to work against another animal represents a cost-benefit decision. Is the resource worth an investment of competitive effort? The anterior cingulate cortex (ACC) has been implicated in cost-benefit decision-making, but its role in competitive effort has not been examined. We recorded ACC neurons in freely moving rats as they performed a competitive foraging choice task. When at least one of the two choice options demanded competitive effort, the majority of ACC neurons exhibited heightened and differential firing between the goal trajectories. Inter- and intrasession manipulations revealed that differential firing was not attributable to effort or reward in isolation; instead ACC encoding patterns appeared to indicate net utility assessments of available choice options. Our findings suggest that the ACC is important for encoding competitive effort, a cost-benefit domain that has received little neural-level investigation despite its predominance in nature.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Experimental apparatus.
Figure 2: Example firing in the baseline 2:12C configuration.
Figure 3: Development of the firing rate bias and correlation to behavior.
Figure 4: Intersession cost-benefit manipulations.
Figure 5: Intrasession cost-benefit manipulations.
Figure 6: Manipulations of peer rat pairings.

Similar content being viewed by others

References

  1. Danchin, E., Giraldeau, L.-A. & Cezilly, F. Behavioural Ecology (Oxford University Press, 2008).

  2. Stephens, D. & Krebs, J. Foraging Theory (Princeton University Press, 1986).

  3. Alcock, J. & Sherman, P. The utility of the proximate-ultimate dichotomy in ethology. Ethology 96, 58–62 (1994).

    Article  Google Scholar 

  4. Hull, C.L. Principles of Behavior (Appleton-Century, 1943).

  5. Archer, J. The Behavioural Biology of Aggression (Cambridge University Press, 1988).

  6. Looney, T.A. & Cohen, P.S. Aggression induced by intermittent positive reinforcement. Neurosci. Biobehav. Rev. 6, 15–37 (1982).

    Article  CAS  Google Scholar 

  7. Smith, J.M. & Price, G.R. Logic of animal conflict. Nature 246, 15–18 (1973).

    Article  Google Scholar 

  8. Walton, M.E., Bannerman, D.M., Alterescu, K. & Rushworth, M.F. Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J. Neurosci. 23, 6475–6479 (2003).

    Article  CAS  Google Scholar 

  9. Schweimer, J., Saft, S. & Hauber, W. Involvement of catecholamine neurotransmission in the rat anterior cingulate in effort-related decision making. Behav. Neurosci. 119, 1687–1692 (2005).

    Article  CAS  Google Scholar 

  10. Amiez, C., Joseph, J.P. & Procyk, E. Reward encoding in the monkey anterior cingulate cortex. Cereb. Cortex 16, 1040–1055 (2006).

    Article  CAS  Google Scholar 

  11. Kennerley, S.W., Walton, M.E., Behrens, T.E., Buckley, M.J. & Rushworth, M.F. Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 9, 940–947 (2006).

    Article  CAS  Google Scholar 

  12. Devinsky, O., Morrell, M.J. & Vogt, B.A. Contributions of anterior cingulate cortex to behavior. Brain 118, 279–306 (1995).

    Article  Google Scholar 

  13. Lavretsky, H., Ballmaier, M., Pham, D., Toga, A. & Kumar, A. Neuroanatomical characteristics of geriatric apathy and depression: a magnetic resonance imaging study. Am. J. Geriatr. Psychiatry 15, 386–394 (2007).

    Article  Google Scholar 

  14. Marsh, R., Maia, T.V. & Peterson, B.S. Functional disturbances within frontostriatal circuits across multiple childhood psychopathologies. Am. J. Psychiatry 166, 664–674 (2009).

    Article  Google Scholar 

  15. Mars, R.B. et al. Neural dynamics of error processing in medial frontal cortex. Neuroimage 28, 1007–1013 (2005).

    Article  Google Scholar 

  16. Matsumoto, M., Matsumoto, K., Abe, H. & Tanaka, K. Medial prefrontal cell activity signaling prediction errors of action values. Nat. Neurosci. 10, 647–656 (2007).

    Article  CAS  Google Scholar 

  17. Hillman, K.L. & Bilkey, D.K. Neurons in the rat anterior cingulate cortex dynamically encode cost-benefit in a spatial decision-making task. J. Neurosci. 30, 7705–7713 (2010).

    Article  CAS  Google Scholar 

  18. Quilodran, R., Rothe, M. & Procyk, E. Behavioral shifts and action valuation in the anterior cingulate cortex. Neuron 57, 314–325 (2008).

    Article  CAS  Google Scholar 

  19. Shidara, M. & Richmond, B.J. Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 296, 1709–1711 (2002).

    Article  Google Scholar 

  20. Hayden, B.Y., Pearson, J.M. & Platt, M.L. Neuronal basis of sequential foraging decisions in a patchy environment. Nat. Neurosci. 14, 933–939 (2011).

    Article  CAS  Google Scholar 

  21. Rilling, J. et al. A neural basis for social cooperation. Neuron 35, 395–405 (2002).

    Article  CAS  Google Scholar 

  22. Tomlin, D. et al. Agent-specific responses in the cingulate cortex during economic exchanges. Science 312, 1047–1050 (2006).

    Article  CAS  Google Scholar 

  23. Rudebeck, P.H., Buckley, M.J., Walton, M.E. & Rushworth, M.F. A role for the macaque anterior cingulate gyrus in social valuation. Science 313, 1310–1312 (2006).

    Article  CAS  Google Scholar 

  24. Gemmell, C., Anderson, M. & O'Mara, S.M. Deep layer prefrontal cortex unit discharge in a cue-controlled open-field environment in the freely moving rat. Behav. Brain Res. 133, 1–10 (2002).

    Article  Google Scholar 

  25. Jung, M.W., Qin, Y., McNaughton, B.L. & Barnes, C.A. Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb. Cortex 8, 437–450 (1998).

    Article  CAS  Google Scholar 

  26. Scott, J.P. & Fredericson, E. The causes of fighting in mice and rats. Physiol. Zool. 24, 273–309 (1951).

    Article  Google Scholar 

  27. Frith, C.D. & Frith, U. Interacting minds: a biological basis. Science 286, 1692–1695 (1999).

    Article  CAS  Google Scholar 

  28. Rilling, J.K., Sanfey, A.G., Aronson, J.A., Nystrom, L.E. & Cohen, J.D. The neural correlates of theory of mind within interpersonal interactions. Neuroimage 22, 1694–1703 (2004).

    Article  Google Scholar 

  29. Amodio, D.M. & Frith, C.D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268–277 (2006).

    Article  CAS  Google Scholar 

  30. Hadland, K.A., Rushworth, M.F., Gaffan, D. & Passingham, R.E. The effect of cingulate lesions on social behavior and emotion. Neuropsychologia 41, 919–931 (2003).

    Article  CAS  Google Scholar 

  31. Rudebeck, P.H. et al. Distinct contributions of frontal areas to emotion and social behavior in the rat. Eur. J. Neurosci. 26, 2315–2326 (2007).

    Article  Google Scholar 

  32. von Neumann, J. & Morgenstern, O. Theory of Games and Economic Behavior (Princeton University Press, 1944).

  33. Croxson, P.L., Walton, M.E., O'Reilly, J.X., Behrens, T.E. & Rushworth, M.F. Effort-based cost-benefit valuation and the human brain. J. Neurosci. 29, 4531–4541 (2009).

    Article  CAS  Google Scholar 

  34. Forstmann, B.U., Brass, M., Koch, I. & von Cramon, D.Y. Voluntary selection of task sets revealed by functional magnetic resonance imaging. J. Cogn. Neurosci. 18, 388–398 (2006).

    Article  Google Scholar 

  35. Walton, M.E., Devlin, J.T. & Rushworth, M.F. Interactions between decision making and performance monitoring within prefrontal cortex. Nat. Neurosci. 7, 1259–1265 (2004).

    Article  CAS  Google Scholar 

  36. Yoshida, W. & Ishii, S. Resolution of uncertainty in prefrontal cortex. Neuron 50, 781–789 (2006).

    Article  CAS  Google Scholar 

  37. Sutton, R.S. & Barto, A.G. Reinforcement Learning: an Introduction (MIT Press, 1998).

  38. Kennerley, S.W., Dahmubed, A.F., Lara, A.H. & Wallis, J.D. Neurons in the frontal lobe encode the value of multiple decision variables. J. Cogn. Neurosci. 21, 1162–1178 (2009).

    Article  Google Scholar 

  39. Alexander, W.H. & Brown, J.W. Medial prefrontal cortex as an action-outcome predictor. Nat. Neurosci. 14, 1338–1344 (2011).

    Article  CAS  Google Scholar 

  40. Lapish, C.C., Durstewitz, D., Chandler, L.J. & Seamans, J.K. Successful choice behavior is associated with distinct and coherent network states in anterior cingulate cortex. Proc. Natl. Acad. Sci. USA 105, 11963–11968 (2008).

    Article  CAS  Google Scholar 

  41. Sallet, J. et al. Expectations, gains and losses in the anterior cingulate cortex. Cogn. Affect. Behav. Neurosci. 7, 327–336 (2007).

    Article  Google Scholar 

  42. Behrens, T.E., Woolrich, M.W., Walton, M.E. & Rushworth, M.F. Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214–1221 (2007).

    Article  CAS  Google Scholar 

  43. Seo, H. & Lee, D. Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game. J. Neurosci. 27, 8366–8377 (2007).

    Article  CAS  Google Scholar 

  44. Frith, C.D., Friston, K., Liddle, P.F. & Frackowiak, R.S. Willed action and the prefrontal cortex in man: a study with PET. Proc. Biol. Sci. 244, 241–246 (1991).

    Article  CAS  Google Scholar 

  45. Raichle, M.E. et al. Practice-related changes in human brain functional anatomy during nonmotor learning. Cereb. Cortex 4, 8–26 (1994).

    Article  CAS  Google Scholar 

  46. Naccache, L. et al. Effortless control: executive attention and conscious feeling of mental effort are dissociable. Neuropsychologia 43, 1318–1328 (2005).

    Article  Google Scholar 

  47. Procyk, E., Tanaka, Y.L. & Joseph, J.P. Anterior cingulate activity during routine and non-routine sequential behaviors in macaques. Nat. Neurosci. 3, 502–508 (2000).

    Article  CAS  Google Scholar 

  48. Matsumoto, K., Suzuki, W. & Tanaka, K. Neuronal correlates of goal-based motor selection in the prefrontal cortex. Science 301, 229–232 (2003).

    Article  CAS  Google Scholar 

  49. Barrash, J., Tranel, D. & Anderson, S.W. Acquired personality disturbances associated with bilateral damage to the ventromedial prefrontal region. Dev. Neuropsychol. 18, 355–381 (2000).

    Article  CAS  Google Scholar 

  50. Mayberg, H.S. et al. Deep brain stimulation for treatment-resistant depression. Neuron 45, 651–660 (2005).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding was provided by the Marsden Fund.

Author information

Authors and Affiliations

Authors

Contributions

K.L.H. and D.K.B. designed the study, K.L.H. performed the experiments, and K.L.H. and D.K.B. wrote the manuscript.

Corresponding author

Correspondence to Kristin L Hillman.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3 (PDF 432 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hillman, K., Bilkey, D. Neural encoding of competitive effort in the anterior cingulate cortex. Nat Neurosci 15, 1290–1297 (2012). https://doi.org/10.1038/nn.3187

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3187

This article is cited by

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