Motivation and cognitive control in the human prefrontal cortex

Article metrics

Abstract

The prefrontal cortex (PFC) subserves cognitive control, that is, the ability to select thoughts or actions in relation to internal goals. Little is known, however, about how the PFC combines motivation and the selection processes underlying cognitive control. We used functional magnetic resonance imaging in humans and found that the medial and lateral PFC have a parallel hierarchical organization from posterior to anterior regions for motivating and selecting behaviors, respectively. Moreover, using functional connectivity analyses, we found that functional interactions in this parallel system from medial to lateral PFC regions convey motivational incentives on the basis of rewards/penalties regulating the differential engagement of lateral PFC regions in top-down selection. Our results indicate that motivation is a dissociable function, reveal how the PFC integrates motivation and cognitive control in the service of decision-making, and have major implications for current theories of prefrontal executive function.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Behavioral protocol.
Figure 2: Cognitive control in the prefrontal cortex.
Figure 3: Motivational processes in the prefrontal cortex.
Figure 4: Motivational effects on reaction times according to control demands.
Figure 5: Motivational activations in medial and lateral frontal regions according to control demands.
Figure 6: Diagram of effective connectivity between frontal regions.
Figure 7: Factorial analyses of medial frontal activations according to cognitive factors.
Figure 8: Variations of effective connectivity with response conflict.

References

  1. 1

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

  2. 2

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

  3. 3

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

  4. 4

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

  5. 5

    Badre, D. Cognitive control, hierarchy and the rostrocaudal organization of the frontal lobes. Trends Cogn. Sci. (in the press) (2008).

  6. 6

    Braver, T.S., Reynolds, J.R. & Donaldson, D.I. Neural mechanisms of transient and sustained cognitive control during task switching. Neuron 39, 713–726 (2003).

  7. 7

    Ridderinkhof, K.R., Ullsperger, M., Crone, E.A. & Nieuwenhuis, S. The role of the medial frontal cortex in cognitive control. Science 306, 443–447 (2004).

  8. 8

    Rushworth, M.F., Walton, M.E., Kennerley, S.W. & Bannerman, D.M. Action sets and decisions in the medial frontal cortex. Trends Cogn. Sci. 8, 410–417 (2004).

  9. 9

    Rushworth, M.F., Buckley, M.J., Behrens, T.E., Walton, M.E. & Bannerman, D.M. Functional organization of the medial frontal cortex. Curr. Opin. Neurobiol. 17, 220–227 (2007).

  10. 10

    Gehring, W.J. & Knight, R.T. Prefrontal-cingulate interactions in action monitoring. Nat. Neurosci. 3, 516–520 (2000).

  11. 11

    Pochon, J.B. et al. The neural system that bridges reward and cognition in humans: an fMRI study. Proc. Natl. Acad. Sci. USA 99, 5669–5674 (2002).

  12. 12

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

  13. 13

    Johansen-Berg, H. et al. Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc. Natl. Acad. Sci. USA 101, 13335–13340 (2004).

  14. 14

    Aron, A.R., Behrens, T.E., Smith, S., Frank, M.J. & Poldrack, R.A. Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J. Neurosci. 27, 3743–3752 (2007).

  15. 15

    Beckmann, M., Johansen-Berg, H. & Rushworth, M.F. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 29, 1175–1190 (2009).

  16. 16

    Hull, C.L. Principles of Behavior (Appleton-Century-Crofts, New York, 1943).

  17. 17

    Duffy, E. Activation and Behavior (Wiley, New York, 1962).

  18. 18

    Kennerley, S.W., Sakai, K. & Rushworth, M.F. Organization of action sequences and the role of the pre-SMA. J. Neurophysiol. 91, 978–993 (2004).

  19. 19

    Lau, H.C., Rogers, R.D., Haggard, P. & Passingham, R.E. Attention to intention. Science 303, 1208–1210 (2004).

  20. 20

    Sumner, P. et al. Human medial frontal cortex mediates unconscious inhibition of voluntary action. Neuron 54, 697–711 (2007).

  21. 21

    Isoda, M. & Hikosaka, O. Switching from automatic to controlled action by monkey medial frontal cortex. Nat. Neurosci. 10, 240–248 (2007).

  22. 22

    Knutson, B., Taylor, J., Kaufman, M., Peterson, R. & Glover, G. Distributed neural representation of expected value. J. Neurosci. 25, 4806–4812 (2005).

  23. 23

    Campos, M., Breznen, B., Bernheim, K. & Andersen, R.A. Supplementary motor area encodes reward expectancy in eye-movement tasks. J. Neurophysiol. 94, 1325–1335 (2005).

  24. 24

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

  25. 25

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

  26. 26

    Sohn, M.H., Albert, M.V., Jung, K., Carter, C.S. & Anderson, J.R. Anticipation of conflict monitoring in the anterior cingulate cortex and the prefrontal cortex. Proc. Natl. Acad. Sci. USA 104, 10330–10334 (2007).

  27. 27

    Hester, R., Barre, N., Mattingley, J.B., Foxe, J.J. & Garavan, H. Avoiding another mistake: error and post-error neural activity associated with adaptive posterror behavior change. Cogn. Affect. Behav. Neurosci. 7, 317–326 (2007).

  28. 28

    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).

  29. 29

    Rushworth, M.F. & Behrens, T.E. Choice, uncertainty and value in prefrontal and cingulate cortex. Nat. Neurosci. 11, 389–397 (2008).

  30. 30

    Bartels, A., Logothetis, N.K. & Moutoussis, K. fMRI and its interpretations: an illustration on directional selectivity in area V5/MT. Trends Neurosci. 31, 444–453 (2008).

  31. 31

    Stephan, K.E. On the role of general system theory for functional neuroimaging. J. Anat. 205, 443–470 (2004).

  32. 32

    Stephan, K.E. et al. Lateralized cognitive processes and lateralized task control in the human brain. Science 301, 384–386 (2003).

  33. 33

    Nachev, P. Cognition and medial frontal cortex in health and disease. Curr. Opin. Neurol. 19, 586–592 (2006).

  34. 34

    Ullsperger, M. & von Cramon, D.Y. Neuroimaging of performance monitoring: error detection and beyond. Cortex 40, 593–604 (2004).

  35. 35

    Swick, D. & Turken, A.U. Dissociation between conflict detection and error monitoring in the human anterior cingulate cortex. Proc. Natl. Acad. Sci. USA 99, 16354–16359 (2002).

  36. 36

    Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S. & Cohen, J.D. Conflict monitoring and cognitive control. Psychol. Rev. 108, 624–652 (2001).

  37. 37

    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).

  38. 38

    Hyafil, A., Summerfield, C. & Koechlin, E. Two mechanisms for task switching in the prefrontal cortex. J. Neurosci. 29, 5135–5142 (2009).

  39. 39

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

  40. 40

    Hertz, J., Krogh, A. & Palmer, R.G. Introduction to the Theory of Neural Computation (Addison-Wesley Publishing Company, Redwood City, California, 1991).

  41. 41

    Friston, K.J. & Stephan, K.E. Free-energy and the brain. Synthese 159, 417–458 (2007).

  42. 42

    Shima, K. & Tanji, J. Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J. Neurophysiol. 80, 3247–3260 (1998).

  43. 43

    Rushworth, M.F., Hadland, K.A., Gaffan, D. & Passingham, R.E. The effect of cingulate cortex lesions on task switching and working memory. J. Cogn. Neurosci. 15, 338–353 (2003).

  44. 44

    Shima, K. & Tanji, J. Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282, 1335–1338 (1998).

  45. 45

    Beck, R.C. Motivation: Theories ad Principles (Prentice Hall, New Jersey, 2004).

  46. 46

    Genovese, C.R., Lazar, N.A. & Nichols, T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870–878 (2002).

  47. 47

    Mueller, R.O. Basic Principles of Structural Equation Modeling (Springer-Verlag, New York, 1996).

  48. 48

    Penny, W.D., Stephan, K.E., Mechelli, A. & Friston, K.J. Modeling functional integration: a comparison of structural equation and dynamic causal models. Neuroimage 23 Suppl 1: S264–S274 (2004).

  49. 49

    Gitelman, D.R., Penny, W.D., Ashburner, J. & Friston, K.J. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 19, 200–207 (2003).

Download references

Acknowledgements

We thank J.-L. Anton, B. Nazarian and M. Roth at the Magnetic Resonance Imaging Center in Hospital La Timone for MRI facilities and technical assistance. We also thank C. Summerfield and E. Procyk for helpful comments on an earlier version of the manuscript. This work was supported by a European Young Investigator Award and a Prize from the Bettencourt-Schueller Foundation to E.K.

Author information

F.K. and E.K. designed the experiments. F.K. and S.C. conducted the experiments. F.K. analyzed the data. E.K. supervised the project and wrote the paper.

Correspondence to Etienne Koechlin.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3, Supplementary Data and Supplementary Methods (PDF 4304 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kouneiher, F., Charron, S. & Koechlin, E. Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci 12, 939–945 (2009) doi:10.1038/nn.2321

Download citation

Further reading