COGNITION AND BEHAVIOR merical reference may play a role in the emer 12.E.M.B n The Co and pp. th.The Eds.(MIT Pres ECIAL 13 6.C.R.Gallis 97 okofhn Gleitr R the st (MIT 10.0 ot2ooe0ng uk/info n. 。 mton 25.24 L N 131097 REVIEW The Role of the Medial Frontal Cortex in Cognitive Control K.Richard Ridderinkhof,12 Markus Ullsperger,Eveline A.Crone,Sander Nieuwenhuiss and learning is nce cor tha g behavio We A re primate and human studies,along with a meta-analysis of the human functio ncuroimaging stu ture,suggest the detectic outcom hat poi 14 mportan c rs of activat n foci in an ext nsive part of the pos e o omes,resp errors.and (pMFC).A activity ubsequen bet d the) so that monitorin goals may v not be t engages regulatory processes i ea un Although the pMFC can also be activated ing contextually relevant info mation and for formance ring.espec consequences Because errors and conflicts Evaluatin g the quential for the tion of cognitive review recent studies in cognitive iate behavioral adius ents Fot our understan of a performance error rvative speed/accura balance ron ntrol Based on the evidence reviewed b thow.we and lateral prefrontal cortex (LPFC)are im of the pMFC is performance ulations in the pMFC particularly in the to annc e rostra ersstr rors or negative feedback)or reduced pro- rtment of AK Leider the need for increased control ward (5). pecifi 04103 Leip roup of Performance monitoring the a h of the cingu Flexible adjustments of behavior and wards(5).Thesc be add and the outcomes of these actions.The abil and actual outcomes. www.sciencemag-org SCIENCE VOL 306 15 OCTOBER 2004 443merical reference may play a role in the emer￾gence of a fully formed conception of number. The challenge now is to delineate that role. References and Notes 1. L. Gleitman, A. Papafragou, in Handbook of Thinking and Reasoning, K. J. Holyoak, R. Morrison, Eds. (Cambridge Univ. Press, New York, in press). 2. D. Gentner, S. Golden-Meadow, Eds., Language and Mind: Advances in the Study of Language and Thought (MIT Press, Cambridge, MA, 2003). 3. S. C. Levinson, in Language and Space, P. Bloom, M. Peterson, L. Nadel, M. Garrett, Eds. (MIT Press, Cambridge, MA, 1996), Chap. 4. 4. R. Gelman, S. A. Cordes, in Language, Brain, and Cognitive Development: Essays in Honor of Jacques Mehler, E. Dupoux, Ed. (MIT Press, Cambridge, MA, 2001), pp. 279–301. 5. B. Butterworth, The Mathematical Brain (McMillan, London, 1999). 6. C. R. Gallistel, The Organization of Learning (Bradford Books/MIT Press, Cambridge, MA, 1990). 7. J. A. Fodor, The Language of Thought (T. Y. Crowell, New York, 1975). 8. P. Gordon, Science 306, 496 (2004). 9. P. Pica, C. Lemer, V. Izard, S. Dehaene, Science 306, 499 (2004). 10. D. L. Everett, (2004) http://lings.In.man.ac.uk/info/ staff/DE/cultgram.pdf (cited by permission). 11. C. R. Gallistel, R. Gelman, in Handbook of Thinking and Reasoning, K. J. Holyoak, R. Morrison, Eds. (Cambridge University Press, New York, in press). 12. E. M. Brannon, H. S. Terrace, in The Cognitive Animal: Empirical and Theoretical Perspectives on Animal Cognition, M. Bekoff, C. Allen, Eds. (MIT Press, Cambridge, MA, 2002), pp. 197–204. 13. S. Dehaene, The Number Sense (Oxford University Press, Oxford, 1997). 14. R. Gelman, B. Butterworth, Trends Cognit. Sci., in press. 15. L. Gleitman, J. Trueswell, K. Cassidy, R. Nappa, A. Papafragou, Lang. Learn. Dev., in press. 16. S. Carey, Daedalus 133, 59 (2004). 17. E. von Glaserfield, in The Development of Numerical Competence: Animal and Human Models, S. T. Boysen, E. J. Capaldi (Lawrence Erlbaum Associates, Hillsdale, NJ, 1993), pp. 225<244. 18. H. Davis, R. Pe´russe, Behav. Brain Sci. 11, 561 (1988). 19. P. B. Buckley, C. B. Gillman, J. Exp. Psychol. 103, 1131 (1974). REVIEW The Role of the Medial Frontal Cortex in Cognitive Control K. Richard Ridderinkhof,1,2* Markus Ullsperger,3 Eveline A. Crone,4 Sander Nieuwenhuis5 Adaptive goal-directed behavior involves monitoring of ongoing actions and per￾formance outcomes, and subsequent adjustments of behavior and learning. We evaluate new findings in cognitive neuroscience concerning cortical interactions that subserve the recruitment and implementation of such cognitive control. A review of primate and human studies, along with a meta-analysis of the human functional neuroimaging literature, suggest that the detection of unfavorable outcomes, re￾sponse errors, response conflict, and decision uncertainty elicits largely overlapping clusters of activation foci in an extensive part of the posterior medial frontal cortex (pMFC). A direct link is delineated between activity in this area and subsequent adjustments in performance. Emerging evidence points to functional interactions between the pMFC and the lateral prefrontal cortex (LPFC), so that monitoring￾related pMFC activity serves as a signal that engages regulatory processes in the LPFC to implement performance adjustments. Flexible goal-directed behavior requires an adaptive cognitive control system for select￾ing contextually relevant information and for organizing and optimizing information pro￾cessing. Such adaptive control is effortful, and therefore it may not be efficient to main￾tain high levels of control at all times. Here we review recent studies in cognitive neu￾roscience that have advanced our understand￾ing of how the brain determines and communicates the need to recruit cognitive control. Convergent evidence suggests that the posterior medial frontal cortex (pMFC) and lateral prefrontal cortex (LPFC) are im￾portant contributors to cognitive control. Our focus is on the role of the pMFC in per￾formance monitoring, especially in situa￾tions in which pMFC activity is followed by performance adjustments. Evaluating the adequacy and success of performance is instrumental in determining and implement￾ing appropriate behavioral adjustments. For instance, detection of a performance error may be used to shift performance strategy to a more conservative speed/accuracy balance. Based on the evidence reviewed below, we develop the tentative hypothesis that one unified function of the pMFC is performance monitoring in relation to anticipated rewards. The monitored signals may index the failure (errors or negative feedback) or reduced pro￾bability (conflicts or decision uncertainty) of obtaining such rewards, and as such signal the need for increased control. Performance Monitoring Flexible adjustments of behavior and reward-based association learning require the continuous assessment of ongoing actions and the outcomes of these actions. The abil￾ity to monitor and compare actual perform￾ance with internal goals and standards is critical for optimizing behavior. We first review evidence from primate, electrophysi￾ological, and functional neuroimaging studies that points toward the importance of pMFC areas (Fig. 1A) in monitoring unfavorable performance outcomes, response errors, and response conflicts, respectively. These con￾ditions have in common that they signal that goals may not be achieved or rewards may not be obtained unless the level of cognitive control is subsequently increased. Although the pMFC can also be activated by positive events (such as rewards) (1, 2), we focus here on negative events and their consequences. Because errors and conflicts are intrinsically negative, and because unfa￾vorable outcomes are typically more conse￾quential for the regulation of cognitive control than are favorable outcomes, our review focuses on the role of the pMFC in monitoring negative events. Monitoring unfavorable outcomes. Elec￾trophysiological recordings in nonhuman primates implicate the pMFC in monitoring performance outcomes. Distinct neuron pop￾ulations in the pMFC, particularly in the supplementary eye fields and the rostral cingulate motor area (CMAr), are sensitive to reward expectancy and reward delivery (1, 3, 4). In addition, CMAr neurons exhibit sensitivity to unexpected reductions in re￾ward (5). Likewise, specific groups of neurons in the depth of the cingulate sulcus (area 24c) react to response errors and to unexpected omissions of rewards (5). These findings are consistent with a role for these neuronal populations in comparing expected and actual outcomes. 1 Department of Psychology, University of Amster￾dam, Roetersstraat 15, 1018 WB Amsterdam, Neth￾erlands. 2 Department of Psychology, Leiden University, Wassenaarseweg 52, 2333 AK Leiden, Netherlands. 3 Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1A, 04103 Leipzig, Germany. 4 Center for Mind and Brain, University of California Davis, 202 Cousteau Place, Suite 201, Davis, CA 95616, USA. 5 Department of Cognitive Psychology, Vrije Universiteit, Van der Boechorststraat 1, 1081 BT Amsterdam, Netherlands. *To whom correspondence should be addressed. E-mail: K.R.Ridderinkhof@uva.nl C OGNITION AND B EHAVIOR www.sciencemag.org SCIENCE VOL 306 15 OCTOBER 2004 443 S PECIAL S ECTION