Debates over the function(s) of dorsal anterior cingulate cortex (dACC) have persisted for decades. So too have demonstrations of the region's association with cognitive control. Researchers have struggled to account for this association and, simultaneously, dACC's involvement in phenomena related to evaluation and motivation. We describe a recent integrative theory that achieves this goal. It proposes that dACC serves to specify the currently optimal allocation of control by determining the overall expected value of control (EVC), thereby licensing the associated cognitive effort. The EVC theory accounts for dACC's sensitivity to a wide array of experimental variables, and their relationship to subsequent control adjustments. Finally, we contrast our theory with a recent theory proposing a primary role for dACC in foraging-like decisions. We describe why the EVC theory offers a more comprehensive and coherent account of dACC function, including dACC's particular involvement in decisions regarding foraging or otherwise altering one's behavior.
Your institute does not have access to this article
Open Access articles citing this article.
Scientific Reports Open Access 11 April 2022
Scalp recorded theta activity is modulated by reward, direction, and speed during virtual navigation in freely moving humans
Scientific Reports Open Access 07 February 2022
Neuropsychopharmacology Open Access 28 September 2021
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
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).
Holroyd, C.B. & Yeung, N. Motivation of extended behaviors by anterior cingulate cortex. Trends Cogn. Sci. 16, 122–128 (2012).
Rushworth, M.F.S., Kolling, N., Sallet, J. & Mars, R.B. Valuation and decision-making in frontal cortex: one or many serial or parallel systems? Curr. Opin. Neurobiol. 22, 946–955 (2012).
Shenhav, A., Botvinick, M.M. & Cohen, J.D. The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 79, 217–240 (2013).
Heilbronner, S.R. & Hayden, B.Y. Dorsal anterior cingulate cortex: a bottom-up view. Annu. Rev. Neurosci. 39, 149–170 (2016).
Shackman, A.J. et al. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12, 154–167 (2011).
Cole, M.W., Yeung, N., Freiwald, W.A. & Botvinick, M. Cingulate cortex: diverging data from humans and monkeys. Trends Neurosci. 32, 566–574 (2009).
Vogt, B.A. Midcingulate cortex: Structure, connections, homologies, functions and diseases. J. Chem. Neuroanat. 74, 28–46 (2016).
Procyk, E. et al. Midcingulate motor map and feedback detection: converging data from humans and monkeys. Cereb. Cortex 26, 467–476 (2016).
Petersen, S.E. & Posner, M.I. The attention system of the human brain: 20 years after. Annu. Rev. Neurosci. 35, 73–89 (2012).
Botvinick, M.M. & Cohen, J.D. The computational and neural basis of cognitive control: charted territory and new frontiers. Cogn. Sci. 38, 1249–1285 (2014).
Stuss, D.T. & Alexander, M.P. Is there a dysexecutive syndrome? Phil. Trans. R. Soc. Lond. B 362, 901–915 (2007).
Wallis, J.D. & Kennerley, S.W. Contrasting reward signals in the orbitofrontal cortex and anterior cingulate cortex. Ann. NY Acad. Sci. 1239, 33–42 (2011).
Ullsperger, M., Danielmeier, C. & Jocham, G. Neurophysiology of performance monitoring and adaptive behavior. Physiol. Rev. 94, 35–79 (2014).
Cavanagh, J.F. & Frank, M.J. Frontal theta as a mechanism for cognitive control. Trends Cogn. Sci. 18, 414–421 (2014).
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).
Botvinick, M. & Braver, T. Motivation and cognitive control: from behavior to neural mechanism. Annu. Rev. Psychol. 66, 83–113 (2015).
Westbrook, A. & Braver, T.S. Cognitive effort: a neuroeconomic approach. Cogn. Affect. Behav. Neurosci. 15, 395–415 (2015).
Hare, T.A., Schultz, W., Camerer, C.F., O'Doherty, J.P. & Rangel, A. Transformation of stimulus value signals into motor commands during simple choice. Proc. Natl. Acad. Sci. USA 108, 18120–18125 (2011).
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).
Venkatraman, V. & Huettel, S.A. Strategic control in decision-making under uncertainty. Eur. J. Neurosci. 35, 1075–1082 (2012).
Shen, C. et al. Anterior cingulate cortex cells identify process-specific errors of attentional control prior to transient prefrontal-cingulate inhibition. Cereb. Cortex 25, 2213–2228 (2015).
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).
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).
Narayanan, N.S., Cavanagh, J.F., Frank, M.J. & Laubach, M. Common medial frontal mechanisms of adaptive control in humans and rodents. Nat. Neurosci. 16, 1888–1895 (2013).
Phillips, J.M. & Everling, S. Event-related potentials associated with performance monitoring in non-human primates. Neuroimage 97, 308–320 (2014).
Warren, C.M., Hyman, J.M., Seamans, J.K. & Holroyd, C.B. Feedback-related negativity observed in rodent anterior cingulate cortex. J. Physiol. Paris 109, 87–94 (2015).
Amiez, C., Sallet, J., Procyk, E. & Petrides, M. Modulation of feedback related activity in the rostral anterior cingulate cortex during trial and error exploration. Neuroimage 63, 1078–1090 (2012).
Quilodran, R., Rothé, M. & Procyk, E. Behavioral shifts and action valuation in the anterior cingulate cortex. Neuron 57, 314–325 (2008).
Ebitz, R.B. & Platt, M.L. Neuronal activity in primate dorsal anterior cingulate cortex signals task conflict and predicts adjustments in pupil-linked arousal. Neuron 85, 628–640 (2015).
Sheth, S.A. et al. Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature 488, 218–221 (2012).
Michelet, T. et al. Electrophysiological correlates of a versatile executive control system in the monkey anterior cingulate cortex. Cereb. Cortex 26, 1684–1697 (2016).
Oehrn, C.R. et al. Neural communication patterns underlying conflict detection, resolution, and adaptation. J. Neurosci. 34, 10438–10452 (2014).
Tang, H. et al. Cascade of neural processing orchestrates cognitive control in human frontal cortex. eLife 5, 4671 (2016).
McGuire, J.T., Nassar, M.R., Gold, J.I. & Kable, J.W. Functionally dissociable influences on learning rate in a dynamic environment. Neuron 84, 870–881 (2014).
O'Reilly, J.X. et al. Dissociable effects of surprise and model update in parietal and anterior cingulate cortex. Proc. Natl. Acad. Sci. USA 110, E3660–E3669 (2013).
Kouneiher, F., Charron, S. & Koechlin, E. Motivation and cognitive control in the human prefrontal cortex. Nat. Neurosci. 12, 939–945 (2009).
Kaping, D., Vinck, M., Hutchison, R.M., Everling, S. & Womelsdorf, T. Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation. PLoS Biol. 9, e1001224 (2011).
Cavanagh, J.F. & Shackman, A.J. Frontal midline theta reflects anxiety and cognitive control: meta-analytic evidence. J. Physiol. Paris 109, 3–15 (2015).
Mulder, M.J., Wagenmakers, E.-J., Ratcliff, R., Boekel, W. & Forstmann, B.U. Bias in the brain: a diffusion model analysis of prior probability and potential payoff. J. Neurosci. 32, 2335–2343 (2012).
Payzan-LeNestour, E., Dunne, S., Bossaerts, P. & O'Doherty, J.P. The neural representation of unexpected uncertainty during value-based decision making. Neuron 79, 191–201 (2013).
Ma, L., Hyman, J.M., Phillips, A.G. & Seamans, J.K. Tracking progress toward a goal in corticostriatal ensembles. J. Neurosci. 34, 2244–2253 (2014).
Womelsdorf, T., Johnston, K., Vinck, M. & Everling, S. Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors. Proc. Natl. Acad. Sci. USA 107, 5248–5253 (2010).
Johnston, K., Levin, H.M., Koval, M.J. & Everling, S. Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching. Neuron 53, 453–462 (2007).
Metzler-Baddeley, C. et al. Cingulum microstructure predicts cognitive control in older age and mild cognitive impairment. J. Neurosci. 32, 17612–17619 (2012).
de Wit, S. et al. Corticostriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control. J. Neurosci. 32, 12066–12075 (2012).
Hochman, E.Y., Wang, S., Milner, T.E. & Fellows, L.K. Double dissociation of error inhibition and correction deficits after basal ganglia or dorsomedial frontal damage in humans. Neuropsychologia 69, 130–139 (2015).
Newman, L.A., Creer, D.J. & McGaughy, J.A. Cognitive control and the anterior cingulate cortex: how conflicting stimuli affect attentional control in the rat. J. Physiol. Paris 109, 95–103 (2015).
Kennerley, S.W., Walton, M.E., Behrens, T.E.J., Buckley, M.J. & Rushworth, M.F.S. Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 9, 940–947 (2006).
Chudasama, Y. et al. The role of the anterior cingulate cortex in choices based on reward value and reward contingency. Cereb. Cortex 23, 2884–2898 (2013).
Gläscher, J. et al. Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc. Natl. Acad. Sci. USA 109, 14681–14686 (2012).
Gaymard, B. et al. Effects of anterior cingulate cortex lesions on ocular saccades in humans. Exp. Brain Res. 120, 173–183 (1998).
Phillips, J.M., Johnston, K. & Everling, S. Effects of anterior cingulate microstimulation on pro- and antisaccades in nonhuman primates. J. Cogn. Neurosci. 23, 481–490 (2011).
Reinhart, R.M.G. & Woodman, G.F. Causal control of medial-frontal cortex governs electrophysiological and behavioral indices of performance monitoring and learning. J. Neurosci. 34, 4214–4227 (2014).
Reinhart, R.M.G., Zhu, J., Park, S. & Woodman, G.F. Synchronizing theta oscillations with direct-current stimulation strengthens adaptive control in the human brain. Proc. Natl. Acad. Sci. USA 112, 9448–9453 (2015).
Fellows, L.K. & Farah, M.J. Is anterior cingulate cortex necessary for cognitive control? Brain 128, 788–796 (2005).
Tolomeo, S. et al. A causal role for the anterior mid-cingulate cortex in negative affect and cognitive control. Brain 139, 1844–1854 (2016).
McGuire, J.T. & Botvinick, M.M. Prefrontal cortex, cognitive control, and the registration of decision costs. Proc. Natl. Acad. Sci. USA 107, 7922–7926 (2010).
Magno, E., Foxe, J.J., Molholm, S., Robertson, I.H. & Garavan, H. The anterior cingulate and error avoidance. J. Neurosci. 26, 4769–4773 (2006).
Spunt, R.P., Lieberman, M.D., Cohen, J.R. & Eisenberger, N.I. The phenomenology of error processing: the dorsal ACC response to stop-signal errors tracks reports of negative affect. J. Cogn. Neurosci. 24, 1753–1765 (2012).
Botvinick, M.M., Huffstetler, S. & McGuire, J.T. Effort discounting in human nucleus accumbens. Cogn. Affect. Behav. Neurosci. 9, 16–27 (2009).
Cavanagh, J.F., Masters, S.E., Bath, K. & Frank, M.J. Conflict acts as an implicit cost in reinforcement learning. Nat. Commun. 5, 5394 (2014).
Hosking, J.G., Cocker, P.J. & Winstanley, C.A. Dissociable contributions of anterior cingulate cortex and basolateral amygdala on a rodent cost-benefit decision-making task of cognitive effort 39, 1558–1567 (2014).
Parvizi, J., Rangarajan, V., Shirer, W.R., Desai, N. & Greicius, M.D. The will to persevere induced by electrical stimulation of the human cingulate gyrus. Neuron 80, 1359–1367 (2013).
Kolling, N., Behrens, T.E.J., Mars, R.B. & Rushworth, M.F.S. Neural mechanisms of foraging. Science 336, 95–98 (2012).
Charnov, E.L. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129–136 (1976).
Shenhav, A., Straccia, M.A., Cohen, J.D. & Botvinick, M.M. Anterior cingulate engagement in a foraging context reflects choice difficulty, not foraging value. Nat. Neurosci. 17, 1249–1254 (2014).
Shenhav, A., Straccia, M.A., Botvinick, M.M. & Cohen, J.D. Dorsal anterior cingulate and ventromedial prefrontal cortex have inverse roles in both foraging and economic choice. Cogn. Affect. Behav. Neurosci. http://dx.doi.org/10.3758/s13415-016-0458-8 (2016).
Schlund, M.W. et al. The tipping point: value differences and parallel dorsal-ventral frontal circuits gating human approach-avoidance behavior. Neuroimage 136, 94–105 (2016).
Kolling, N., Behrens, T., Wittmann, M.K. & Rushworth, M. Multiple signals in anterior cingulate cortex. Curr. Opin. Neurobiol. 37, 36–43 (2016).
Schall, J.D. & Emeric, E.E. Conflict in cingulate cortex function between humans and macaque monkeys: more apparent than real. Brain Behav. Evol. 75, 237–238 (2010).
Alexander, W.H. & Brown, J.W. Hierarchical error representation: a computational model of anterior cingulate and dorsolateral prefrontal cortex. Neural Comput. 27, 2354–2410 (2015).
Westbrook, A. & Braver, T.S. Dopamine does double duty in motivating cognitive effort. Neuron 89, 695–710 (2016).
Musslick, S., Shenhav, A., Botvinick, M.M. & Cohen, J.D. A computational model of control allocation based on the expected value of control. in The 2nd Multidisciplinary Conference on Reinforcement Learning and Decision Making http://rldm.org/wp-content/uploads/2015/06/RLDM15AbstractsBooklet.pdf (2015).
Manohar, S.G. et al. Reward pays the cost of noise reduction in motor and cognitive control. Curr. Biol. 25, 1707–1716 (2015).
The authors would like to thank J. Cavanagh for his feedback on an earlier draft of the manuscript. This work was supported by the C.V. Starr Foundation (A.S.) and the John Templeton Foundation. The opinions expressed in this publication are those of the authors and do not necessarily reflect the views of the John Templeton Foundation.
The authors declare no competing financial interests.
About this article
Cite this article
Shenhav, A., Cohen, J. & Botvinick, M. Dorsal anterior cingulate cortex and the value of control. Nat Neurosci 19, 1286–1291 (2016). https://doi.org/10.1038/nn.4384
Nature Human Behaviour (2022)
Scientific Reports (2022)
Nature Human Behaviour (2022)