Monitoring Demands for Executive Control: Shared Functions between Human and Nonhuman Primates

Fifteen years ago, an influential model proposed that the human dorsal anterior cingulate cortex (dACC) detects conflict and induces adaptive control of behavior. Over the years support for this model has been mixed, in particular due to divergent findings in human versus nonhuman primates. We here review recent findings that suggest greater commonalities across species. These include equivalent behavioral consequences of conflict and similar neuronal signals in the dACC, but also a common failure of dACC lesions to reliably abolish conflict-driven behavior. We conclude that conflict might be one among many drivers of adjustments in executive control and that the ACC might be just one component of overlapping distributed systems involved in context-dependent learning and behavioral control.

[1]  J. Schall,et al.  Performance monitoring by the supplementary eye ® eld , 2000 .

[2]  Elisa Ciaramelli,et al.  The Regulation of Cognitive Control following Rostral Anterior Cingulate Cortex Lesion in Humans , 2007, Journal of Cognitive Neuroscience.

[3]  T. Egner,et al.  Bayesian modeling of flexible cognitive control , 2014, Neuroscience & Biobehavioral Reviews.

[4]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[5]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[6]  Marco K. Wittmann,et al.  Multiple signals in anterior cingulate cortex , 2016, Current Opinion in Neurobiology.

[7]  Keiji Tanaka,et al.  Mnemonic Function of the Dorsolateral Prefrontal Cortex in Conflict-Induced Behavioral Adjustment , 2007, Science.

[8]  Benjamin Y Hayden,et al.  Dorsal Anterior Cingulate Cortex: A Bottom-Up View. , 2016, Annual review of neuroscience.

[9]  Tobias Egner,et al.  The neural correlates and functional integration of cognitive control in a Stroop task , 2005, NeuroImage.

[10]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[11]  E. Procyk,et al.  Reward encoding in the monkey anterior cingulate cortex. , 2006, Cerebral cortex.

[12]  Keiji Tanaka,et al.  Prefrontal Cell Activities Related to Monkeys' Success and Failure in Adapting to Rule Changes in a Wisconsin Card Sorting Test Analog , 2006, The Journal of Neuroscience.

[13]  Keiji Tanaka,et al.  Medial prefrontal cell activity signaling prediction errors of action values , 2007, Nature Neuroscience.

[14]  Kimberly L. Ray,et al.  Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions , 2012, Cognitive, affective & behavioral neuroscience.

[15]  William H. Alexander,et al.  Hierarchical Error Representation: A Computational Model of Anterior Cingulate and Dorsolateral Prefrontal Cortex , 2015, Neural Computation.

[16]  M. Farah,et al.  Is anterior cingulate cortex necessary for cognitive control? , 2005, Brain : a journal of neurology.

[17]  James L. McClelland,et al.  On the control of automatic processes: a parallel distributed processing account of the Stroop effect. , 1990, Psychological review.

[18]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[19]  Jordan Grafman,et al.  The role of prefrontal regions in the Stroop task , 1995, Neuropsychologia.

[20]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[21]  Jeffrey D. Schall,et al.  Conflict in Cingulate Cortex Function between Humans and Macaque Monkeys: More Apparent than Real , 2010, Brain, Behavior and Evolution.

[22]  B. Vogt,et al.  Architecture and neurocytology of monkey cingulate gyrus , 2005, The Journal of comparative neurology.

[23]  K. A. Hadland,et al.  The anterior cingulate and reward-guided selection of actions. , 2003, Journal of neurophysiology.

[24]  T. Egner,et al.  Using neural pattern classifiers to quantify the modularity of conflict-control mechanisms in the human brain. , 2014, Cerebral cortex.

[25]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[26]  B. Peterson,et al.  Adaptation to Conflict via Context-Driven Anticipatory Signals in the Dorsomedial Prefrontal Cortex , 2011, The Journal of Neuroscience.

[27]  D. Stuss,et al.  Stroop performance in focal lesion patients: dissociation of processes and frontal lobe lesion location , 2001, Neuropsychologia.

[28]  Parashkev Nachev,et al.  Volition and Conflict in Human Medial Frontal Cortex , 2005, Current Biology.

[29]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[30]  Timothy Edward John Behrens,et al.  Value, search, persistence and model updating in anterior cingulate cortex , 2016, Nature Neuroscience.

[31]  E. Murray,et al.  The role of the anterior cingulate cortex in choices based on reward value and reward contingency. , 2013, Cerebral cortex.

[32]  Keiji Tanaka,et al.  Neuronal Correlates of Goal-Based Motor Selection in the Prefrontal Cortex , 2003, Science.

[33]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[34]  Yoshikazu Isomura,et al.  Neural Coding of “Attention for Action” and “Response Selection” in Primate Anterior Cingulate Cortex , 2003, The Journal of Neuroscience.

[35]  John M. Pearson,et al.  Surprise Signals in Anterior Cingulate Cortex: Neuronal Encoding of Unsigned Reward Prediction Errors Driving Adjustment in Behavior , 2011, The Journal of Neuroscience.

[36]  Keiji Tanaka,et al.  The Essential Role of Primate Orbitofrontal Cortex in Conflict-Induced Executive Control Adjustment , 2014, The Journal of Neuroscience.

[37]  B. Vogt,et al.  Human cingulate cortex: Surface features, flat maps, and cytoarchitecture , 1995, The Journal of comparative neurology.

[38]  M. Rosa,et al.  Working Memory in the Service of Executive Control Functions , 2015, Front. Syst. Neurosci..

[39]  Thomas Michelet,et al.  Electrophysiological Correlates of a Versatile Executive Control System in the Monkey Anterior Cingulate Cortex. , 2016, Cerebral cortex.

[40]  Erich O. Richter,et al.  Human Anterior Cingulate Cortex Neurons Encode Cognitive and Emotional Demands , 2005, The Journal of Neuroscience.

[41]  T. Egner.  Creatures of habit (and control): a multi-level learning perspective on the modulation of congruency effects , 2014, Front. Psychol..

[42]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[43]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[44]  N. Cohen,et al.  The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. , 2001, Brain research. Cognitive brain research.

[45]  Timothy E. J. Behrens,et al.  Functional organization of the medial frontal cortex , 2007, Current Opinion in Neurobiology.

[46]  Keiji Tanaka,et al.  Behavioral evidence for working memory of sensory dimension in macaque monkeys , 2002, Behavioural Brain Research.

[47]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[48]  Joshua H. Balsters,et al.  The role of the midcingulate cortex in monitoring others' decisions , 2013, Front. Neurosci..

[49]  J S Fowler,et al.  Addiction changes orbitofrontal gyrus function: involvement in response inhibition , 2001, Neuroreport.

[50]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[51]  M. E. Walton,et al.  Cognitive Neuroscience: Resolving Conflict in and over the Medial Frontal Cortex , 2005, Current Biology.

[52]  M. Buckley,et al.  Distinct Roles for the Anterior Cingulate and Dorsolateral Prefrontal Cortices During Conflict Between Abstract Rules , 2016, Cerebral cortex.

[53]  Michael Petrides,et al.  Midcingulate Motor Map and Feedback Detection: Converging Data from Humans and Monkeys. , 2014, Cerebral cortex.

[54]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[55]  H. Seo,et al.  Temporal Filtering of Reward Signals in the Dorsal Anterior Cingulate Cortex during a Mixed-Strategy Game , 2007, The Journal of Neuroscience.

[56]  Massimo Silvetti,et al.  Value and Prediction Error in Medial Frontal Cortex: Integrating the Single-Unit and Systems Levels of Analysis , 2011, Front. Hum. Neurosci..

[57]  O. Hikosaka,et al.  Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex. , 2002, Journal of neurophysiology.

[58]  M. Roesch,et al.  Neuronal activity in macaque SEF and ACC during performance of tasks involving conflict. , 2005, Journal of neurophysiology.

[59]  G. Logan.  Skill and automaticity: Relations, implications, and future directions. , 1985 .

[60]  T. Egner,et al.  Determinants of congruency sequence effects without learning and memory confounds. , 2014, Journal of experimental psychology. Human perception and performance.

[61]  Tobias Egner,et al.  Simultaneous transcranial magnetic stimulation and single neuron recording in alert non-human primates , 2014, Nature Neuroscience.

[62]  Joshua W. Brown,et al.  Performance monitoring local field potentials in the medial frontal cortex of primates: supplementary eye field. , 2010, Journal of neurophysiology.

[63]  E. Procyk,et al.  Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex , 2008, Neuron.

[64]  Jonathan D. Cohen,et al.  The Expected Value of Control: An Integrative Theory of Anterior Cingulate Cortex Function , 2013, Neuron.

[65]  Brent A. Vogt,et al.  Midcingulate cortex: Structure, connections, homologies, functions and diseases , 2016, Journal of Chemical Neuroanatomy.

[66]  Shaun R. Patel,et al.  Human Dorsal Anterior Cingulate Cortex Neurons Mediate Ongoing Behavioral Adaptation , 2012, Nature.

[67]  H. van Steenbergen,et al.  Practice explains abolished behavioural adaptation after human dorsal anterior cingulate cortex lesions , 2015, Scientific Reports.

[68]  Michael W. Cole,et al.  Cingulate cortex: Diverging data from humans and monkeys , 2009, Trends in Neurosciences.

[69]  Veit Stuphorn,et al.  Role of supplementary eye field in saccade initiation: executive, not direct, control. , 2010, Journal of neurophysiology.

[70]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[71]  R. B. Ebitz,et al.  Neuronal Activity in Primate Dorsal Anterior Cingulate Cortex Signals Task Conflict and Predicts Adjustments in Pupil-Linked Arousal , 2015, Neuron.

[72]  M. Rushworth,et al.  Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex , 2015, Proceedings of the National Academy of Sciences.

[73]  Keiji Tanaka,et al.  Cognitive Control Functions of Anterior Cingulate Cortex in Macaque Monkeys Performing a Wisconsin Card Sorting Test Analog , 2014, The Journal of Neuroscience.

[74]  R. Mitchell,et al.  The BOLD response during Stroop task-like inhibition paradigms: Effects of task difficulty and task-relevant modality , 2005, Brain and Cognition.

[75]  Keiji Tanaka,et al.  Conflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex , 2009, Nature Reviews Neuroscience.

[76]  Philip G. F. Browning,et al.  Dissociable Components of Rule-Guided Behavior Depend on Distinct Medial and Prefrontal Regions , 2009, Science.

[77]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[78]  E. Awh,et al.  Conflict adaptation effects in the absence of executive control , 2003, Nature Neuroscience.

[79]  Karl J. Friston,et al.  Investigations of the functional anatomy of attention using the stroop test , 1993, Neuropsychologia.

[80]  Tobias Egner,et al.  An insula-frontostriatal network mediates flexible cognitive control by adaptively predicting changing control demands , 2015, Nature Communications.

[81]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[82]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[83]  Mark A. Straccia,et al.  Anterior Cingulate Engagement in a Foraging Context Reflects Choice Difficulty, Not Foraging Value , 2014, Nature Neuroscience.

[84]  Lawrence H Snyder,et al.  Single Neurons in Posterior Parietal Cortex of Monkeys Encode Cognitive Set , 2004, Neuron.

[85]  T. Egner.  Congruency sequence effects and cognitive control , 2007, Cognitive, affective & behavioral neuroscience.

[86]  C. Summerfield,et al.  Two Mechanisms for Task Switching in the Prefrontal Cortex , 2009, The Journal of Neuroscience.

[87]  Keiji Tanaka,et al.  Behavioral consequences of selective damage to frontal pole and posterior cingulate cortices , 2015, Proceedings of the National Academy of Sciences.

[88]  Michael W. Cole,et al.  Conflict over Cingulate Cortex: Between-Species Differences in Cingulate May Support Enhanced Cognitive Flexibility in Humans , 2010, Brain, Behavior and Evolution.

[89]  J. Duncan.  The Structure of Cognition: Attentional Episodes in Mind and Brain , 2013, Neuron.