Dorsal Anterior Cingulate, Medial Superior Frontal Cortex, and Anterior Insula Show Performance Reporting‐Related Late Task Control Signals

Abstract The cingulo‐opercular network (including the dorsal anterior cingulate and bilateral anterior insula) shows 3 distinct task‐control signals across a wide variety of tasks, including trial‐related signals that appear to come online at or near the end of the trial. Previous work suggests that there are separable responses in this network for errors and ambiguity, implicating multiple types of processing units within these regions. Using a unique paradigm, we directly show that these separable responses withhold activity to the end of the trial, in the service of reporting performance back into the task set. Participants performed a slow reveal task where images were presented behind a black mask which was gradually degraded, and they pressed a button when they could recognize the object that was being revealed. A behavioral pilot was used to identify ambiguous stimuli. We found interactive effects of accuracy and ambiguity, which suggests that these regions are computing and utilizing information, at one time, about both types of performance indices. Importantly, we showed a relationship between cingulo‐opercular activity and behavioral performance, suggesting a role for these regions in performance reporting, per se. We discuss these results in the context of task control.

[1]  Matthew D. Lieberman,et al.  The dorsal anterior cingulate cortex is selective for pain: Results from large-scale reverse inference , 2015, Proceedings of the National Academy of Sciences.

[2]  Naoyuki Matsuzaki,et al.  Gamma activity modulated by naming of ambiguous and unambiguous images: Intracranial recording , 2015, Clinical Neurophysiology.

[3]  Joseph W. Dubis,et al.  Spatial and Temporal Characteristics of Error-Related Activity in the Human Brain , 2015, The Journal of Neuroscience.

[4]  Steven E. Petersen,et al.  Separable responses to error, ambiguity, and reaction time in cingulo-opercular task control regions , 2014, NeuroImage.

[5]  Joshua W. Brown,et al.  Distinct regions of anterior cingulate cortex signal prediction and outcome evaluation , 2014, NeuroImage.

[6]  Timothy E. J. Behrens,et al.  Dissociable effects of surprise and model update in parietal and anterior cingulate cortex , 2013, Proceedings of the National Academy of Sciences.

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

[8]  Paul J. Whalen,et al.  Neural Responses to Ambiguity Involve Domain-general and Domain-specific Emotion Processing Systems , 2013, Journal of Cognitive Neuroscience.

[9]  Markus Ullsperger,et al.  Surprise and Error: Common Neuronal Architecture for the Processing of Errors and Novelty , 2012, The Journal of Neuroscience.

[10]  Timothy E. J. Behrens,et al.  Neural Mechanisms of Foraging , 2012, Science.

[11]  Elisabeth J. Ploran,et al.  High quality but limited quantity perceptual evidence produces neural accumulation in frontal and parietal cortex. , 2011, Cerebral cortex.

[12]  Joshua W. Brown,et al.  Medial prefrontal cortex as an action-outcome predictor , 2011, Nature Neuroscience.

[13]  Tobias Teichert,et al.  The dorsal medial frontal cortex is sensitive to time on task, not response conflict or error likelihood , 2011, NeuroImage.

[14]  Joshua W. Brown Medial prefrontal cortex activity correlates with time-on-task: What does this tell us about theories of cognitive control? , 2011, NeuroImage.

[15]  Sabine Kastner,et al.  Functional heterogeneity of conflict, error, task-switching, and unexpectedness effects within medial prefrontal cortex , 2011, NeuroImage.

[16]  P. Whalen,et al.  The Primacy of Negative Interpretations When Resolving the Valence of Ambiguous Facial Expressions , 2010, Psychological science.

[17]  Maital Neta,et al.  Corrugator muscle responses are associated with individual differences in positivity-negativity bias. , 2009, Emotion.

[18]  Steven E. Petersen,et al.  Dissociating Early and Late Error Signals in Perceptual Recognition , 2008, Journal of Cognitive Neuroscience.

[19]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[20]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

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

[22]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[23]  L. Pessoa,et al.  Neural Correlates of Perceptual Choice and Decision Making during Fear–Disgust Discrimination , 2007, The Journal of Neuroscience.

[24]  Frans A. J. Verstraten,et al.  Dynamics of visual recognition revealed by fMRI , 2006, NeuroImage.

[25]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[26]  Abraham Z. Snyder,et al.  Transient BOLD responses at block transitions , 2005, NeuroImage.

[27]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

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

[29]  B. Rossion,et al.  Revisiting Snodgrass and Vanderwart's Object Pictorial Set: The Role of Surface Detail in Basic-Level Object Recognition , 2004, Perception.

[30]  Tom Johnstone,et al.  Inverse amygdala and medial prefrontal cortex responses to surprised faces , 2003, Neuroreport.

[31]  Jeffrey M. Zacks,et al.  Neural correlates of incongruous visual information An event-related fMRI study , 2003, NeuroImage.

[32]  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.

[33]  M. Petrides,et al.  Wisconsin Card Sorting Revisited: Distinct Neural Circuits Participating in Different Stages of the Task Identified by Event-Related Functional Magnetic Resonance Imaging , 2001, The Journal of Neuroscience.

[34]  K. R. Ridderinkhof,et al.  Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. , 2001, Psychophysiology.

[35]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[36]  Christine Preibisch,et al.  Neural Correlates of Spontaneous Direction Reversals in Ambiguous Apparent Visual Motion , 2001, NeuroImage.

[37]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

[38]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI I. The Method , 2001, NeuroImage.

[39]  Colin M. Macleod,et al.  Interdimensional interference in the Stroop effect: uncovering the cognitive and neural anatomy of attention , 2000, Trends in Cognitive Sciences.

[40]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[41]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[42]  Y. Miyashita,et al.  Transient activation of inferior prefrontal cortex during cognitive set shifting , 1998, Nature Neuroscience.

[43]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[44]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[46]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

[47]  B. Kopp,et al.  N200 in the flanker task as a neurobehavioral tool for investigating executive control. , 1996, Psychophysiology.

[48]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[49]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[50]  E. Donchin,et al.  Detecting early communication: Using measures of movement-related potentials to illuminate human information processing , 1988, Biological Psychology.

[51]  M. D’Esposito,et al.  Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. , 1997, NeuroImage.

[52]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[53]  R J Armitage,et al.  MONITORING OF PERFORMANCE , 1997 .

[54]  Alan C. Evans,et al.  Searching scale space for activation in PET images , 1996, Human brain mapping.

[55]  Abraham Z. Snyder,et al.  CHAPTER 26 – Difference Image vs Ratio Image Error Function Forms in PET—PET Realignment , 1996 .

[56]  Jack L. Lancaster,et al.  A modality‐independent approach to spatial normalization of tomographic images of the human brain , 1995 .

[57]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.