Specific frontal neural dynamics contribute to decisions to check

Curiosity and information seeking potently shapes our behaviour and are thought to rely on the frontal cortex. Yet, the frontal regions and neural dynamics that control the drive to check for information remain unknown. Here we trained monkeys in a task where they had the opportunity to gain information about the potential delivery of a large bonus reward or continue with a default instructed decision task. Single-unit recordings in behaving monkeys reveal that decisions to check for additional information first engage midcingulate cortex and then lateral prefrontal cortex. The opposite is true for instructed decisions. Importantly, deciding to check engages neurons also involved in performance monitoring. Further, specific midcingulate activity could be discerned several trials before the monkeys actually choose to check the environment. Our data show that deciding to seek information on the current state of the environment is characterized by specific dynamics of neural activity within the prefrontal cortex.

[1]  Peter Dalgaard,et al.  R Development Core Team (2010): R: A language and environment for statistical computing , 2010 .

[2]  T. Womelsdorf,et al.  Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts , 2015, Proceedings of the National Academy of Sciences.

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

[4]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[5]  Xavier A. Harrison,et al.  Using observation-level random effects to model overdispersion in count data in ecology and evolution , 2014, PeerJ.

[6]  Joseph R. Smith,et al.  Historic Evolution of Open Cingulectomy and Stereotactic Cingulotomy in the Management of Medically Intractable Psychiatric Disorders, Pain and Drug Addiction , 2009, Stereotactic and Functional Neurosurgery.

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

[8]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[9]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[10]  Ethan S. Bromberg-Martin,et al.  Midbrain Dopamine Neurons Signal Preference for Advance Information about Upcoming Rewards , 2009, Neuron.

[11]  Henry Kennedy,et al.  Cortical High-Density Counterstream Architectures , 2013, Science.

[12]  Xiao-Jing Wang Decision Making in Recurrent Neuronal Circuits , 2008, Neuron.

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

[14]  S. Kennerley,et al.  Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables , 2009, The European journal of neuroscience.

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

[16]  Jeffrey D Schall,et al.  Performance monitoring local field potentials in the medial frontal cortex of primates: supplementary eye field. , 2010, Journal of neurophysiology.

[17]  Pierre-Yves Oudeyer,et al.  Information-seeking, curiosity, and attention: computational and neural mechanisms , 2013, Trends in Cognitive Sciences.

[18]  Stefan Everling,et al.  Specific Contributions of Ventromedial, Anterior Cingulate, and Lateral Prefrontal Cortex for Attentional Selection and Stimulus Valuation , 2011, PLoS biology.

[19]  Cedric E. Ginestet ggplot2: Elegant Graphics for Data Analysis , 2011 .

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

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

[22]  J. Wallis,et al.  Dynamic Encoding of Responses and Outcomes by Neurons in Medial Prefrontal Cortex , 2009, The Journal of Neuroscience.

[23]  G. Feng,et al.  Striatal circuits, habits, and implications for obsessive–compulsive disorder , 2014, Current Opinion in Neurobiology.

[24]  Timothy E. J. Behrens,et al.  Perceptual Classification in a Rapidly Changing Environment , 2011, Neuron.

[25]  Timothy E. J. Behrens,et al.  Double dissociation of value computations in orbitofrontal and anterior cingulate neurons , 2011, Nature Neuroscience.

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

[27]  R H S Carpenter,et al.  Supplementary Eye Field: Keeping an Eye on Eye Movement , 2004, Current Biology.

[28]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[29]  Daniel N Hill,et al.  Quality Metrics to Accompany Spike Sorting of Extracellular Signals , 2011, The Journal of Neuroscience.

[30]  John M. Pearson,et al.  Neuronal basis of sequential foraging decisions in a patchy environment , 2011, Nature Neuroscience.

[31]  K. N’diaye,et al.  Excessive checking for non-anxiogenic stimuli in obsessive-compulsive disorder , 2013, European Psychiatry.

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

[33]  M. Ullsperger,et al.  Specificity of performance monitoring changes in obsessive-compulsive disorder , 2014, Neuroscience & Biobehavioral Reviews.

[34]  Elisabeth A. Murray,et al.  Rhesus monkeys (Macaca mulatta) discriminate between knowing and not knowing and collect information as needed before acting , 2004, Animal Cognition.

[35]  Peter Ford Dominey,et al.  Comparison of Classifiers for Decoding Sensory and Cognitive Information from Prefrontal Neuronal Populations , 2014, PloS one.

[36]  E. Procyk,et al.  Anterior cingulate activity during routine and non-routine sequential behaviors in macaques , 2000, Nature Neuroscience.

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

[38]  Peter Ford Dominey,et al.  Behavioral Regulation and the Modulation of Information Coding in the Lateral Prefrontal and Cingulate Cortex. , 2015, Cerebral cortex.

[39]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[40]  Etienne Koechlin,et al.  Foundations of human reasoning in the prefrontal cortex , 2014, Science.

[41]  K. Johnston,et al.  Top-Down Control-Signal Dynamics in Anterior Cingulate and Prefrontal Cortex Neurons following Task Switching , 2007, Neuron.

[42]  James F. Cavanagh,et al.  Altered cingulate sub-region activation accounts for task-related dissociation in ERN amplitude as a function of obsessive-compulsive symptoms , 2010, Neuropsychologia.

[43]  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.

[44]  M. Rushworth,et al.  Valuation and decision-making in frontal cortex: one or many serial or parallel systems? , 2012, Current Opinion in Neurobiology.

[45]  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.

[46]  D. Berlyne Curiosity and exploration. , 1966, Science.

[47]  M. Kerszberg,et al.  A Neuronal Model of a Global Workspace in Effortful Cognitive Tasks , 2001 .

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

[49]  Joshua W. Brown,et al.  Computational and neural mechanisms of task switching , 2006, Neurocomputing.

[50]  B. Aouizerate,et al.  Pathophysiology of obsessive–compulsive disorder A necessary link between phenomenology, neuropsychology, imagery and physiology , 2004, Progress in Neurobiology.

[51]  G. Loewenstein The psychology of curiosity: A review and reinterpretation. , 1994 .

[52]  Emmanuel Procyk,et al.  Coordination of High Gamma Activity in Anterior Cingulate and Lateral Prefrontal Cortical Areas during Adaptation , 2011, The Journal of Neuroscience.

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