Midcingulate Motor Map and Feedback Detection: Converging Data from Humans and Monkeys.

The functional and anatomical organization of the cingulate cortex across primate species is the subject of considerable and often confusing debate. The functions attributed to the midcingulate cortex (MCC) embrace, among others, feedback processing, pain, salience, action-reward association, premotor functions, and conflict monitoring. This multiplicity of functional concepts suggests either unresolved separation of functional contributions or integration and convergence. We here provide evidence from recent experiments in humans and from a meta-analysis of monkey data that MCC feedback-related activity is generated in the rostral cingulate premotor area by specific body maps directly related to the modality of feedback. As such, we argue for an embodied mechanism for adaptation and exploration in MCC. We propose arguments and precise tools to resolve the origins of performance monitoring signals in the medial frontal cortex, and to progress on issues regarding homology between human and nonhuman primate cingulate cortex.

[1]  P. Strick,et al.  The Spinothalamic System Targets Motor and Sensory Areas in the Cerebral Cortex of Monkeys , 2009, The Journal of Neuroscience.

[2]  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.

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

[4]  J. Castro-Fornieles,et al.  The Human Cerebral Cortex Flattens during Adolescence , 2013, The Journal of Neuroscience.

[5]  P. Strick,et al.  Corticospinal projections from the medial wall of the hemisphere , 2004, Experimental Brain Research.

[6]  A. Schleicher,et al.  Receptor architecture of human cingulate cortex: Evaluation of the four‐region neurobiological model , 2009, Human brain mapping.

[7]  Brent A. Vogt,et al.  Cingulate Neurobiology and Disease , 2009 .

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

[9]  E. Procyk,et al.  Neuroanatomical Basis of Motivational and Cognitive Control: A Focus on the Medial and Lateral Prefrontal Cortex. , 2011 .

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

[11]  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.

[12]  Dennis Velakoulis,et al.  Variability of the paracingulate sulcus and morphometry of the medial frontal cortex: Associations with cortical thickness, surface area, volume, and sulcal depth , 2008, Human brain mapping.

[13]  C. Padoa-Schioppa,et al.  Neuronal Encoding of Subjective Value in Dorsal and Ventral Anterior Cingulate Cortex , 2012, The Journal of Neuroscience.

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

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

[16]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[17]  M. Petrides The Human Cerebral Cortex: An MRI Atlas of the Sulci and Gyri in MNI Stereotaxic Space , 2011 .

[18]  A. Schleicher,et al.  Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. , 1995, Journal of anatomy.

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

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

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

[22]  Andrew R Mitz,et al.  Somatotopy of monkey premotor cortex examined with microstimulation , 1995, Neuroscience Research.

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

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

[25]  Andrew R. Mitz,et al.  Eye-movement representation in the frontal lobe of rhesus monkeys , 1989, Neuroscience Letters.

[26]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[27]  Stephen A Coombes,et al.  Neuroimaging Evidence of Motor Control and Pain Processing in the Human Midcingulate Cortex. , 2015, Cerebral cortex.

[28]  M. Botvinick Conflict monitoring and decision making: Reconciling two perspectives on anterior cingulate function , 2007, Cognitive, affective & behavioral neuroscience.

[29]  M. Mallar Chakravarty,et al.  An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space) , 2011, NeuroImage.

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

[31]  Michael Petrides,et al.  Local Morphology Predicts Functional Organization of the Dorsal Premotor Region in the Human Brain , 2006, The Journal of Neuroscience.

[32]  Marion Smits,et al.  The anterior cingulate cortex responds differently to the validity and valence of feedback in a time-estimation task , 2011, NeuroImage.

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

[34]  Parashkev Nachev,et al.  The blind executive , 2011, NeuroImage.

[35]  J. Keifer,et al.  Organization of face representation in the cingulate cortex of the rhesus monkey. , 1996, NeuroReport.

[36]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[37]  N Palomero-Gallagher,et al.  Receptor autoradiographic mapping of the mesial motor and premotor cortex of the macaque monkey , 1998, The Journal of comparative neurology.

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

[39]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[40]  Daeyeol Lee,et al.  Behavioral and Neural Changes after Gains and Losses of Conditioned Reinforcers , 2009, The Journal of Neuroscience.

[41]  Brent A. Vogt,et al.  CHAPTER 1 Regions and Subregions of the Cingulate Cortex , 2009 .

[42]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[43]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Erich O. Richter,et al.  Cingulotomy for Psychiatric Disease: Microelectrode Guidance, a Callosal Reference System for Documenting Lesion Location, and Clinical Results , 2004, Neurosurgery.

[45]  S. Gong,et al.  Cerebral cortical control of orbicularis oculi motoneurons , 2005, Brain Research.

[46]  J. Tanji,et al.  Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity. , 2005, Journal of neurophysiology.

[47]  P. Strick,et al.  Spinal Cord Terminations of the Medial Wall Motor Areas in Macaque Monkeys , 1996, The Journal of Neuroscience.

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

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

[50]  M. Inase,et al.  Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements. , 1991, Journal of neurophysiology.

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

[52]  D Akkal,et al.  Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands , 2002, The European journal of neuroscience.

[53]  David W. McNeal,et al.  Amygdala interconnections with the cingulate motor cortex in the rhesus monkey , 2007, The Journal of comparative neurology.

[54]  N. Sadato,et al.  The anterior insular and anterior cingulate cortices in emotional processing for self-face recognition , 2013, Social cognitive and affective neuroscience.

[55]  E. Procyk,et al.  Anterior cingulate error‐related activity is modulated by predicted reward , 2005, The European journal of neuroscience.

[56]  G. Rizzolatti,et al.  Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey , 1991, The Journal of comparative neurology.

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

[58]  Sidney J. Segalowitz,et al.  Individual differences and developmental change in the ERN response: implications for models of ACC function , 2009, Psychological research.

[59]  P. Strick,et al.  Activation on the medial wall during remembered sequences of reaching movements in monkeys. , 1997, Journal of neurophysiology.

[60]  Alan C. Evans,et al.  Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. , 1996, Cerebral cortex.

[61]  M. Petrides,et al.  Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas. , 2014, Cerebral cortex.

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

[63]  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.

[64]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[66]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  G. Paxinos,et al.  The human cerebral cortex , 2010 .

[68]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[69]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[70]  G. Luppino,et al.  ß Federation of European Neuroscience Societies Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey , 2022 .

[71]  G. Bush Dorsal Anterior Midcingulate Cortex: Roles in Normal Cognition and Disruption in Attention-Defi cit/ Hyperactivity Disorder , 2015 .

[72]  Timothy S. Coalson,et al.  A Surface-Based Analysis of Hemispheric Asymmetries and Folding of Cerebral Cortex in Term-Born Human Infants , 2010, The Journal of Neuroscience.

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

[74]  Karl Zilles,et al.  Cytology and receptor architecture of human anterior cingulate cortex , 2008, The Journal of comparative neurology.

[75]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[77]  C. Woolsey,et al.  Patterns of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area. , 1952, Research publications - Association for Research in Nervous and Mental Disease.

[78]  E. Bizzi,et al.  Neuronal activity in the cingulate motor areas during adaptation to a new dynamic environment. , 2008, Journal of neurophysiology.

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

[80]  R. Morecraft,et al.  The Motor Cortex and Facial Expression:: New Insights From Neuroscience , 2004, The neurologist.

[81]  Atsushi Iriki,et al.  Social error monitoring in macaque frontal cortex , 2012, Nature Neuroscience.

[82]  N. Yeung,et al.  Neural basis of motivational and cognitive control , 2011 .

[83]  Jonathan D. Cohen,et al.  Computational roles for dopamine in behavioural control , 2004, Nature.

[84]  Kenneth Knoblauch,et al.  The Location of Feedback-Related Activity in the Midcingulate Cortex Is Predicted by Local Morphology , 2013, The Journal of Neuroscience.

[85]  M. Inase,et al.  Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey , 1997, The Journal of comparative neurology.

[86]  Atsushi Nambu,et al.  Somatotopic arrangement and corticocortical inputs of the hindlimb region of the primary motor cortex in the macaque monkey , 2001, Neuroscience Research.

[87]  Kathryn M. McMillan,et al.  A comparison of label‐based review and ALE meta‐analysis in the Stroop task , 2005, Human brain mapping.

[88]  S P Wise,et al.  The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[90]  Yan Wang,et al.  Cingulate cortical cells projecting to monkey frontal eye field and primary motor cortex , 2004, Neuroreport.