The Location of Feedback-Related Activity in the Midcingulate Cortex Is Predicted by Local Morphology

Information processing in the medial frontal cortex is often said to be modulated in pathological conditions or by individual traits. This has been observed in neuroimaging and event-related potential studies centered in particular on midcingulate cortex (MCC) functions. This region of the brain is characterized by considerable intersubject morphological variability. Whereas in a subset of hemispheres only a single cingulate sulcus (cgs) is present, a majority of hemispheres exhibit an additional sulcus referred to as the paracingulate sulcus (pcgs). The present functional magnetic resonance imaging study defined the relationship between the local morphology of the cingulate/paracingulate sulcal complex and feedback-related activity. Human subjects performed a trial-and-error learning task in which they had to discover which one of a set of abstract stimuli was the best option. Feedback was provided by means of fruit juice, as in studies with monkeys. A subject-by-subject analysis revealed that the feedback-related activity during exploration was systematically located in the cgs when no pcgs was observed, but in the pcgs when the latter sulcus was present. The activations had the same functional signature when located in either the cgs or in the pcgs, confirming that both regions were homologues. Together, the results show that the location of feedback-related MCC activity can be predicted from morphological features of the cingulate/paracingulate complex.

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

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

[3]  J. Dreher,et al.  The Architecture of Reward Value Coding in the Human Orbitofrontal Cortex , 2010, The Journal of Neuroscience.

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

[5]  Keith D. White,et al.  Regional changes in word-production laterality after a naming treatment designed to produce a rightward shift in frontal activity , 2009, Brain and Language.

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

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

[8]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[9]  E. Procyk,et al.  The effects of sequence structure and reward schedule on serial reaction time learning in the monkey. , 2000, Brain research. Cognitive brain research.

[10]  Michael Petrides,et al.  Modulation of feedback related activity in the rostral anterior cingulate cortex during trial and error exploration , 2012, NeuroImage.

[11]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[12]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

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

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

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

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

[17]  D. Y. von Cramon,et al.  Functional organization of the left inferior precentral sulcus: Dissociating the inferior frontal eye field and the inferior frontal junction , 2012, NeuroImage.

[18]  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.

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

[20]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

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

[22]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[24]  Alan C. Evans,et al.  In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior‐rostral sulci: Hemispheric asymmetries, gender differences and probability maps , 1996, The Journal of comparative neurology.

[25]  Michael Petrides,et al.  Chapter 9. Feedback valuation processing within the prefrontal cortex , 2009 .

[26]  M. Petrides,et al.  Preoperative functional magnetic resonance imaging assessment of higher-order cognitive function in patients undergoing surgery for brain tumors. , 2008, Journal of neurosurgery.

[27]  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.

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

[29]  N. Bargalló,et al.  Anterior cingulate and paracingulate sulci morphology in patients with schizophrenia , 2010, Schizophrenia Research.

[30]  E. Rolls,et al.  Thirst following water deprivation in humans. , 1980, The American journal of physiology.

[31]  A. Berthoz,et al.  An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. , 1999, Cerebral cortex.

[32]  M. Mesulam,et al.  Brain mapping : from neural basis of cognition to surgical applications , 2011 .

[33]  S. Kastner,et al.  Complex organization of human primary motor cortex: a high-resolution fMRI study. , 2008, Journal of neurophysiology.

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

[35]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[36]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

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

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

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

[40]  Zara M. Bergström,et al.  A Specific Brain Structural Basis for Individual Differences in Reality Monitoring , 2011, The Journal of Neuroscience.