Parcellation of the cingulate cortex at rest and during tasks: a meta-analytic clustering and experimental study

Anatomical, morphological, and histological data have consistently shown that the cingulate cortex can be divided into four main regions. However, less is known about parcellations of the cingulate cortex when involved in active tasks. Here, we aimed at comparing how the pattern of clusterization of the cingulate cortex changes across different levels of task complexity. We parcellated the cingulate cortex using the results of a meta-analytic study and of three experimental studies. The experimental studies, which included two active tasks and a resting state protocol, were used to control the results obtained with the meta-analytic parcellation. We explored the meta-analytic parcellation by applying a meta-analytic clustering (MaC) to papers retrieved from the BrainMap database. The MaC is a meta-analytic connectivity driven parcellation technique recently developed by our group which allowed us to parcellate the cingulate cortex on the basis of its pattern of co-activations during active tasks. The MaC results indicated that the cingulate cortex can be parcellated into three clusters. These clusters covered different percentages of the cingulate parenchyma and had a different density of foci, with the first cluster being more densely connected. The control experiments showed different clusterization results, suggesting that the co-activations of the cingulate cortex are highly dependent on the task that is tested. Our results highlight the importance of the cingulate cortex as a hub, which modifies its pattern of co-activations depending on the task requests and on the level of task complexity. The neurobiological meaning of these results is discussed.

[1]  Brain activity. , 2014, Nature nanotechnology.

[2]  Franco Cauda,et al.  How many clusters in the insular cortex? , 2013, Cerebral cortex.

[3]  K. Zilles,et al.  An investigation of the structural, connectional, and functional subspecialization in the human amygdala , 2012, Human brain mapping.

[4]  Anastasia Konsta,et al.  Cingulate Neurobiology and Disease, B.A. Vogt (Ed.). Oxford University Press Inc., New York (2009), ISBN: 978-0-19-856696-0 , 2012 .

[5]  Katiuscia Sacco,et al.  Meta-analytic clustering of the insular cortex Characterizing the meta-analytic connectivity of the insula when involved in active tasks , 2012, NeuroImage.

[6]  Ning Zhong,et al.  Changes in the brain intrinsic organization in both on-task state and post-task resting state , 2012, NeuroImage.

[7]  Michael P. Milham,et al.  A convergent functional architecture of the insula emerges across imaging modalities , 2012, NeuroImage.

[8]  Rodrigo M. Braga,et al.  Echoes of the Brain within the Posterior Cingulate Cortex , 2012, The Journal of Neuroscience.

[9]  Katiuscia Sacco,et al.  Functional anatomy of cortical areas characterized by Von Economo neurons , 2012, Brain Structure and Function.

[10]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[11]  Simon B. Eickhoff,et al.  Coordinate-based meta-analysis of experimentally induced and chronic persistent neuropathic pain , 2011, NeuroImage.

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

[13]  Franco Cauda,et al.  Different functions in the cingulate cortex, a meta-analytic connectivity modeling study , 2011, NeuroImage.

[14]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[15]  K. Sacco,et al.  Unawareness of deficits in Alzheimer's disease: role of the cingulate cortex. , 2011, Brain : a journal of neurology.

[16]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[17]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

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

[19]  Yuan Zhou,et al.  Functional segregation of the human cingulate cortex is confirmed by functional connectivity based neuroanatomical parcellation , 2011, NeuroImage.

[20]  A. Cavanna,et al.  Functional Connectivity of the Posteromedial Cortex , 2010, PloS one.

[21]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[22]  U. Baumgärtner,et al.  Multiple somatotopic representations of heat and mechanical pain in the operculo-insular cortex: a high-resolution fMRI study. , 2010, Journal of neurophysiology.

[23]  H. Critchley,et al.  Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response , 2010, Brain Structure and Function.

[24]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[25]  Nicholas A. Ketz,et al.  Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences , 2010, Neuron.

[26]  P. Fox,et al.  Metaanalytic connectivity modeling: Delineating the functional connectivity of the human amygdala , 2009, Human brain mapping.

[27]  Rune Matthiesen,et al.  Overview on techniques in cluster analysis. , 2010, Methods in molecular biology.

[28]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[29]  Angela R. Laird,et al.  Lost in localization? The focus is meta-analysis , 2009, NeuroImage.

[30]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[31]  Remco J. Renken,et al.  Group analyses of connectivity-based cortical parcellation using repeated k-means clustering , 2009, NeuroImage.

[32]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[33]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

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

[35]  H. Nusbaum,et al.  Task-dependent organization of brain regions active during rest , 2009, Proceedings of the National Academy of Sciences.

[36]  I Daubechies,et al.  Independent component analysis for brain fMRI does not select for independence , 2009 .

[37]  Jessica A. Turner,et al.  Neuroinformatics Original Research Article , 2022 .

[38]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[39]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[40]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[41]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[42]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[43]  David J Bucci,et al.  Neurotoxic lesions of retrosplenial cortex disrupt signaled and unsignaled contextual fear conditioning. , 2008, Behavioral neuroscience.

[44]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[45]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[46]  M. Posner,et al.  The functional integration of the anterior cingulate cortex during conflict processing. , 2008, Cerebral cortex.

[47]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[48]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[49]  M. Petrides,et al.  Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps , 2007, The European journal of neuroscience.

[50]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[51]  A. Dagher,et al.  Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. , 2006, Cerebral cortex.

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

[53]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[54]  Guang H. Yue,et al.  Reductions in interhemispheric motor cortex functional connectivity after muscle fatigue , 2005, Brain Research.

[55]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

[56]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[57]  Angela R Laird,et al.  Brainmap taxonomy of experimental design: Description and evaluation , 2005, Human brain mapping.

[58]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[59]  G. Jackson,et al.  Effect of prior cognitive state on resting state networks measured with functional connectivity , 2005, Human brain mapping.

[60]  Angela R. Laird,et al.  BrainMap , 2007, Neuroinformatics.

[61]  Steven Laureys,et al.  Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. , 2005, Progress in brain research.

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

[63]  Tianzi Jiang,et al.  Modulation of functional connectivity during the resting state and the motor task , 2004, Human brain mapping.

[64]  Brent A. Vogt,et al.  Cytology of human dorsal midcingulate and supplementary motor cortices , 2003, Journal of Chemical Neuroanatomy.

[65]  B. Vogt,et al.  Structural and functional dichotomy of human midcingulate cortex , 2003, The European journal of neuroscience.

[66]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[67]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[68]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[69]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

[70]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[71]  W. Gehring,et al.  Functions of the Medial Frontal Cortex in the Processing of Conflict and Errors , 2001, The Journal of Neuroscience.

[72]  B. Vogt,et al.  Cytology of human caudomedial cingulate, retrosplenial, and caudal parahippocampal cortices , 2001, The Journal of comparative neurology.

[73]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[74]  J. Allman,et al.  The Anterior Cingulate Cortex , 2001, Annals of the New York Academy of Sciences.

[75]  J. Lurito,et al.  Correlations in Low-Frequency BOLD Fluctuations Reflect Cortico-Cortical Connections , 2000, NeuroImage.

[76]  Karl J. Friston,et al.  Attentional modulation of effective connectivity from V2 to V5/MT in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[77]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[78]  T. Paus,et al.  Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis , 2000, Experimental Brain Research.

[79]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[80]  Edward Awh,et al.  The anterior cingulate cortex lends a hand in response selection , 1999, Nature Neuroscience.

[81]  P. Fox,et al.  Temporal dissociation of parallel processing in the human subcortical outputs , 1999, Nature.

[82]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[83]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

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

[85]  Michael I. Posner,et al.  Mapping the Cingulate Cortex in Response Selection and Monitoring , 1998, NeuroImage.

[86]  Clay B. Holroyd,et al.  Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans , 1998, Neuroscience Letters.

[87]  Amanda Parker,et al.  The effect of anterior thalamic and cingulate cortex lesions on object-in-place memory in monkeys , 1997, Neuropsychologia.

[88]  P. Ekman,et al.  Matsumoto and Ekman's Japanese and Caucasian Facial Expressions of Emotion (JACFEE): Reliability Data and Cross-National Differences , 1997 .

[89]  Alan C. Evans,et al.  Anticipation causes increased blood flow to the anterior cingulate cortex , 1996, Human brain mapping.

[90]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[91]  M. Posner,et al.  Attentional networks , 1994, Trends in Neurosciences.

[92]  Ioannis G. Tollis,et al.  Graph Drawing , 1994, Lecture Notes in Computer Science.

[93]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[94]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[95]  Edward M. Reingold,et al.  Graph drawing by force‐directed placement , 1991, Softw. Pract. Exp..

[96]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[97]  Rolf Klein,et al.  Concrete and Abstract Voronoi Diagrams , 1990, Lecture Notes in Computer Science.

[98]  Azriel Rosenfeld,et al.  Computer Vision , 1988, Adv. Comput..

[99]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[100]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[101]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[102]  R. Mojena,et al.  Hierarchical Grouping Methods and Stopping Rules: An Evaluation , 1977, Comput. J..

[103]  W. Wilson,et al.  Pain and emotion. , 1970, Postgraduate medicine.

[104]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[105]  E. Benarroch Executive Control , 2022, Neuroscience for Clinicians.