Functional connectivity of the human rostral and caudal cingulate motor areas in the brain resting state at 3T

IntroductionThree cingulate motor areas have been described in monkeys, the rostral, dorsal, and ventral cingulate motor areas, and would control limbic-related motor activity. However, little anatomical data are available in human about the functional networks these cingulate areas underlie. Therefore, networks anchored in the rostral and caudal cingulate motor areas (rCMA and cCMA, respectively) were studied in human using functional connectivity during the brain resting state. Since the rCMA and cCMA are located just under the pre-supplementary and supplementary motor areas (pre-SMA and SMA), the pre-SMA- and SMA-centered networks were also studied to ensure that these four circuits were correctly dissociated.MethodsData from 14 right-handed healthy volunteers were acquired at rest and analyzed by region of interest (ROI)-based functional connectivity. The blood oxygenation level-dependent (BOLD) signal fluctuations of separate ROIs located in rCMA, cCMA, pre-SMA, and SMA were successively used to identify significant temporal correlations with BOLD signal fluctuations of other brain regions.ResultsLow-frequency BOLD signal of the CMA was correlated with signal fluctuations in the prefrontal, cingulate, insular, premotor, motor, medial and inferior parietal cortices, putamen and thalamus, and anticorrelated with the default-mode network. rCMA was more in relation with prefrontal, orbitofrontal, and language-associated cortices than cCMA more related to sensory cortex. These cingulate networks were very similar to the pre-SMA- and SMA-centered networks, although pre-SMA and SMA showed stronger correlation with the prefrontal and inferior parietal cortices and with the cerebellum and the superior parietal cortex, respectively.ConclusionThe human cingulate motor areas constitute an interface between sensorimotor, limbic and executive systems, sharing common cortical, striatal, and thalamic relays with the overlying premotor medial areas.

[1]  G. Rizzolatti,et al.  The Organization of the Frontal Motor Cortex. , 2000, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[2]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[3]  G. S. Russo,et al.  Neural activity in monkey dorsal and ventral cingulate motor areas: comparison with the supplementary motor area. , 2002, Journal of neurophysiology.

[4]  K. Rockland,et al.  Localization of area prostriata and its projection to the cingulate motor cortex in the rhesus monkey. , 2000, Cerebral cortex.

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

[6]  M. Inase,et al.  Organization of inputs from cingulate motor areas to basal ganglia in macaque monkey , 2001, The European journal of neuroscience.

[7]  Ivan Toni,et al.  Neural dynamics of error processing in medial frontal cortex , 2005, NeuroImage.

[8]  M. Greicius.  Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

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

[10]  J. Voogd,et al.  The human central nervous system , 1978 .

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

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

[13]  Emily S. Cross,et al.  Building a motor simulation de novo: Observation of dance by dancers , 2006, NeuroImage.

[14]  W. Prinz,et al.  Dissociating What and When of Intentional Actions , 2009, Front. Hum. Neurosci..

[15]  Lorenzo Ll.  Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas , 2008 .

[16]  Takashi Hanakawa,et al.  The representation of blinking movement in cingulate motor areas: a functional magnetic resonance imaging study. , 2008, Cerebral cortex.

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

[18]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[19]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[20]  M. Brázdil,et al.  Rostral cingulate motor area and paroxysmal alien hand syndrome , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[21]  P. B. Cipolloni,et al.  Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey , 2004, The Journal of comparative neurology.

[22]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[23]  Jan Voogd,et al.  The human central nervous system : a synopsis and atlas , 1978 .

[24]  K. Zilles,et al.  The role of ventral medial wall motor areas in bimanual co-ordination. A combined lesion and activation study. , 1999, Brain : a journal of neurology.

[25]  Noriaki Hattori,et al.  Discrete parieto-frontal functional connectivity related to grasping. , 2009, Journal of neurophysiology.

[26]  G. V. Van Hoesen,et al.  Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey , 1993, The Journal of comparative neurology.

[27]  Jörn Diedrichsen,et al.  Neural substrates of visuomotor learning based on improved feedback control and prediction , 2008, NeuroImage.

[28]  Naomi Hasegawa,et al.  Thalamocortical and intracortical connections of monkey cingulate motor areas , 2003, The Journal of comparative neurology.

[29]  Philippe Mailly,et al.  Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: an anatomical substrate for cognition to action , 2007, The European journal of neuroscience.

[30]  Aaron L. Berkowitz,et al.  Generation of novel motor sequences: The neural correlates of musical improvisation , 2008, NeuroImage.

[31]  R. Morecraft,et al.  Convergence of Limbic Input to the Cingulate Motor Cortex in the Rhesus Monkey , 1998, Brain Research Bulletin.

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

[33]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[34]  Wolfgang Prinz,et al.  The role of the preSMA and the rostral cingulate zone in internally selected actions , 2007, NeuroImage.