Distinct cerebellar contributions to intrinsic connectivity networks - PubMed (original) (raw)
Distinct cerebellar contributions to intrinsic connectivity networks
Christophe Habas et al. J Neurosci. 2009.
Abstract
Convergent data from various scientific approaches strongly implicate cerebellar systems in nonmotor functions. The functional anatomy of these systems has been pieced together from disparate sources, such as animal studies, lesion studies in humans, and structural and functional imaging studies in humans. To better define this distinct functional anatomy, in the current study we delineate the role of the cerebellum in several nonmotor systems simultaneously and in the same subjects using resting state functional connectivity MRI. Independent component analysis was applied to resting state data from two independent datasets to identify common cerebellar contributions to several previously identified intrinsic connectivity networks (ICNs) involved in executive control, episodic memory/self-reflection, salience detection, and sensorimotor function. We found distinct cerebellar contributions to each of these ICNs. The neocerebellum participates in (1) the right and left executive control networks (especially crus I and II), (2) the salience network (lobule VI), and (3) the default-mode network (lobule IX). Little to no overlap was detected between these cerebellar regions and the sensorimotor cerebellum (lobules V-VI). Clusters were also located in pontine and dentate nuclei, prominent points of convergence for cerebellar input and output, respectively. The results suggest that the most phylogenetically recent part of the cerebellum, particularly crus I and II, make contributions to parallel cortico-cerebellar loops involved in executive control, salience detection, and episodic memory/self-reflection. The largest portions of the neocerebellum take part in the executive control network implicated in higher cognitive functions such as working memory.
Figures
Figure 1.
Diagram of the flattened cerebellar surface. The four major subdivisions of the cerebellum are represented according to Schmahmann et al. (2000): (1) Division in lobes: anterior lobe (gray stipple), posterior lobe, and flocullo-nodular lobe, and in lobules numbered from I to X, (2) (para-)sagittal division: vermis and left and right hemispheres further subdivided into paravermis and lateral part of the hemispheres, and (3) phylogenetic division: archicerebellum (flocculonodular lobe in dark), paleocerebellum (green hachures), and neocerebellum (in white). The cerebellar cortex of the vermal, paravermal, and lateral hemispherical divisions projects during the fastigial (FN), globose/emboliform (G/EN), and dentate nuclei (DN), respectively. The main longitudinal fissures are also represented: AF, ansoparamedian fissure; HF, horizontal fissure; PLF, posterolateral fissure; PF, precentral fissure; PpF, prepyramidal fissure; PrF, primary fissure; SPF, superior posterior fissure.
Figure 2.
Cortical, subcortical, and cerebellar regions of the sensorimotor network. A, Cortical and subcortical regions of the sensorimotor network are shown on axial, coronal, and sagittal slices. B, Cerebellar regions are shown on coronal slices and in C on an axial slice. The left side of the image corresponds to the right side of the brain (radiologic convention). This is an intersection map showing only voxels that were present in the sensorimotor network of both datasets at a corrected threshold of p < 0.01. CN, Caudate nucleus; dMC, dorsal motormotor cingulate cortex; DN, dentate nucleus; PUT, putamen; RN, red nucleus; SMA, supplementary motor cortex; THAL, thalamus.
Figure 3.
Cortical, subcortical, and cerebellar regions of the default mode network. A, Cortical and subcortical regions of the default mode network are shown on axial, coronal, and sagittal slices. B, Cerebellar regions are shown on a coronal slice and in C on axial slices, which also highlight a pontine region. The left side of the image corresponds to the right side of the brain. This is an intersection map showing only voxels that were present in the default mode network of both datasets at a corrected threshold of p < 0.01. HC, Hippocampus; IPC, inferior parietal cortex; MPFC, median prefrontal cortex; PCC, posterior cingulate cortex; PHC, parahippocampal cortex; PN, pontine nucleus; RN, red nucleus; RSC, retrosplenial cortex.
Figure 4.
Cortical, subcortical, and cerebellar regions of the left executive control network. A, Cortical and subcortical regions of the left executive control network are shown on axial, coronal, and sagittal slices. B, C, Cerebellar regions are shown on coronal slices (B), and on an axial slice (C), which also highlights a pontine region. The left side of the image corresponds to the right side of the brain. This is an intersection map showing only voxels that were present in the left executive control network of both datasets at a corrected threshold of p < 0.01. CN, Caudate nucleus; DLPFC, dorsolateral prefrontal cortex; DMPFC, dorsomedial prefrontal cortex; PN, pontine nucleus; SPC, superior parietal cortex; THAL, thalamus.
Figure 5.
Cortical, subcortical, and cerebellar regions of the right executive control network. A, Cortical and subcortical regions of the right executive control network are shown on axial, coronal, and sagittal slices. B, Cerebellar regions are shown on coronal slices and in C on an axial slice, which also highlights a pontine region. The left side of the image corresponds to the right side of the brain. This is an intersection map showing only voxels that were present in the right executive control network of both datasets at a corrected threshold of p < 0.01. CN, Caudate nucleus; DLPFC, dorsolateral prefrontal cortex; DMPFC, dorsomedial prefrontal cortex; PN, pontine nucleus; SPC, superior parietal cortex.
Figure 6.
Cortical, subcortical, and cerebellar regions of the salience network. A, Cortical and subcortical regions of the salience network are shown on axial, coronal, and sagittal slices. B, C, Cerebellar regions are shown on coronal slices (B), and on an axial slice (C). The left side of the image corresponds to the right side of the brain. This is an intersection map showing only voxels that were present in the salience network of both datasets at a corrected threshold of p < 0.01.CN, Caudate nucleus; dACC, dorsal anterior cingulate; DN, dentate nucleus; INS, insula; RN, red nucleus; THAL, thalamus.
Figure 7.
Distinct cerebellar contributions to the five intrinsic connectivity networks. The cerebellar clusters from all five ICN maps are overlayed on the same axial slices. With rare exceptions, such as the cluster in left lobule VI (at slices z = −24 and z = −19) which contributes to the sensorimotor and salience networks, there is remarkably little cerebellar overlap across the five ICNs. SPS, Superior posterior sulcus.
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References
- Allen G, McColl R, Barnard H, Ringe WK, Fleckenstein J, Cullum CM. Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. Neuroimage. 2005;28:39–48. - PubMed
- Azizi SA, Mihailoff GA, Burne RA, Woodward DJ. The pontocerebellar system in the rat: an HRP study. I. Posterior vermis. J Comp Neurol. 1981;197:543–548. - PubMed
- Beckmann CF, Smith SM. Tensorial extension of independent component analysis for multi-subject FMRI analysis. IEEE Trans Med Imaging. 2004;23:137–152. - PubMed
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