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Focal Pontine Lesions Provide Evidence That Intrinsic Functional Connectivity Reflects Polysynaptic Anatomical Pathways

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Focal Pontine Lesions Provide Evidence That Intrinsic Functional Connectivity Reflects Polysynaptic Anatomical Pathways The Journal of Neuroscience, October 19, 2011 • 31(42):15065–15071 • 15065 Behavioral/Systems/Cognitive Focal Pontine Lesions Provide Evidence That Intrinsic Functional Connectivity Reflects Polysynaptic Anatomical Pathways Jie Lu,1* Hesheng Liu,3* Miao Zhang,1 Danhong Wang,3 Yanxiang Cao,1 Qingfeng Ma,2 Dongdong Rong,1 Xiaoyi Wang,1 Randy L. Buckner,3,4,5,6 and Kuncheng Li1 Departments of 1Radiology and 2Neurology, Xuanwu Hospital of Capital Medical University, Beijing 100053, China, 3Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology and 4Department of Psychiatry, Massachusetts General Hospital, Charlestown, Massachusetts 02129, 5Psychology and Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and 6Howard Hughes Medical Institute, Cambridge, Massachusetts 02138 Intrinsic functional connectivity detected by functional MRI (fMRI) provides a useful but indirect approach to study the organization of human brain systems. An unresolved question is whether functional connectivity measured by resting-state fMRI reflects anatomical connections. In this study, we used the well-characterized anatomy of cerebrocerebellar circuits to directly test whether intrinsic func- tional connectivity is associated with an anatomic pathway. Eleven first-episode stroke patients were scanned five times during a period of 6 months, and 11 healthy control subjects were scanned three times within 1 month. In patients with right pontine strokes, the functional connectivity between the right motor cortex and the left cerebellum was selectively reduced. This connectivity pattern was reversed in patients with left pontine strokes. Although factors beyond anatomical connectivity contribute to fMRI measures of func- tional correlation, these results provide direct evidence that functional connectivity depends on intact connections within a specific polysynaptic pathway. Introduction velopment, advanced aging, and in brain disease (Greicius, 2008; Intrinsic functional connectivity MRI (fcMRI) provides an indi- Fornito and Bullmore, 2010; Fox and Greicius, 2010; Vogel et al., rect approach to measure the organization of brain systems 2010; Zhang and Raichle, 2010). (Biswal et al., 1995; for review, see Fox and Raichle, 2007; Cole et Recent studies further suggest that intrinsic functional con- al., 2010; Van Dijk et al., 2010). The method takes advantage nectivity reflects polysynaptic connections. A particularly inter- of spontaneous fluctuations in the blood oxygenation level- esting observation is that intrinsic functional connectivity reveals dependent fMRI signal that are coupled selectively between cer- cerebrocerebellar circuits that are exclusively polysynaptic (Ha- tain regions. Although the physiological basis of the slow intrinsic bas et al., 2009; Krienen and Buckner, 2009; O’Reilly et al., 2010; activity fluctuations that underlie fcMRI remain incompletely Buckner et al., 2011). Intrinsic fluctuations in the motor cortex, understood, the correlation patterns suggest that a major (but for example, are functionally coupled to their topographically not exclusive) determinant of functional coupling is anatomic appropriate contralateral regions in the anterior lobe of the cer- connectivity (Vincent et al., 2007; Greicius et al., 2009; Honey et ebellum (Buckner et al., 2011). A direct test of the relation be- al., 2009; Margulies et al., 2009). fcMRI has been widely used to tween fcMRI and anatomic connectivity thus would be to understand the architecture of human brain systems during de- examine functional connectivity in cases in which anatomical pathways are selectively disrupted. A recent study showed that severing the corpus callosum reduces functional correlation be- Received May 11, 2011; revised Aug. 22, 2011; accepted Aug. 26, 2011. tween homologous regions in the left and right hemispheres Author contributions: J.L., H.L., R.L.B., and K.L. designed research; J.L., H.L., M.Z., Y.C., Q.M., D.R., and K.L. performed research; K.L. contributed unpublished reagents/analytic tools; H.L., D.W., and X.W. analyzed data; H.L., (Johnston et al., 2008). R.L.B., and J.L. wrote the paper. In the present study, we used the well-characterized anatomy ThisworkwassupportedbyNINDSGrantK25NS069805,NIAGrantAG021910,NCRRGrantP41RR14074,andthe of the cerebro-ponto-cerebellar pathway to directly test whether Howard Hughes Medical Institute. We thank Fenna Krienen, Avram Holmes, and Jorge Sepulcre for assistance with functional connectivity is dependent on a specific polysynaptic data analysis, Judith Schaechter for discussion of behavioral assessment, Jeremy Schmahmann for discussion of anatomy, and Haderer & Mu¨ller Biomedical Art for illustration. pathway (Evarts and Thach, 1969; Kemp and Powell, 1971; *J.L. and H.L. contributed equally to this work. Strick, 1985; Schmahmann and Pandya, 1997). Cortical areas Correspondence should be addressed to either of the following: Dr. Kuncheng Li, Department of Radiology, project predominantly to the contralateral cerebellum via effer- Xuanwu Hospital of Capital Medical University, Beijing 100053, China, E-mail: [email protected]; or ents to the pons and then to the cerebellar cortex. Afferents pass Dr. Randy Buckner, Psychology and Center for Brain Science, Harvard University, Cambridge, MA 02138, E-mail: [email protected]. through the deep cerebellar nuclei and then to the thalamus (see DOI:10.1523/JNEUROSCI.2364-11.2011 Fig. 3A). These connections are organized as closed, parallel cir- Copyright © 2011 the authors 0270-6474/11/3115065-07$15.00/0 cuits: neocortical areas receive input from the same cerebellar 15066 • J. Neurosci., October 19, 2011 • 31(42):15065–15071 Lu et al. • Resting-State Connectivity Table 1. Demography and clinical characteristics of the patients Subject Gender Age (years) Handedness Lesion side Lesion description Symptoms 045 F 34 L L (mainly) L PVTML R PVM R hemiparesis, dysarthria 024 M 48 R L PVU R hemiparesis, dysarthria 022 M 59 R L PVML R hemiparesis, dysarthria 096 M 62 R L PVL R hemiparesis, dizziness 015 F 54 R R VLU L hemiparesis 084 M 56 R R PVML L hemiparesis 021 M 57 R R PVTML L hemiparesis 057 M 60 L R PVTUM L hemiparesis, dizziness 072 M 61 R R PVML L hemiparesis, dysarthria 038 M 63 R R PVU L pure motor hemiparesis 090 M 68 R R PVL L pure motor hemiparesis, dizziness F, Female; M, male; L, left; R, right. Table 2. Motor performance measured during five visits for each subject Subject ID FM1 FM2 FM3 FM4 FM5 FMC1 FMC2 FMC3 FMC4 FMC5 045 25.0 97.0 93.9 100.0 N/A 0556N/A 024 50.0 68.2 75.8 74.2 78.0 33356 022 66.7 81.8 86.4 100.0 97.0 3 4.5 5 6 6 096 72.7 90.2 98.5 90.9 98.5 66656 015 75.0 90.9 95.5 98.5 100.0 34566 084 44.7 14.4 40.2 43.2 57.5 10032 021 88.6 94.7 96.2 100.0 99.2 4 4 4.5 6 6 057 42.4 59.9 84.9 98.5 100.0 0.5 1466 072 75.0 90.9 99.2 98.5 97.0 15665 038 62.9 83.3 96.2 100.0 100.0 2 2 3.5 6 6 090 100.0 100.0 100.0 100.0 100.0 66666 FM, Fugl–Meyer score; FMC, motor coordination score; the numbers indicate visit number (e.g., FM2 is the second visit). Each score represents the average score of two independent raters. regions to which they project (Middleton and Strick, 2001). A confined to the pons identified on MRI, and no other concomitant brain recent anatomical study revealed that the pontocerebellar fibers lesion or previous infarcts. The exclusion criteria were as follows: contra- cross the midline horizontally and then disperse widely in the indications for MRI, unclear onset of symptoms, lesions outside the pons opposite hemipons before regrouping in the brachium pontis or extensive infarcts involving the midbrain or the medulla, recurrence (Schmahmann et al., 2004a). Because of this anatomical arrange- infarction or secondary hemorrhage during follow-up, deafness and/or ment of pontocerebellar fibers, focal lesions to the pons (which blindness, aphasia, or a visual field deficit. Eleven healthy control subjects arise from infarcts involving small penetrating branches of (matched to the patients on age, gender, and handedness) were recruited and scanned three times within 1 month (between-scan interval was the basilar artery) disrupt the efferent connections to the con- 15 d). Written informed consent was obtained from all participants un- tralateral cerebellum but mostly spare ipsilateral connections der the guidelines of Xuanwu Hospital of Capital Medical University. (Schmahmann et al., 2004a,b). Lesions of the basilar pons thus MRI data acquisition. Patients were scanned five times during a period create a rare opportunity to study the effects on functional cou- of 6 months (7, 14, 30, 90, and 180 d after stroke onset). Scanning was pling after disruption of a specific anatomic pathway. performed on a 3 tesla TimTrio system (Siemens) using the 12-channel We investigated the resting-state functional correlation be- phased-array head coil supplied by the vendor. Structural images were tween the cerebral cortex and the cerebellum in first-episode acquired using a sagittal MP-RAGE three-dimensional T1-weighted se- stroke patients (Table 1). The subjects were scanned five times quence (TR, 1600 ms; TE, 2.15 ms; flip angle, 9°; 1.0 mm isotropic voxels; during a period of 6 months. Seven subjects had right pontine FOV, 256 ϫ 256). Each MRI session involved two to four runs (360 s each infarcts, and four had left infarcts. All subjects had unilateral run) of resting-state fMRI. Subjects were instructed to stay awake and motor deficits at the acute stage. As a control group, 11 healthy keep their eyes open; no other task instruction was provided. Images were matched subjects were scanned three times within 1 month. acquired using the gradient-echo echo-planar pulse sequence (TR, 3000 ms; TE, 30 ms; flip angle, 90°; 3 mm isotropic voxels).
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