Abstract
Hypometabolism has been observed in the contralesional cerebellar hemisphere after various supratentorial cortical lesions. It is unknown whether the consequences of the dee- and deafferentation subsequent to wide-awake surgery for brain diffuse low-grade glioma can be assessed within remote and unresected subcortical structures such as the cerebellum or thalamus. To answer this question, we have conducted several regional analyses. More specifically, we have performed amplitude of low-frequency fluctuations (neuronal activity magnitude) and regional homogeneity (local temporal correlations) analyses on resting state functional magnetic resonance imaging (rs-fMRI) data and at different time points, before and after surgery. Our main results demonstrated that it is possible to evaluate subtle subcortical changes using these tools dedicated to the analysis of rs-fMRI data. The observed variations of spontaneous neuronal activity were particularly significant within the cerebellum which showed altered regional homogeneity and neuronal activity intensity in very different, specialized and non-overlapping subregions, in accordance to its neuro-anatomo-functional topography. These variations were moreover observed in the immediate postoperative period and recovered after 3 months.
Similar content being viewed by others
References
Duffau H. Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol. 2005;4(8):476–86.
Bonnetblanc F, Desmurget M, Duffau H. Low grade gliomas and cerebral plasticity: fundamental and clinical implications. Med Sci. 2006;22(4):389–94.
Desmurget M, Bonnetblanc F, Duffau H. Contrasting acute and slow-growing lesions: a new door to brain plasticity. Brain. 2007;130(4):898–914.
Sallard E, Duffau H, Bonnetblanc F. Ultra-fast recovery from right neglect after 'awake surgery' for slow-growing tumor invading the left parietal area. Neurocase. 2012;18(1):80–90.
Finger S .Lesion momentum and behaviour. In: Recovery from brain damage: research and theory. Plenum Press. 1978:135–64.
Finger S, Stein D. Brain damage and recovery: research and clinical perspectives. Academic Press. 1982; 368.
Stein DG, Finger S, Hart T. Brain damage and recovery: problems and perspectives. Behav Neural Biol. 1983;37(2):185–222.
Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gassers S, Duffau H. Is the right frontal cortex really crucial in the mentalizing network? A longitudinal study in patients with a slow-growing lesion. Cortex. 2013;49(10):2711–27.
Charras P, Herbet G, Deverdun J, de Champfleur NM, Duffau H, Bartolomeo P, et al. Functional reorganization of the attentional networks in low-grade glioma patients: a longitudinal study. Cortex. 2015;63:27–41.
Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, et al. Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry. 2003;74(7):901–7.
Carrera E, Tononi G. Diaschisis: past, present, future. Brain. 2014;137(9):2408–22.
Pantano P, Baron JC, Samson Y, Bousser MG, Derouesne C, Comar D. Crossed cerebellar diaschisis. Further studies. Brain. 1986;109(4):677–94.
Yamauchi H, Fukuyama H, Kimura J, Ishikawa M, Kikuchi H. Crossed cerebellar hypoperfusion indicates the degree of uncoupling between blood flow and metabolism in major cerebral arterial occlusion. Stroke. 1994;25(10):1945–51.
Meneghetti G, Vorstrup S, Mickey B, Lindewald H, Lassen NA. Crossed cerebellar diaschisis in ischemic stroke: a study of regional cerebral blood flow by 133Xe inhalation and single photon emission computerized tomography. J Cereb Blood Flow Metab. 1984;4(2):235–40.
Chen S, Guan M, Lian HJ, Ma LJ, Shang JK, He S, et al. Crossed cerebellar diaschisis detected by arterial spin-labeled perfusion magnetic resonance imaging in subacute ischemic stroke. J Stroke Cerebrovasc Dis. 2014;23(9):2378–83.
Ayrignac X, Taïeb G, Castelnovo G, Renard D, Collombier L, Menjot de Champfleur N, et al. Cortical and cerebellar hypometabolism after bilateral antero-inferior cerebellar artery infarct. Neurology. 2012;78(1):69–70.
Otte A, Roelcke U, von Ammon K, Hausmann O, Maguire RP, Missimer J, et al. Crossed cerebellar diaschisis and brain tumor biochemistry studied with positron emission tomography, [18F]fluorodeoxyglucose and [11C]methionine. J Neurol Sci. 1998;156(1):73–7.
Kajimoto K, Oku N, Kimura Y, Kato H, Tanaka MR, Kanai Y, et al. Crossed cerebellar diaschisis: a positron emission tomography study with L-[methyl-11C]methionine and 2-deoxy-2-[18F]fluoro-D-glucose. Ann Nucl Med. 2007;21(2):109–13.
Snyder AZ, Raichle ME. A brief history of the resting state: the Washington University perspective. Neuroimage. 2012;62(2):902–10.
Rosazza C, Minati L. Resting-state brain networks: literature review and clinical applications. Neurol Sci. 2011;32(5):773–85.
Lee MH, Smyser CD, Shimony JS. Resting-state fMRI: a review of methods and clinical applications. AJNR Am J Neuroradiol. 2013;34(10):1866–72.
Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29(26):8586–94.
Sang L, Qin W, Liu Y, Han W, Zhang Y, Jiang T, et al. Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. Neuroimage. 2012;61(4):1213–25.
Margulies DS, Böttger J, Long X, Lv Y, Kelly C, Schäfer A, et al. Resting developments: a review of fMRI post-processing methodologies for spontaneous brain activity. MAGMA. 2010;23(5-6):289–307.
Murphy K, Birn RM, Bandettini PA. Resting-state FMRI confounds and cleanup. Neuroimage. 2013;80(1):349–59.
Zang Y, Jiang T, Lu Y, He Y, Tian L. Regional homogeneity approach to fMRI data analysis. Neuroimage. 2004;22(1):394–400.
Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;29(2):83–91.
Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, et al. The oscillating brain: complex and reliable. Neuroimage. 2010;49(2):1432–45.
Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, et al. An improved approach to detection of amplitude of low frequency fluctuation (ALFF) for resting-state MRI: fractional ALFF. J Neurosci Methods. 2008;172(1):137–41.
Wang CX, Fu KL, Liu HJ, Xing F and Zhang SY. Spontaneous brain activity in type 2 diabetics revealed by amplitude of low frequency fluctuations and its association with diabetic vascular disease: a resting-state fMRI study. PLoS ONE. 2014;9(10): doi: 10.1371/journal.pone.0108883.
Wang L, Dai W, Su Y, Wang G, Tan Y, Jin Z, Zeng Y, Yu X, Chen W, Wang X and Si T. Amplitude of low-frequency oscillations in first-episode, treatment-naive patients with major depressive disorder: a resting-state functional MRI study. PloS ONE. 2012;7(10): doi: 10.1371/journal.pone.0048658.
Y Kwak, SJ Peltier, NI Bohnen, ML Müller, P Dayalu and RD Seidler. L-DOPA changes spontaneous low-frequency BOLD signal oscillations in Parkinson’s disease: a resting state fMRI study. Front Syst Neurosci. 2014;6(52): doi: 10.3389/fnsys.2012.00052.
Liu H, Liu Z, Liang M, Hao Y, Tan L, Kuang F, et al. Decreased regional homogeneity in schizophrenia: a resting state functional magnetic resonance imaging study. Neuroreport. 2006;17(1):19–22.
He Y, Wang L, Zang Y, Tian L, Zhang X, Li K, et al. Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. Neuroimage. 2007;35(2):488–500.
Cao Q, Zang Y, Sun L, Sui M, Long X, Zou Q, et al. Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study. Neuroreport. 2006;17(10):1033–6.
Niu C, Zhang M, Min Z, Rana N, Zhang Q, Liu X, Li M and Lin P. Motor network plasticity and low-frequency oscillations abnormalities in patients with brain gliomas: a functional MRI study. PLoS One. 2014;9(5): doi: 10.1371/journal.pone.0096850.
Wu J, Qian Z, Tao L, Yin J, Ding S, Zhang Y, et al. Resting state fMRI feature-based cerebral glioma grading by support vector machine. Int J Comput Assist Radiol Surg. 2015;10(7):1167–74.
Boyer A, Deverdun J, Duffau H, Le Bars E, Menjot de Champfleur N and Bonnetblanc F. Crossed cerebellar diaschisis after awake brain surgery: can we measure pre/post operative changes on resting state fMRI data? IEEE, Conference proceeding. 2015.
Q Zou, J Wang, H Gu, Y Zang Y Yang. Correlations between cerebral blood flow and amplitude of BOLD fluctuation in the Resting State, Proc. Intl.Soc.Mag.Reson.Med.18, 2010.
Li Z, Zhu Y, Childress AR, Detre JA Wang Z. Relations between BOLD fMRI-derived resting brain activity and cerebral blood flow. PLoS ONE. 2012;7(9).
Ashburner J. SPM: a history. Neuroimage. 2012;62(2):791–800.
XW Song, Z-Y Dong, XY Long, SF Li, XN Zuo, CZ Zhu, Y He, CG Yan YF Zang. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE. 2011;6(9): doi: 10.1371/journal.pone.0025031.
Lowe MJ, Russell DP. Treatment of baseline drifts in fMRI time series analysis. J Comput Assist Tomogr. 1999;23(3):463–73.
Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, et al. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am J Neuroradiol. 2001;22(7):1326–33.
Diedrichsen J, Balster JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage. 2009;46(1):39–46.
Diedrichsen J, Maderwald S, Küper M, Thürling M, Rabe K, Gizewski ER, et al. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage. 2011;54(3):1786–94.
Manto M, Bower JM, Conforto AB, Delgado-García JM, da Guarda SN, Gerwig M, et al. Consensus paper: roles of the cerebellum in motor control—the diversity of ideas on cerebellar involvement in movement. Cerebellum. 2012;11(2):457–87.
Ouchi Y, Okada H, Yoshikawa E, Nobezawa S, Futatsubashi M. Brain activation during maintenance of standing postures in humans. Brain. 1999;122(2):329–38.
Spencer RM, Verstynen T, Brett M, Ivry R. Cerebellar activation during discrete and not continuous timed movements: an fMRI study. Neuroimage. 2007;36(2):378–87.
Koziol LF, Budding D, Andreasen N, D'Arrigo S, Bulgheroni S, Imamizu H, et al. Consensus paper: the cerebellum's role in movement and cognition. Cerebellum. 2014;13(1):151–77.
Wolf U, Rapoport MJ, Schweizer TA. Evaluating the affective component of the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci. 2009;21(3):245–53.
Leiner HC, Leiner AL, Dow RS. Does the cerebellum contribute to mental skills? Behav Neurosci. 1986;100(4):443–54.
Leiner HC. Solving the mystery of the human cerebellum. Neuropsychol Rev. 2010;20(3):229–35.
Shakiba A. The role of the cerebellum in neurobiology of psychiatric disorders. Neurol Clin. 2014;32(4):1105–15.
Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.
Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BTT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45.
Schlerf JE, Verstynen TD, Ivry RB, Spencer RM. Evidence of a novel somatopic map in the human neocerebellum during complex actions. J Neurophysiol. 2010;103(6):3330–06.
Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp. 2001;13(2):55–73.
Roostaei T, Nazeri A, Sahraian MA, Minagar A. The human cerebellum: a review of physiologic neuroanatomy. Neurol Clin. 2014;32(4):859–69.
Fine EJ, Ionita CC, Lohr L. The history of the development of the cerebellar examination. Semin Neurol. 2002;22(4):375–84.
Conflict of Interest
The authors declare that they have no competing interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Nicolas Menjot de Champfleur and François Bonnetblanc contributed equally to this work.
Rights and permissions
About this article
Cite this article
Boyer, A., Deverdun, J., Duffau, H. et al. Longitudinal Changes in Cerebellar and Thalamic Spontaneous Neuronal Activity After Wide-Awake Surgery of Brain Tumors: a Resting-State fMRI Study. Cerebellum 15, 451–465 (2016). https://doi.org/10.1007/s12311-015-0709-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12311-015-0709-1