Skip to main content
  • Visual, Salience and Motor Networks are Related to Tremor Recovery after Stereotactic Radiosurgical Thalamtomy: A Resting-State fMRI Study

    Final Number:

    Constantin Tuleasca MD; Jean Regis MD; Elena Najdenovska; Tatiana Witjas; Nadine Girard; Jerome Champoudry; Jean-Philippe Thiran; Meritxell Bach Cuadra; Marc Levivier MD, PhD; Dimitri Van de Ville

    Study Design:
    Clinical Trial

    Subject Category:

    Meeting: Congress of Neurological Surgeons 2018 Annual Meeting

    Introduction: Essential tremor (ET) is the most common movement disorder. Drug-resistant ET can benefit from standard procedures (deep brain stimulation, thalamotomy) or minimally invasive high-intensity focused ultrasound (HIFU) or stereotactic radiosurgical thalamotomy (SRS-T). Resting state fMRI (rs-fMRI) is a non-invasive imaging method acquired in absence of a task. We examined whether rs-fMRI correlates with tremor score on the treated hand (TSTH) improvement 1 year after SRS-T.

    Methods: We included 17 consecutive patients treated with left unilateral SRS-T in Marseille, France. Tremor score evaluation and rs-fMRI were acquired at baseline and 1 year after SRS-T. Resting-state data (34 scans) were analyzed without a priori hypothesis, in Lausanne, Switzerland. Based on degree of improvement in TSTH, to consider SRS-T at least as effective as medication, we separated two groups: 1, <= 50% (n=6, 35.3%); 2, > 50% (n=11, 64.7%). They did not differ statistically by age (p=0.86), duration of symptoms (p=0.41) or lesion volume at 1 year (p=0.06).

    Results: We report TSTH improvement correlated with interconnectivity strength between salience network with left claustrum and putamen, as well as between bilateral motor cortices with right visual association area (the former also with lesion volume). Longitudinal changes showed additional associations in inter-connectivity strength between right dorsal attention network with ventro-lateral prefrontal cortex and salience network with fusiform gyrus.

    Conclusions: Brain functional connectivity measured by resting-state fMRI relates to clinical response after SRS-T. Relevant networks are visual, motor and attention. Inter-connectivity between visual and motor areas is a novel finding, revealing implication in movement sensory guidance.

    Patient Care: We aimed at a better understanding of the radiobiology of radiosurgery of the Vim for essential tremor. We report that a focal Vim lesion, produced by SRS-T, is correlated with a distinct functional connectivity pattern, implying changes not only within parts of the pure widely known motor loop, but also on remote areas, including primarily motor (claustrum, putamen; interconnected with salience network) and visual (occipital association cortex; interconnected with bilateral motor cortex) area. Using longitudinal data, at baseline and one year after SRS-T, we suggest that rs-fMRI relates to clinical response. The main areas involved include motor and visual networks, but also cognitive regions, mainly involved in attention (e.g., salience, dorsal attention), suggesting the connection between the former in sensory guidance of movements of hands and fingers.

    Learning Objectives: By the conclusion of this session, participants should be able to: 1- understand the role of resting-state fMRI, as an advanced neuroimaging tool for understanding normal and pathological states, including the use in movement disorders 2- have a basic understanding of the statistical approach used for fMRI data analysis 3- have a basic understanding on the role of each surgical treatment for tremor (inclduign non invasive, such as radiosurgery and HIFU)

    References: 1. Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends in neurosciences 13:266-271 2. Bain PG, Findley LJ, Atchison P, Behari M, Vidailhet M, Gresty M, Rothwell JC, Thompson PD, Marsden CD (1993) Assessing tremor severity. Journal of neurology, neurosurgery, and psychiatry 56:868-873 3. Banati RB, Goerres GW, Tjoa C, Aggleton JP, Grasby P (2000) The functional anatomy of visual-tactile integration in man: a study using positron emission tomography. Neuropsychologia 38:115-124 4. Benabid AL, Pollak P, Gao D, Hoffmann D, Limousin P, Gay E, Payen I, Benazzouz A (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. Journal of neurosurgery 84:203-214 5. Benito-Leon J, Louis ED, Romero JP, Hernandez-Tamames JA, Manzanedo E, Alvarez-Linera J, Bermejo-Pareja F, Posada I, Rocon E (2015) Altered Functional Connectivity in Essential Tremor: A Resting-State fMRI Study. Medicine 94:e1936 6. Bermejo-Pareja F, Puertas-Martin V (2012) Cognitive features of essential tremor: a review of the clinical aspects and possible mechanistic underpinnings. Tremor and other hyperkinetic movements 2 7. Bisley JW (2011) The neural basis of visual attention. The Journal of physiology 589:49-57 8. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic resonance in medicine 34:537-541 9. Blomstedt P, Hariz GM, Hariz MI, Koskinen LO (2007) Thalamic deep brain stimulation in the treatment of essential tremor: a long-term follow-up. British journal of neurosurgery 21:504-509 10. Buijink AW, van der Stouwe AM, Broersma M, Sharifi S, Groot PF, Speelman JD, Maurits NM, van Rootselaar AF (2015) Motor network disruption in essential tremor: a functional and effective connectivity study. Brain : a journal of neurology 138:2934-2947 11. Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Human brain mapping 14:140-151 12. Calvert GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cerebral cortex 11:1110-1123 13. Campbell AM, Glover J, Chiang VL, Gerrard J, Yu JB (2015) Gamma knife stereotactic radiosurgical thalamotomy for intractable tremor: a systematic review of the literature. Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology 114:296-301 14. Crick FC, Koch C (2005) What is the function of the claustrum? Philosophical transactions of the Royal Society of London. Series B, Biological sciences 360:1271-1279 15. Fahn S, Tolosa E, Marin C (1988) Clinical rating scale for tremor. Parkinson’s Disease and Movement Disorders. Baltimore: Urban and Schwarzenberg, pp 225–234 16. Fang W, Chen H, Wang H, Zhang H, Liu M, Puneet M, Lv F, Cheng O, Wang X, Lu X, Luo T (2015) Multiple Resting-State Networks Are Associated With Tremors and Cognitive Features in Essential Tremor. Movement disorders : official journal of the Movement Disorder Society 30:1926-1936 17. Fang W, Chen H, Wang H, Zhang H, Puneet M, Liu M, Lv F, Luo T, Cheng O, Wang X, Lu X (2016) Essential tremor is associated with disruption of functional connectivity in the ventral intermediate Nucleus--Motor Cortex--Cerebellum circuit. Human brain mapping 37:165-178 18. Fang W, Lv F, Luo T, Cheng O, Liao W, Sheng K, Wang X, Wu F, Hu Y, Luo J, Yang QX, Zhang H (2013) Abnormal regional homogeneity in patients with essential tremor revealed by resting-state functional MRI. PloS one 8:e69199 19. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature reviews. Neuroscience 8:700-711 20. Gallea C, Popa T, Garcia-Lorenzo D, Valabregue R, Legrand AP, Marais L, Degos B, Hubsch C, Fernandez-Vidal S, Bardinet E, Roze E, Lehericy S, Vidailhet M, Meunier S (2015) Intrinsic signature of essential tremor in the cerebello-frontal network. Brain : a journal of neurology 138:2920-2933 21. Glickstein M (2000) How are visual areas of the brain connected to motor areas for the sensory guidance of movement? Trends in neurosciences 23:613-617 22. Goldman MS, Ahlskog JE, Kelly PJ (1992) The symptomatic and functional outcome of stereotactic thalamotomy for medically intractable essential tremor. Journal of neurosurgery 76:924-928 23. Guo CC, Kurth F, Zhou J, Mayer EA, Eickhoff SB, Kramer JH, Seeley WW (2012) One-year test-retest reliability of intrinsic connectivity network fMRI in older adults. NeuroImage 61:1471-1483 24. Jang C, Park HJ, Chang WS, Pae C, Chang JW (2016) Immediate and Longitudinal Alterations of Functional Networks after Thalamotomy in Essential Tremor. Frontiers in neurology 7:184 25. Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annual review of neuroscience 23:315-341 26. Kondziolka D, Ong JG, Lee JY, Moore RY, Flickinger JC, Lunsford LD (2008) Gamma Knife thalamotomy for essential tremor. Journal of neurosurgery 108:111-117 27. Lefranc M, Carron R, Regis J (2015) Prelemniscal Radiations: A New Reliable Landmark of the Thalamic Nucleus Ventralis Intermedius Location. Stereotactic and functional neurosurgery 93:400-406 28. Lenka A, Bhalsing KS, Panda R, Jhunjhunwala K, Naduthota RM, Saini J, Bharath RD, Yadav R, Pal PK (2017) Role of altered cerebello-thalamo-cortical network in the neurobiology of essential tremor. Neuroradiology 59:157-168 29. Lipsman N, Schwartz ML, Huang Y, Lee L, Sankar T, Chapman M, Hynynen K, Lozano AM (2013) MR-guided focused ultrasound thalamotomy for essential tremor: a proof-of-concept study. The Lancet. Neurology 12:462-468 30. Louis ED (2005) Essential tremor. The Lancet. Neurology 4:100-110 31. Louis ED (2009) Essential tremors: a family of neurodegenerative disorders? Archives of neurology 66:1202-1208 32. Louis ED (2016) Essential Tremor with Head Tremor: Trait or State? The Canadian journal of neurological sciences. Le journal canadien des sciences neurologiques 43:443-444 33. Lyons KE, Pahwa R (2008) Pharmacotherapy of essential tremor : an overview of existing and upcoming agents. CNS drugs 22:1037-1045 34. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142-2154 35. Regis J, Carron R, Park M (2010) Is radiosurgery a neuromodulation therapy? : A 2009 Fabrikant award lecture. Journal of neuro-oncology 98:155-162 36. Rizzolatti G, Fogassi L, Gallese V (2002) Motor and cognitive functions of the ventral premotor cortex. Current opinion in neurobiology 12:149-154 37. Saint-Cyr JA, Ungerleider LG, Desimone R (1990) Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. The Journal of comparative neurology 298:129-156 38. Schmidt R, Freidl W, Fazekas F, Reinhart B, Grieshofer P, Koch M, Eber B, Schumacher M, Polmin K, Lechner H (1994) The Mattis Dementia Rating Scale: normative data from 1,001 healthy volunteers. Neurology 44:964-966 39. Tardif E, Richer L, Bergeron A, Lepore F, Guillemot JP (1997) Spatial resolution and contrast sensitivity of single neurons in area 19 of split-chiasm cats: a comparison with primary visual cortex. The European journal of neuroscience 9:1929-1939 40. Tuleasca C, Pralong E, Najdenovska E, Cuadra MB, Marques JRF, Vingerhoets F, Regis J, Bloch J, Levivier M (2017) Deep brain stimulation after previous gamma knife thalamotomy of the Vim for essential tremor is feasible! Clinical, electrophysiological and radiological findings. Acta neurochirurgica 159:1371-1373 41. Tuleasca C, Witjas T, Najdenovska E, Verger A, Girard N, Champoudry J, Thiran JP, Van de Ville D, Cuadra MB, Levivier M, Guedj E, Regis J (2017) Assessing the clinical outcome of Vim radiosurgery with voxel-based morphometry: visual areas are linked with tremor arrest! Acta neurochirurgica 159:2139-2144 42. Tuleasca C, Witjas T, Van de Ville D, Najdenovska E, Verger A, Girard N, Champoudry J, Thiran JP, Cuadra MB, Levivier M, Guedj E, Regis J (2017) Right Brodmann area 18 predicts tremor arrest after Vim radiosurgery: a voxel-based morphometry study. Acta neurochirurgica 43. Witjas T, Carron R, Azulay JP, Regis J (2013) Gammaknife Thamamotomy For Intractable Tremors: Clinical Outcome And Correlations With Neuroimaging Features. MDS 17th International Congress of Parkinson's Disease and Movement Disorders, vol Volume 28, p 1247 44. Witjas T, Carron R, Krack P, Eusebio A, Vaugoyeau M, Hariz M, Azulay JP, Regis J (2015) A prospective single-blind study of Gamma Knife thalamotomy for tremor. Neurology 85:1562-1568 45. Zeki S (1993) The visual association cortex. Current opinion in neurobiology 3:155-159

We use cookies to improve the performance of our site, to analyze the traffic to our site, and to personalize your experience of the site. You can control cookies through your browser settings. Please find more information on the cookies used on our site. Privacy Policy