Mapping the network underpinnings of central poststroke pain and analgesic neuromodulation.


Journal

Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686

Informations de publication

Date de publication:
12 2020
Historique:
pubmed: 23 7 2020
medline: 15 5 2021
entrez: 23 7 2020
Statut: ppublish

Résumé

Central poststroke pain (CPSP) is a debilitating and often treatment-refractory condition that affects numerous stroke patients. The location of lesions most likely to cause pain and the identity of the functional brain networks that they impinge upon remain incompletely understood. We aimed to (1) elucidate which lesion locations are most frequently accompanied by pain; (2) explore CPSP-associated functional networks; and (3) examine how neuromodulation interacts with these networks. This multisite study investigated 17 CPSP patients who received deep brain stimulation (DBS; n = 12) or motor cortex stimulation (MCS; n = 5). Pain-causing lesions were manually segmented and normalized to standard space. To identify areas linked to high risk of pain, the locations of CPSP lesions and 220 control lesions were compared using voxelwise odds ratio mapping. The functional connectivity of pain-causing lesions was obtained using a large (n = 1000) normative resting-state functional MRI connectome and compared to that of control lesions and therapeutic DBS activation volumes. Brain regions most associated with CPSP risk (highest value = 63 times) were located along the ascending somatosensory pathways. These areas and the majority of individual CPSP lesions were functionally connected to anterior/middle cingulate cortex, insula, thalamus, and inferior parietal lobule (PBonferroni < 0.05). The extent of connectivity to the thalamus, inferior parietal lobule, and precuneus also differed between CPSP and control lesions (PBonferroni < 0.05). Posterior insula and thalamus shared connectivity with both CPSP lesions and pain-alleviating DBS activation volumes (PBonferroni < 0.05). These findings further clarify the topography and functional connectivity of pain-causing brain lesions, and provide new insights into the network-level mechanism of CPSP neuromodulation.

Identifiants

pubmed: 32694384
doi: 10.1097/j.pain.0000000000001998
pii: 00006396-202012000-00016
doi:

Substances chimiques

Analgesics 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2805-2819

Subventions

Organisme : CIHR
ID : 164235
Pays : Canada

Références

Andersen G, Vestergaard K, Ingeman-Nielsen M, Jensen TS. Incidence of central post-stroke pain. PAIN 1995;61:187–93.
Aprile I, Briani C, Pazzaglia C, Cecchi F, Negrini S, Padua L; Don Carlo Gnocchi Pain-Rehab Group. Pain in stroke patients: characteristics and impact on the rehabilitation treatment: a multicenter cross-sectional study. Eur J Phys Rehabil Med 2015;51:725–36.
Baliki MN, Baria AT, Apkarian AV. The cortical rhythms of chronic back pain. J Neurosci 2011;31:13981–90.
Bassetti C, Bogousslavsky J, Regli F. Sensory syndromes in parietal stroke. Neurology 1993;43:1942–9.
Benarroch EE. Descending monoaminergic pain modulation: bidirectional control and clinical relevance. Neurology 2008;71:217–21.
Birklein F, Rolke R, Müller-Forell W. Isolated insular infarction eliminates contralateral cold, cold pain, and pinprick perception. Neurology 2005;65:1381.
Bittar RG, Kar-Purkayastha I, Owen SL, Bear RE, Green A, Wang S, Aziz TZ. Deep brain stimulation for pain relief: a meta-analysis. J Clin Neurosci 2005;12:515–19.
Blomqvist A, Zhang ET, Craig AD. Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the posterior portion of the ventral medial nucleus, in the human thalamus. Brain J Neurol 2000;123:601–19.
Boes AD, Prasad S, Liu H, Liu Q, Pascual-Leone A, Caviness VS, Fox MD. Network localization of neurological symptoms from focal brain lesions. Brain J Neurol 2015;138:3061–75.
Boivie J, Leijon G, Johansson I. Central post-stroke pain—a study of the mechanisms through analyses of the sensory abnormalities. PAIN 1989;37:173–85.
Boutet A, Gramer R, Steele CJ, Elias GJB, Germann J, Maciel R, Kucharczyk W, Zrinzo L, Lozano AM, Fasano A. Neuroimaging technological advancements for targeting in functional neurosurgery. Curr Neurol Neurosci Rep 2019;19:42.
Boutet A, Ranjan M, Zhong J, Germann J, Xu D, Schwartz ML, Lipsman N, Hynynen K, Devenyi GA, Chakravarty M, Hlasny E, Llinas M, Lozano CS, Elias GJB, Chan J, Coblentz A, Fasano A, Kucharczyk W, Hodaie M, Lozano AM. Focused ultrasound thalamotomy location determines clinical benefits in patients with essential tremor. Brain 2018;141:3405–14.
Bowsher D. Central pain: clinical and physiological characteristics. J Neurol Neurosurg Psychiatry 1996;61:62–9.
Chai SC, Kung JC, Shyu BC. Roles of the anterior cingulate cortex and medial thalamus in short-term and long-term aversive information processing. Mol Pain 2010;6:42.
Chakravarty MM, Bertrand G, Hodge CP, Sadikot AF, Collins DL. The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage 2006;30:359–76.
Craig ADB. Topographically organized projection to posterior insular cortex from the posterior portion of the ventral medial nucleus in the long-tailed macaque monkey. J Comp Neurol 2014;522:36–63.
Darby RR, Joutsa J, Fox MD. Network localization of heterogeneous neuroimaging findings. Brain 2019;142:70–9.
Davidson S, Zhang X, Khasabov SG, Simone DA, Giesler GJ. Termination zones of functionally characterized spinothalamic tract neurons within the primate posterior thalamus. J Neurophysiol 2008;100:2026–37.
De Vloo P, Morlion B, van Loon J, Nuttin B. Animal models for central poststroke pain: a critical comprehensive review. PAIN 2017;158:17–29.
Denis DJ, Marouf R, Rainville P, Bouthillier A, Nguyen DK. Effects of insular stimulation on thermal nociception. Eur J Pain 2016;20:800–10.
Dum RP, Levinthal DJ, Strick PL. The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 2009;29:14223–35.
Duncan GH, Kupers RC, Marchand S, Villemure JG, Gybels JM, Bushnell MC. Stimulation of human thalamus for pain relief: possible modulatory circuits revealed by positron emission tomography. J Neurophysiol 1998;80:3326–30.
Elias GJB, Giacobbe P, Boutet A, Germann J, Beyn ME, Gramer RM, Pancholi A, Joel SE, Lozano AM. Probing the circuitry of panic with deep brain stimulation: connectomic analysis and review of the literature. Brain Stimul 2020;13:10–4.
Ewert S, Plettig P, Li N, Chakravarty MM, Collins DL, Herrington TM, Kühn AA, Horn A. Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. Neuroimage 2018;170:271–82.
Fletcher PD, Downey LE, Golden HL, Clark CN, Slattery CF, Paterson RW, Rohrer JD, Schott JM, Rossor MN, Warren JD. Pain and temperature processing in dementia: a clinical and neuroanatomical analysis. Brain J Neurol 2015;138:3360–72.
Fox MD, Buckner RL, Liu H, Chakravarty MM, Lozano AM, Pascual-Leone A. Resting-state networks link invasive and noninvasive brain stimulation across diverse psychiatric and neurological diseases. Proc Natl Acad Sci U S A 2014;111:E4367–75.
Garcia-Larrea L, Maarrawi J, Peyron R, Costes N, Mertens P, Magnin M, Laurent B. On the relation between sensory deafferentation, pain and thalamic activity in Wallenberg's syndrome: a PET-scan study before and after motor cortex stimulation. Eur J Pain 2006;10:677–88.
Garcia-Larrea L, Perchet C, Creac’h C, Convers P, Peyron R, Laurent B, Mauguière F, Magnin M. Operculo-insular pain (parasylvian pain): a distinct central pain syndrome. Brain J Neurol 2010;133:2528–39.
Green AL, Wang S, Stein JF, Pereira EAC, Kringelbach ML, Liu X, Brittain JS, Aziz TZ. Neural signatures in patients with neuropathic pain. Neurology 2009;72:569–71.
Gritsch S, Bali KK, Kuner R, Vardeh D. Functional characterization of a mouse model for central post-stroke pain. Mol Pain 2016;12:1744806916629049.
Hamani C, Schwalb JM, Rezai AR, Dostrovsky CO, Davis KD, Lozano AM. Deep brain stimulation for chronic neuropathic pain: long-term outcome and the incidence of insertional effect. PAIN 2006;125:188–96.
Hansson P. Post-stroke pain case study: clinical characteristics, therapeutic options and long-term follow-up. Eur J Neurol 2004;11(suppl 1):22–30.
Harston GWJ, Minks D, Sheerin F, Payne SJ, Chappell M, Jezzard P, Jenkinson M, Kennedy J. Optimizing image registration and infarct definition in stroke research. Ann Clin Transl Neurol 2017;4:166–74.
Hemington KS, Wu Q, Kucyi A, Inman RD, Davis KD. Abnormal cross-network functional connectivity in chronic pain and its association with clinical symptoms. Brain Struct Funct 2016;221:4203–19.
Henry JL, Lalloo C, Yashpal K. Central poststroke pain: an abstruse outcome. Pain Res Manag 2008;13:41–9.
Hirai T, Jones EG. A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev 1989;14:1–34.
Hong JH, Bai DS, Jeong JY, Choi BY, Chang CH, Kim SH, Ahn SH, Jang SH. Injury of the spino-thalamo-cortical pathway is necessary for central post-stroke pain. Eur Neurol 2010;64:163–8.
Horn A, Kühn AA. Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage 2015;107:127–35.
Horn A, Reich M, Vorwerk J, Li N, Wenzel G, Fang Q, Schmitz-Hübsch T, Nickl R, Kupsch A, Volkmann J, Kühn AA, Fox MD. Connectivity Predicts deep brain stimulation outcome in Parkinson disease: DBS outcome in PD. Ann Neurol 2017;82:67–78.
Hosomi K, Seymour B, Saitoh Y. Modulating the pain network—neurostimulation for central poststroke pain. Nat Rev Neurol 2015;11:290–9.
Hosomi K, Shimizu T, Maruo T, Watanabe Y, Hui MK, Tani N, Goto Y, Kishima H, Yoshimine T, Saitoh Y. Functional connectivity of the primary motor cortex stimulation in patients with central post-stroke pain. PAIN Res 2015;30:173–6.
Jang SH, Kwon HG. Anatomical location of the medial lemniscus and spinothalamic tract at the pons in the human brain: a diffusion tensor tractography study. Somatosens Mot Res 2013;30:206–9.
Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002;17:825–41.
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage 2012;62:782–90.
Joutsa J, Horn A, Hsu J, Fox MD. Localizing parkinsonism based on focal brain lesions. Brain 2018;141:2445–56.
Kawahara N, Sato K, Muraki M, Tanaka K, Kaneko M, Uemura K. CT classification of small thalamic hemorrhages and their clinical implications. Neurology 1986;36:165–72.
Kim JS. Central post-stroke pain or paresthesia in lenticulocapsular hemorrhages. Neurology 2003;61:679–82.
Kim JS. Delayed-onset ipsilateral sensory symptoms in patients with central poststroke pain. Eur Neurol 1998;40:201–6.
Kim JS. Pure sensory stroke. Clinical-radiological correlates of 21 cases. Stroke 1992;23:983–7.
Kishima H, Saitoh Y, Osaki Y, Nishimura H, Kato A, Hatazawa J, Yoshimine T. Motor cortex stimulation in patients with deafferentation pain: activation of the posterior insula and thalamus. J Neurosurg 2007;107:43–8.
Klit H, Finnerup NB, Andersen G, Jensen TS. Central poststroke pain: a population-based study. PAIN 2011;152:818–24.
Klit H, Finnerup NB, Jensen TS. Central post-stroke pain: clinical characteristics, pathophysiology, and management. Lancet Neurol 2009;8:857–68.
Krause T, Brunecker P, Pittl S, Taskin B, Laubisch D, Winter B, Lentza ME, Malzahn U, Villringer K, Villringer A, Jungehulsing GJ. Thalamic sensory strokes with and without pain: differences in lesion patterns in the ventral posterior thalamus. J Neurol Neurosurg Psychiatry 2012;83:776–84.
Kucyi A, Davis KD. The dynamic pain connectome. Trends Neurosci 2015;38:86–95.
Kung JC, Shyu BC. Potentiation of local field potentials in the anterior cingulate cortex evoked by the stimulation of the medial thalamic nuclei in rats. Brain Res 2002;953:37–44.
Lefaucheur JP, Holsheimer J, Goujon C, Keravel Y, Nguyen JP. Descending volleys generated by efficacious epidural motor cortex stimulation in patients with chronic neuropathic pain. Exp Neurol 2010;223:609–14.
Lefaucheur JP, Ménard-Lefaucheur I, Goujon C, Keravel Y, Nguyen JP. Predictive value of rTMS in the identification of responders to epidural motor cortex stimulation therapy for pain. J Pain 2011;12:1102–11.
Lempka SF, Malone DA, Hu B, Baker KB, Wyant A, Ozinga JG, Plow EB, Pandya M, Kubu CS, Ford PJ, Machado AG. Randomized clinical trial of deep brain stimulation for poststroke pain: DBS for Pain. Ann Neurol 2017;81:653–63.
Li X, Feng Y, Gao F. Maladaptive reorganization in pain-related brain network contributing to the central post-stroke pain. Neuropsychiatry 2018;8:1861–71.
Liew SL, Anglin JM, Banks NW, Sondag M, Ito KL, Kim H, Chan J, Ito J, Jung C, Khoshab N, Lefebvre S, Nakamura W, Saldana D, Schmiesing A, Tran C, Vo D, Ard T, Heydari P, Kim B, Aziz-Zadeh L, Cramer SC, Liu J, Soekadar S, Nordvik JE, Westlye LT, Wang J, Winstein C, Yu C, Ai L, Koo B, Craddock RC, Milham M, Lakich M, Pienta A, Stroud A. A large, open source dataset of stroke anatomical brain images and manual lesion segmentations. Sci Data 2018;5:180011.
Lozano AM. Harnessing plasticity to reset dysfunctional neurons. N Engl J Med 2011;364:1367–8.
Mainero C, Boshyan J, Hadjikhani N. Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol 2011;70:838–45.
Mazzola L, Isnard J, Peyron R, Mauguière F. Stimulation of the human cortex and the experience of pain: Wilder Penfield's observations revisited. Brain J Neurol 2012;135:631–40.
McIntyre CC, Hahn PJ. Network perspectives on the mechanisms of deep brain stimulation. Neurobiol Dis 2010;38:329–37.
Napadow V, LaCount L, Park K, As-Sanie S, Clauw DJ, Harris RE. Intrinsic brain connectivity in fibromyalgia is associated with chronic pain intensity. Arthritis Rheum 2010;62:2545–55.
Paciaroni M, Bogousslavsky J. Pure sensory syndromes in thalamic stroke. Eur Neurol 1998;39:211–17.
Peyron R, García-Larrea L, Grégoire MC, Convers P, Lavenne F, Veyre L, Froment JC, Mauguière F, Michel D, Laurent B. Allodynia after lateral-medullary (Wallenberg) infarct. A PET study. Brain J Neurol 1998;121(pt 2):345–56.
Radhakrishnan V, Tsoukatos J, Davis KD, Tasker RR, Lozano AM, Dostrovsky JO. A comparison of the burst activity of lateral thalamic neurons in chronic pain and non-pain patients. PAIN 1999;80:567–75.
Raffaeli W, Minella CE, Magnani F, Sarti D. Population-based study of central post-stroke pain in Rimini district, Italy. J Pain Res 2013;6:705–11.
Rorden C, Brett M. Stereotaxic display of brain lesions. Behav Neurol 2000;12:191–200.
Şahin-Onat Ş, Ünsal-Delialioğlu S, Kulakli F, Özel S. The effects of central post-stroke pain on quality of life and depression in patients with stroke. J Phys Ther Sci 2016;28:96–101.
Samuelsson M, Samuelsson L, Lindell D. Sensory symptoms and signs and results of quantitative sensory thermal testing in patients with lacunar infarct syndromes. Stroke 1994;25:2165–70.
Schmahmann JD, Leifer D. Parietal pseudothalamic pain syndrome. Clinical features and anatomic correlates. Arch Neurol 1992;49:1032–7.
Sprenger T, Seifert CL, Valet M, Andreou AP, Foerschler A, Zimmer C, Collins DL, Goadsby PJ, Tölle TR, Chakravarty MM. Assessing the risk of central post-stroke pain of thalamic origin by lesion mapping. Brain 2012;135:2536–45.
Thomas Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zöllei L, Polimeni JR, Fischl B, Liu H, Buckner RL. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 2011;106:1125–65.
Treede RD, Jensen TS, Campbell JN, Cruccu G, Dostrovsky JO, Griffin JW, Hansson P, Hughes R, Nurmikko T, Serra J. Neuropathic pain: redefinition and a grading system for clinical and research purposes. Neurology 2008;70:1630–5.
Tsubokawa T, Katayama Y, Yamamoto T, Hirayama T, Koyama S. Chronic motor cortex stimulation in patients with thalamic pain. J Neurosurg 1993;78:393–401.
Veldhuijzen DS, Greenspan JD, Kim JH, Lenz FA. Altered pain and thermal sensation in subjects with isolated parietal and insular cortical lesions. Eur J Pain 2010;14:535.e1–11.
Vorwerk J, Cho JH, Rampp S, Hamer H, Knösche TR, Wolters CH. A guideline for head volume conductor modeling in EEG and MEG. Neuroimage 2014;100:590–607.
Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E. An fMRI-based neurologic signature of physical pain. N Engl J Med 2013;368:1388–97.
Wasner G, Lee BB, Engel S, McLachlan E. Residual spinothalamic tract pathways predict development of central pain after spinal cord injury. Brain J Neurol 2008;131:2387–400.
Widar M, Samuelsson L, Karlsson-Tivenius S, Ahlström G. Long-term pain conditions after a stroke. J Rehabil Med 2002;34:165–70.
Willis WD, Zhang X, Honda CN, Giesler GJ. Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus. PAIN 2001;92:267–76.
Xue T, Yuan K, Zhao L, Yu D, Zhao L, Dong T, Cheng P, von Deneen KM, Qin W, Tian J. Intrinsic brain network abnormalities in migraines without aura revealed in resting-state fMRI. PLoS One 2012;7:e52927.
Zhang Y, Hedo R, Rivera A, Rull R, Richardson S, Tu XM. Post hoc power analysis: is it an informative and meaningful analysis? Gen Psychiatry 2019;32:e100069.

Auteurs

Gavin J B Elias (GJB)

Department of Neurosurgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

Philippe De Vloo (P)

Department of Neurosurgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.
Department of Neurosurgery, University Hospitals Leuven, Leuven, Belgium.

Jürgen Germann (J)

Department of Neurosurgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

Alexandre Boutet (A)

Department of Neurosurgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.
Joint Department of Medical Imaging, University of Toronto, Toronto, ON, Canada.

Robert M Gramer (RM)

Department of Neurosurgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

Suresh E Joel (SE)

General Electric Global Research, Bangalore, India.

Bart Morlion (B)

Department of Algology, University Hospitals Leuven, Leuven, Belgium.

Bart Nuttin (B)

Department of Algology, University Hospitals Leuven, Leuven, Belgium.

Andres M Lozano (AM)

Department of Neurosurgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH