Top

Published in:

04-01-2024 | Deep Brain Stimulation | Original Article

Somatotopic organization of the ventral nuclear group of the dorsal thalamus: deep brain stimulation for neuropathic pain reveals new insights into the facial homunculus

Authors: Ziad Rifi, Luigi Gianmaria Remore, Meskerem Tolossa, Wenxin Wei, Xiaonan R. Sun, Ausaf A. Bari

Published in: Brain Structure and Function | Issue 2/2024

Abstract

Deep Brain Stimulation (DBS) is an experimental treatment for medication-refractory neuropathic pain. The ventral posteromedial (VPM) and ventral posterolateral (VPL) nuclei of the thalamus are popular targets for the treatment of facial and limb pain, respectively. While intraoperative testing is used to adjust targeting of patient-specific pain locations, a better understanding of thalamic somatotopy may improve targeting of specific body regions including the individual trigeminal territories, face, arm, and leg. To elucidate the somatotopic organization of the ventral nuclear group of the dorsal thalamus using in vivo macrostimulation data from patients undergoing DBS for refractory neuropathic pain. In vivo macrostimulation data was retrospectively collected for 14 patients who underwent DBS implantation for neuropathic pain syndromes at our institution. 56 contacts from 14 electrodes reconstructed with LeadDBS were assigned to macrostimulation-related body regions: tongue, face, arm, or leg. 33 contacts from 9 electrodes were similarly assigned to one of three trigeminal territories: V1, V2, or V3. MNI coordinates in the x, y, and z axes were compared by using MANOVA. Across the horizontal plane of the ventral nuclear group of the dorsal thalamus, the tongue was represented significantly medially, followed by the face, arm, and leg most laterally (p < 0.001). The trigeminal territories displayed significant mediolateral distribution, proceeding from V1 and V2 most medial to V3 most lateral (p < 0.001). Along the y-axis, V2 was also significantly anterior to V3 (p = 0.014). While our results showed that the ventral nuclear group of the dorsal thalamus displayed mediolateral somatotopy of the tongue, face, arm, and leg mirroring the cortical homunculus, the mediolateral distribution of trigeminal territories did not mirror the established cortical homunculus. This finding suggests that the facial homunculus may be inverted in the ventral nuclear group of the dorsal thalamus.

Abdallat M, Saryyeva A, Blahak C et al (2021) Centromedian-parafascicular and somatosensory thalamic deep brain stimulation for treatment of chronic neuropathic pain: a contemporary series of 40 patients. Biomedicines 9(7):731. https://doi.org/10.3390/biomedicines9070731. (Published 2021 Jun 25)CrossRefPubMedPubMedCentral

Abreu V, Vaz R, Rebelo V et al (2017) Thalamic deep brain stimulation for neuropathic pain: efficacy at three years’ follow-up. Neuromodulation 20(5):504–513. https://doi.org/10.1111/ner.12620CrossRefPubMed

Abreu V, Vaz R, Chamadoira C et al (2022) Thalamic deep brain stimulation for post-traumatic neuropathic limb pain: efficacy at five years’ follow-up and effective volume of activated brain tissue. Neurochirurgie 68(1):52–60. https://doi.org/10.1016/j.neuchi.2021.06.006CrossRefPubMed

Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12(1):26–41. https://doi.org/10.1016/j.media.2007.06.004CrossRefPubMed

Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54(3):2033–2044. https://doi.org/10.1016/j.neuroimage.2010.09.025CrossRefPubMed

Ben-Haim S, Mirzadeh Z, Rosenberg WS (2018) Deep brain stimulation for intractable neuropathic facial pain. Neurosurg Focus 45(2):E15. https://doi.org/10.3171/2018.5.FOCUS18160CrossRefPubMed

Berkley KJ (1980) Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatic sensory inputs to lateral diencephalon. J Comp Neurol 193(1):283–317. https://doi.org/10.1002/cne.901930119CrossRefPubMed

Berkley KJ (1983) Spatial relationships between the terminations of somatic sensory motor pathways in the rostral brainstem of cats and monkeys. II. Cerebellar projections compared with those of the ascending somatic sensory pathways in lateral diencephalon. J Comp Neurol 220(2):229–251. https://doi.org/10.1002/cne.902200210CrossRefPubMed

Boccard SGJ, Pereira EAC, Aziz TZ (2015) Deep brain stimulation for chronic pain. J Clin Neurosci 22(10):1537–1543. https://doi.org/10.1016/j.jocn.2015.04.005CrossRefPubMed

Bouhassira D (2019) Neuropathic pain: definition, assessment and epidemiology. Rev Neurol (paris). 175(1–2):16–25. https://doi.org/10.1016/j.neurol.2018.09.016CrossRefPubMed

Bouhassira D, Lantéri-Minet M, Attal N, Laurent B, Touboul C (2008) Prevalence of chronic pain with neuropathic characteristics in the general population. Pain 136(3):380–387. https://doi.org/10.1016/j.pain.2007.08.013CrossRefPubMed

Burton H, Loewy AD (1977) Projections to the spinal cord from medullary somatosensory relay nuclei. J Comp Neurol 173(4):773–792. https://doi.org/10.1002/cne.901730408CrossRefPubMed

Coffey RJ (2001) Deep brain stimulation for chronic pain: results of two multicenter trials and a structured review. Pain Med 2(3):183–192. https://doi.org/10.1046/j.1526-4637.2001.01029.xCrossRefPubMed

Dietrich C, Blume KR, Franz M et al (2017) Dermatomal organization of si leg representation in humans: revising the somatosensory homunculus. Cereb Cortex 27(9):4564–4569. https://doi.org/10.1093/cercor/bhx007CrossRefPubMed

Elias GJB, Boutet A, Joel SE et al (2021) Probabilistic mapping of deep brain stimulation: insights from 15 years of therapy. Ann Neurol 89(3):426–443. https://doi.org/10.1002/ana.25975CrossRefPubMed

Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL (2011) Unbiased average age-appropriate atlases for pediatric studies. Neuroimage 54(1):313–327. https://doi.org/10.1016/j.neuroimage.2010.07.033CrossRefPubMed

Frizon LA, Yamamoto EA, Nagel SJ, Simonson MT, Hogue O, Machado AG (2020) Deep brain stimulation for pain in the modern era: a systematic review. Neurosurgery 86(2):191–202. https://doi.org/10.1093/neuros/nyy552CrossRefPubMed

Gandhoke GS, Belykh E, Zhao X, Leblanc R, Preul MC (2019) Edwin Boldrey and Wilder Penfield’s Homunculus: a life given by Mrs. Cantlie (in and out of realism). World Neurosurg. 132:377–388. https://doi.org/10.1016/j.wneu.2019.08.116CrossRefPubMed

Gudmundsson K, Rhoton AL Jr, Rushton JG (1971) Detailed anatomy of the intracranial portion of the trigeminal nerve. J Neurosurg 35(5):592–600. https://doi.org/10.3171/jns.1971.35.5.0592CrossRefPubMed

Henssen DJ, Kurt E, Kozicz T, van Dongen R, Bartels RH, van Cappellen van Walsum R (2016) New insights in trigeminal anatomy: a double orofacial tract for nociceptive input. Front Neuroanat. https://doi.org/10.3389/fnana.2016.00053CrossRefPubMedPubMedCentral

Henssen DJHA, Mollink J, Kurt E et al (2019) Ex vivo visualization of the trigeminal pathways in the human brainstem using 11.7T diffusion MRI combined with microscopy polarized light imaging. Brain Struct Funct 224(1):159–170. https://doi.org/10.1007/s00429-018-1767-1CrossRefPubMed

Hodaj H, Alibeu JP, Payen JF, Lefaucheur JP (2015) Treatment of chronic facial pain including cluster headache by repetitive transcranial magnetic stimulation of the motor cortex with maintenance sessions: a naturalistic study. Brain Stimul 8(4):801–807. https://doi.org/10.1016/j.brs.2015.01.416CrossRefPubMed

Hodaj H, Payen JF, Hodaj E et al (2020) Long-term treatment of chronic orofacial, pudendal, and central neuropathic limb pain with repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol 131(7):1423–1432. https://doi.org/10.1016/j.clinph.2020.03.022CrossRefPubMed

Holtzheimer PE, Mayberg HS (2011) Deep brain stimulation for psychiatric disorders. Annu Rev Neurosci 34:289–307. https://doi.org/10.1146/annurev-neuro-061010-113638CrossRefPubMedPubMedCentral

Horn A, Kühn AA (2015) Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage 107:127–135. https://doi.org/10.1016/j.neuroimage.2014.12.002CrossRefPubMed

Horn A, Li N, Dembek TA et al (2019) Lead-DBS v2: towards a comprehensive pipeline for deep brain stimulation imaging. Neuroimage 184:293–316. https://doi.org/10.1016/j.neuroimage.2018.08.068CrossRefPubMed

Husch A, Petersen MV, Gemmar P, Goncalves J, Hertel F (2018) PaCER—a fully automated method for electrode trajectory and contact reconstruction in deep brain stimulation. Neuroimage Clin 17:80–89. https://doi.org/10.1016/j.nicl.2017.10.004CrossRefPubMed

Institute of Medicine (US) Committee on Advancing Pain Research, Care and E (2011) Relieving pain in America: a blueprint for transforming prevention, care, education, and research. National Academies Press, Washington, DC

Jones EG, Friedman DP (1982) Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. J Neurophysiol 48(2):521–544. https://doi.org/10.1152/jn.1982.48.2.521CrossRefPubMed

Kashanian A, DiCesare JAT, Rohatgi P et al (2020) Case series: deep brain stimulation for facial pain. Oper Neurosurg 19(5):510–517. https://doi.org/10.1093/ons/opaa170CrossRef

Kumar K, Toth C, Math RK (1997) Deep brain stimulation for intractable pain: a 15-year experience. Neurosurgery 40(4):736–747. https://doi.org/10.1097/00006123-199704000-00015CrossRefPubMed

Lenz FA, Dostrovsky JO, Tasker RR, Yamashiro K, Kwan HC, Murphy JT (1988) Single-unit analysis of the human ventral thalamic nuclear group: somatosensory responses. J Neurophysiol 59:299–316CrossRefPubMed

Mantyh PW (1983) The spinothalamic tract in the primate: a re-examination using wheatgerm agglutinin conjugated to horseradish peroxidase. Neuroscience 9(4):847–862. https://doi.org/10.1016/0306-4522(83)90273-7CrossRefPubMed

Mazars GJ (1975) Intermittent stimulation of nucleus ventralis posterolateralis for intractable pain. Surg Neurol 4(1):93–95PubMed

Mazars G, Merienne L, Cioloca C (1974) Traitement de certains types de douleurs par des stimulateurs thalamiques implantables [Treatment of certain types of pain with implantable thalamic stimulators]. Neurochirurgie 20(2):117–124PubMed

Meyerson BA, Lindblom U, Linderoth B, Lind G, Herregodts P (1993) Motor cortex stimulation as treatment of trigeminal neuropathic pain. Acta Neurochir Suppl (Wien) 58:150–153. https://doi.org/10.1007/978-3-7091-9297-9_34CrossRefPubMed

Mountcastle VB (1980) Neural mechanisms in somesthesis. In: Mountcastle VB (ed) Medical physiology. Mosby, Toronto, pp 348–390

Mountcastle VB, Henneman E (1952) The representation of tactile sensibility in the thalamus of the monkey. J Comp Neurol 97:409–440CrossRefPubMed

Muret D, Root V, Kieliba P, Clode D, Makin TR (2022) Beyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus. Cell Rep 38(11):110523. https://doi.org/10.1016/j.celrep.2022.110523CrossRefPubMedPubMedCentral

Nakamura A, Yamada T, Goto A et al (1998) Somatosensory homunculus as drawn by MEG. Neuroimage 7(4 Pt 1):377–386. https://doi.org/10.1006/nimg.1998.0332CrossRefPubMed

Nguyen JP, Lefaucheur JP, Raoul S, Roualdes V, Péréon Y, Keravel Y (2009) Traitement des douleurs trigéminales neuropathiques par stimulation corticale [Treatment of trigeminal neuropathic pain by motor cortex stimulation]. Neurochirurgie 55(2):226–230. https://doi.org/10.1016/j.neuchi.2009.02.008CrossRefPubMed

Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443CrossRef

Penfield W, Jasper H (1954) Epilepsy and the functional anatomy, of the human brain. J and A Churchill, London, pp 105–106, 159

Penfield W, Rasmussen T (1950) The cerebral cortex of man. Macmillan, New York, pp 44, 56, 214–4456215

Pycroft L, Stein J, Aziz T (2018) Deep brain stimulation: an overview of history, methods, and future developments. Brain Neurosci Adv 2:239821281881601CrossRef

Raghu ALB, Martin SC, Parker T, Aziz TZ, Green AL (2021) Connectivity-based thalamus parcellation and surgical targeting of somatosensory subnuclei. J Neurosurg. https://doi.org/10.3171/2021.7.JNS211140. (published online ahead of print, 2021 Nov 19)CrossRefPubMed

Remore LG, Omidbeigi M, Tsolaki E, Bari AA (2023) Deep brain stimulation of thalamic nuclei for the treatment of drug-resistant epilepsy: Are we confident with the precise surgical target? Seizure 105:22–28. https://doi.org/10.1016/j.seizure.2023.01.009CrossRefPubMed

Roux FE, Djidjeli I, Durand JB (2018) Functional architecture of the somatosensory homunculus detected by electrostimulation. J Physiol 596(5):941–956. https://doi.org/10.1113/JP275243CrossRefPubMedPubMedCentral

Schmid AC, Chien JH, Greenspan JD et al (2016) Neuronal responses to tactile stimuli and tactile sensations evoked by microstimulation in the human thalamic principal somatic sensory nucleus (ventral caudal). J Neurophysiol 115(5):2421–2433. https://doi.org/10.1152/jn.00611.2015CrossRefPubMedPubMedCentral

Su JH, Thomas FT, Kasoff WS et al (2019) Thalamus Optimized Multi Atlas Segmentation (THOMAS): fast, fully automated segmentation of thalamic nuclei from structural MRI. Neuroimage 194:272–282. https://doi.org/10.1016/j.neuroimage.2019.03.021CrossRefPubMed

Takeuchi Y, Osaki H, Yagasaki Y, Katayama Y, Miyata M (2017) Afferent fiber remodeling in the somatosensory thalamus of mice as a neural basis of somatotopic reorganization in the brain and ectopic mechanical hypersensitivity after peripheral sensory nerve injury. eNeuro 4(2):):ENEURO.0345-16.2017. https://doi.org/10.1523/ENEURO.0345-16.2017CrossRefPubMed

Torrance N, Smith BH, Bennett MI, Lee AJ (2006) The epidemiology of chronic pain of predominantly neuropathic origin. Results from a general population survey. J Pain 7(4):281–289. https://doi.org/10.1016/j.jpain.2005.11.008CrossRefPubMed

Tubbs RS, Rizk E, Shoja MM et al (2015) Chapter 34—Human dermatomes. Nerves and nerve injuries, vol 1. Academic Press, Amsterdam, pp 477–483

Ueta Y, Miyata M (2023) Functional and structural synaptic remodeling mechanisms underlying somatotopic organization and reorganization in the thalamus. Neurosci Biobehav Rev 152:105332. https://doi.org/10.1016/j.neubiorev.2023.105332CrossRefPubMed

Vidal JP, Danet L, Péran P et al (2023) Robust thalamic nuclei segmentation from T1-weighted MRI. arXiv.org. https://doi.org/10.48550/arXiv.2304.07167CrossRef

Title: Somatotopic organization of the ventral nuclear group of the dorsal thalamus: deep brain stimulation for neuropathic pain reveals new insights into the facial homunculus
Authors: Ziad Rifi
Luigi Gianmaria Remore
Meskerem Tolossa
Wenxin Wei
Xiaonan R. Sun
Ausaf A. Bari
Publication date: 04-01-2024
Publisher: Springer Berlin Heidelberg
Keywords: Deep Brain Stimulation
Neuropathic Pain
Published in: Brain Structure and Function / Issue 2/2024
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-023-02733-9

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Somatotopic organization of the ventral nuclear group of the dorsal thalamus: deep brain stimulation for neuropathic pain reveals new insights into the facial homunculus

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2024

Embracing digital innovation in neuroscience: 2023 in review at NEUROCCINO

Transient expression of heavy-chain neurofilaments in the perigeniculate nucleus of cats

Clustering the cortical laminae: in vivo parcellation

Ketamine ameliorates activity-based anorexia of adolescent female mice through changes in GluN2B-containing NMDA receptors at postsynaptic cytoplasmic locations of pyramidal neurons and interneurons of medial prefrontal cortex

Manual segmentation of the paraventricular nucleus of the hypothalamus and the dorsal and ventral bed nucleus of stria terminalis using multimodal 7 Tesla structural MRI: probabilistic atlases for a stress-control triad

rTMS over the human medial parietal cortex impairs online reaching corrections

Manual segmentation of the paraventricular nucleus of the hypothalamus and the dorsal and ventral bed nucleus of stria terminalis using multimodal 7 Tesla structural MRI: probabilistic atlases for a stress-control triad