Does Vestibular Motion Perception Correlate with Axonal Pathways Stimulated by Subthalamic Deep Brain Stimulation in Parkinson's Disease?
Basal ganglia
Cerebellum
Motion-perception
Movement disorders
Neurodegeneration
Parkinsonism
Journal
Cerebellum (London, England)
ISSN: 1473-4230
Titre abrégé: Cerebellum
Pays: United States
ID NLM: 101089443
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
accepted:
01
06
2023
pubmed:
13
6
2023
medline:
13
6
2023
entrez:
12
6
2023
Statut:
ppublish
Résumé
Perception of our linear motion - heading - is critical for postural control, gait, and locomotion, and it is impaired in Parkinson's disease (PD). Deep brain stimulation (DBS) has variable effects on vestibular heading perception, depending on the location of the electrodes within the subthalamic nucleus (STN). Here, we aimed to find the anatomical correlates of heading perception in PD. Fourteen PD participants with bilateral STN DBS performed a two-alternative forced-choice discrimination task where a motion platform delivered translational forward movements with a heading angle varying between 0 and 30° to the left or to the right with respect to the straight-ahead direction. Using psychometric curves, we derived the heading discrimination threshold angle of each patient from the response data. We created patient-specific DBS models and calculated the percentages of stimulated axonal pathways that are anatomically adjacent to the STN and known to play a major role in vestibular information processing. We performed correlation analyses to investigate the extent of these white matter tracts' involvement in heading perception. Significant positive correlations were identified between improved heading discrimination for rightward heading and the percentage of activated streamlines of the contralateral hyperdirect, pallido-subthalamic, and subthalamo-pallidal pathways. The hyperdirect pathways are thought to provide top-down control over STN connections to the cerebellum. In addition, STN may also antidromically activate collaterals of hyperdirect pathway that projects to the precerebellar pontine nuclei. In select cases, there was strong activation of the cerebello-thalamic projections, but it was not consistently present in all participants. Large volumetric overlap between the volume of tissue activation and the STN in the left hemisphere positively impacted rightward heading perception. Altogether, the results suggest heavy involvement of basal ganglia cerebellar network in STN-induced modulation of vestibular heading perception in PD.
Identifiants
pubmed: 37308757
doi: 10.1007/s12311-023-01576-8
pii: 10.1007/s12311-023-01576-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
554-569Subventions
Organisme : Department of Veterans Affairs CSRD Merit review
ID : CX002086-03
Organisme : American Parkinson's Disease Association
ID : Geroge C. Cotzias Memorial Fellowship
Organisme : American Academy of Neurology
ID : Career Development Award
Organisme : Caresource Ohio
ID : Community Partnership
Informations de copyright
© 2023. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
Beylergil SB, Ozinga S, Walker MF, et al. Vestibular heading perception in Parkinson’s disease. Prog Brain Res. 2019;249:307–19.
doi: 10.1016/bs.pbr.2019.03.034
pubmed: 31325990
Yousif N, Bhatt H, Bain PG, et al. The effect of pedunculopontine nucleus deep brain stimulation on postural sway and vestibular perception. Eur J Neurol. 2016;23:668–70. https://doi.org/10.1111/ene.12947 .
doi: 10.1111/ene.12947
pubmed: 26800658
pmcid: 4819708
Bertolini G, Wicki A, Baumann CR, et al. Impaired tilt perception in Parkinson’s disease: a central vestibular integration failure. Plos One. 2015;10:e0124253. https://doi.org/10.1371/journal.pone.0124253 .
doi: 10.1371/journal.pone.0124253
pubmed: 25874868
pmcid: 4398395
Bronstein AM, Hood JD, Gresty MA, Panagi C. Visual control of balance in cerebellar and parkinsonian syndromes. Brain. 1990;113:767–79. https://doi.org/10.1093/brain/113.3.767 .
doi: 10.1093/brain/113.3.767
pubmed: 2364268
Beylergil SB, Gupta P, ElKasaby M, et al. Does visuospatial motion perception correlate with coexisting movement disorders in Parkinson’s disease? J Neurol. 2022;269:2179–92.
doi: 10.1007/s00415-021-10804-2
pubmed: 34554323
Deuschl G, Schade-Brittinger C, Krack P, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2006;355:896–908. https://doi.org/10.1056/NEJMoa060281 .
doi: 10.1056/NEJMoa060281
pubmed: 16943402
Beylergil SB, Noecker AM, Petersen M, et al. Subthalamic deep brain stimulation affects heading perception in Parkinson’s disease. J Neurol. 2022;269:253–68. https://doi.org/10.1007/s00415-021-10616-4 .
doi: 10.1007/s00415-021-10616-4
pubmed: 34003373
Rochefort C, Lefort J, Rondi-Reig L (2013) The cerebellum: a new key structure in the navigation system. Front Neural Circuits. Mar 13;7:35.
Kirsch V, Keeser D, Hergenroeder T, et al. Structural and functional connectivity mapping of the vestibular circuitry from human brainstem to cortex. Brain Struct Funct. 2016;221:1291–308. https://doi.org/10.1007/s00429-014-0971-x .
doi: 10.1007/s00429-014-0971-x
pubmed: 25552315
Meng H, May PJ, Dickman JD, Angelaki DE. Vestibular signals in primate thalamus: properties and Origins. J Neurosci. 2007;27:13590–602. https://doi.org/10.1523/JNEUROSCI.3931-07.2007 .
doi: 10.1523/JNEUROSCI.3931-07.2007
pubmed: 18077671
pmcid: 6673608
Hill KK, Campbell MC, McNeely ME, et al. Cerebral blood flow responses to dorsal and ventral STN DBS correlate with gait and balance responses in Parkinson’s disease. Exp Neurol. 2013;241:105–12. https://doi.org/10.1016/j.expneurol.2012.12.003 .
doi: 10.1016/j.expneurol.2012.12.003
pubmed: 23262122
Jenkinson N, Nandi D, Muthusamy K, et al. Anatomy, physiology, and pathophysiology of the pedunculopontine nucleus. Mov Disord. 2009;24:319–28. https://doi.org/10.1002/mds.22189 .
doi: 10.1002/mds.22189
pubmed: 19097193
Plaha P, Gill SS. Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson’s disease. NeuroReport. 2005;16:1883–7. https://doi.org/10.1097/01.wnr.0000187637.20771.a0 .
doi: 10.1097/01.wnr.0000187637.20771.a0
pubmed: 16272872
Bostan AC, Strick PL. The cerebellum and basal ganglia are interconnected. Neuropsychol Rev. 2010;20:261–70. https://doi.org/10.1007/s11065-010-9143-9 .
doi: 10.1007/s11065-010-9143-9
pubmed: 20811947
pmcid: 3325093
Moers-Hornikx VMP, Vles JSH, Tan SKH, et al. Cerebellar nuclei are activated by high-frequency stimulation of the subthalamic nucleus. Neurosci Lett. 2011;496:111–5. https://doi.org/10.1016/j.neulet.2011.03.094 .
doi: 10.1016/j.neulet.2011.03.094
pubmed: 21511005
Smith Y, Hazrati L-N, Parent A. Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol. 1990;294:306–23. https://doi.org/10.1002/cne.902940213 .
doi: 10.1002/cne.902940213
pubmed: 2332533
Edley SM, Graybiel AM. The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta. J Comp Neurol. 1983;217:187–215. https://doi.org/10.1002/cne.902170207 .
doi: 10.1002/cne.902170207
pubmed: 6886052
Ricardo JA. Efferent connections of the subthalamic region in the rat II The zona incerta. Brain Res. 1981;214:43–60. https://doi.org/10.1016/0006-8993(81)90437-6 .
doi: 10.1016/0006-8993(81)90437-6
pubmed: 7237165
Semba K, Fibiger HC. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J Comp Neurol. 1992;323:387–410. https://doi.org/10.1002/cne.903230307 .
doi: 10.1002/cne.903230307
pubmed: 1281170
Steininger TL, Rye DB, Wainer BH. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. I Retrograde tracing studies. J Comp Neurol. 1992;321:515–43. https://doi.org/10.1002/cne.903210403 .
doi: 10.1002/cne.903210403
pubmed: 1380518
Noda H, Sugita S, Ikeda Y. Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol. 1990;302:330–48. https://doi.org/10.1002/cne.903020211 .
doi: 10.1002/cne.903020211
pubmed: 1705268
Giolli RA, Gregory KM, Suzuki DA, et al. Cortical and subcortical afferents to the nucleus reticularis tegmenti pontis and basal pontine nuclei in the macaque monkey. Vis Neurosci. 2001;18:725–40. https://doi.org/10.1017/S0952523801185068 .
doi: 10.1017/S0952523801185068
pubmed: 11925008
Liedgren SR, Milne AC, Schwarz DW, Tomlinson RD. Representation of vestibular afferents in somatosensory thalamic nuclei of the squirrel monkey (Saimiri sciureus). J Neurophysiol. 1976;39:601–12. https://doi.org/10.1152/jn.1976.39.3.601 .
doi: 10.1152/jn.1976.39.3.601
pubmed: 820837
Hoshi E, Tremblay L, Féger J, et al. The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005;8:1491–3. https://doi.org/10.1038/nn1544 .
doi: 10.1038/nn1544
pubmed: 16205719
Ni Z, Pinto AD, Lang AE, Chen R. Involvement of the cerebellothalamocortical pathway in Parkinson disease. Ann Neurol. 2010;68:816–24. https://doi.org/10.1002/ana.22221 .
doi: 10.1002/ana.22221
pubmed: 21194152
Middleton FA, Strick PL. Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn. 2000;42:183–200. https://doi.org/10.1006/brcg.1999.1099 .
doi: 10.1006/brcg.1999.1099
pubmed: 10744919
Bremmer F, Klam F, Duhamel J-R, et al. Visual–vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur J Neurosci. 2002;16:1569–86. https://doi.org/10.1046/j.1460-9568.2002.02206.x .
doi: 10.1046/j.1460-9568.2002.02206.x
pubmed: 12405971
Gu Y, DeAngelis GC, Angelaki DE. A functional link between area MSTd and heading perception based on vestibular signals. Nat Neurosci. 2007;10:1038–47. https://doi.org/10.1038/nn1935 .
doi: 10.1038/nn1935
pubmed: 17618278
pmcid: 2430983
Beylergil SB, Petersen M, Gupta P, et al. Severity-dependent effects of Parkinson’s disease on perception of visual and vestibular heading. Mov Disord. 2021;36:360–9.
doi: 10.1002/mds.28352
pubmed: 33103821
Noecker AM, Choi KS, Riva-Posse P, et al. StimVision software: examples and applications in subcallosal cingulate deep brain stimulation for depression. Neuromodulation Technol Neural Interface. 2018;21:191–6. https://doi.org/10.1111/ner.12625 .
doi: 10.1111/ner.12625
Noecker AM, Frankemolle-Gilbert AM, Howell B, et al. StimVision v2: examples and applications in subthalamic deep brain stimulation for Parkinson’s disease. Neuromodulation Technol Neural Interface. 2021;24:248–58.
doi: 10.1111/ner.13350
Goetz CG, Tilley BC, Shaftman SR, et al. Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord. 2008;23:2129–70. https://doi.org/10.1002/mds.22340 .
doi: 10.1002/mds.22340
pubmed: 19025984
Boutet A, Madhavan R, Elias GJB, et al. Predicting optimal deep brain stimulation parameters for Parkinson’s disease using functional MRI and machine learning. Nat Commun. 2021;12:3043. https://doi.org/10.1038/s41467-021-23311-9 .
doi: 10.1038/s41467-021-23311-9
pubmed: 34031407
pmcid: 8144408
Guehl D, Cuny E, Benazzouz A, et al. Side-effects of subthalamic stimulation in Parkinson’s disease: clinical evolution and predictive factors. Eur J Neurol. 2006;13:963–71. https://doi.org/10.1111/j.1468-1331.2006.01405.x .
doi: 10.1111/j.1468-1331.2006.01405.x
pubmed: 16930362
Ravi DK, Baumann CR, Bernasconi E, et al. Does subthalamic deep brain stimulation impact asymmetry and dyscoordination of gait in Parkinson’s disease? Neurorehabil Neural Repair. 2021;35:1020–9. https://doi.org/10.1177/15459683211041309 .
doi: 10.1177/15459683211041309
pubmed: 34551639
pmcid: 8593318
Zonenshayn M, Sterio D, Kelly PJ, et al. Location of the active contact within the subthalamic nucleus (STN) in the treatment of idiopathic Parkinson’s disease. Surg Neurol. 2004;62:216–25. https://doi.org/10.1016/j.surneu.2003.09.039 .
doi: 10.1016/j.surneu.2003.09.039
pubmed: 15336862
Ostrem JL, Galifianakis NB, Markun LC, et al. Clinical outcomes of PD patients having bilateral STN DBS using high-field interventional MR-imaging for lead placement. Clin Neurol Neurosurg. 2013;115:708–12. https://doi.org/10.1016/j.clineuro.2012.08.019 .
doi: 10.1016/j.clineuro.2012.08.019
pubmed: 22944465
Voges J, Volkmann J, Allert N, et al. Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg. 2002;96:269–79. https://doi.org/10.3171/jns.2002.96.2.0269 .
doi: 10.3171/jns.2002.96.2.0269
pubmed: 11838801
Butenko K, van Rienen U. Chapter 7 - DBS imaging methods III: estimating the electric field and volume of tissue activated. In: Horn A, editor. Connectomic Deep Brain Stimulation. Academic Press; 2022. p. 147–68.
doi: 10.1016/B978-0-12-821861-7.00021-X
Lowery MM (2017) Modeling deep brain stimulation for Parkinson’s disease. In: Computational Models of Brain and Behavior. John Wiley & Sons, Ltd, pp 109–123
Fasano A, Aquino CC, Krauss JK, et al. Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol. 2015;11:98–110. https://doi.org/10.1038/nrneurol.2014.252 .
doi: 10.1038/nrneurol.2014.252
pubmed: 25582445
Krack P, Batir A, Van Blercom N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 2003;349:1925–34. https://doi.org/10.1056/NEJMoa035275 .
doi: 10.1056/NEJMoa035275
pubmed: 14614167
Yamada M, Hoshino M, et al. Precerebellar Nuclei. In: Gruol DL, Koibuchi N, Manto M, et al., editors. Essentials of cerebellum and cerebellar disorders: a primer for graduate students. Cham: Springer International Publishing; 2016. p. 63–7.
doi: 10.1007/978-3-319-24551-5_7
Shen L, Jiang C, Hubbard CS, et al. Subthalamic Nucleus Deep Brain Stimulation Modulates 2 Distinct Neurocircuits. Ann Neurol. 2020;88:1178–93. https://doi.org/10.1002/ana.25906 .
doi: 10.1002/ana.25906
pubmed: 32951262
pmcid: 8087166
Wichmann T, DeLong MR. Deep brain stimulation for movement disorders of basal ganglia origin: restoring function or functionality? Neurotherapeutics. 2016;13:264–83. https://doi.org/10.1007/s13311-016-0426-6 .
doi: 10.1007/s13311-016-0426-6
pubmed: 26956115
pmcid: 4824026
Anderson RW, Farokhniaee A, Gunalan K, et al. Action potential initiation, propagation, and cortical invasion in the hyperdirect pathway during subthalamic deep brain stimulation. Brain Stimulat. 2018;11:1140–50. https://doi.org/10.1016/j.brs.2018.05.008 .
doi: 10.1016/j.brs.2018.05.008
Miocinovic S, de Hemptinne C, Chen W, et al. Cortical potentials evoked by subthalamic stimulation demonstrate a short latency hyperdirect pathway in humans. J Neurosci Off J Soc Neurosci. 2018;38:9129–41. https://doi.org/10.1523/JNEUROSCI.1327-18.2018 .
doi: 10.1523/JNEUROSCI.1327-18.2018
Walker HC, Huang H, Gonzalez CL, et al. Short latency activation of cortex during clinically effective subthalamic deep brain stimulation for Parkinson’s disease. Mov Disord. 2012;27:864–73. https://doi.org/10.1002/mds.25025 .
doi: 10.1002/mds.25025
pubmed: 22648508
pmcid: 3636546
Sanders TH, Jaeger D. Optogenetic stimulation of cortico-subthalamic projections is sufficient to ameliorate bradykinesia in 6-ohda lesioned mice. Neurobiol Dis. 2016;95:225–37. https://doi.org/10.1016/j.nbd.2016.07.021 .
doi: 10.1016/j.nbd.2016.07.021
pubmed: 27452483
pmcid: 5010926
Bingham CS, McIntyre CC. Subthalamic deep brain stimulation of an anatomically detailed model of the human hyperdirect pathway. J Neurophysiol. 2022;127:1209–20. https://doi.org/10.1152/jn.00004.2022 .
doi: 10.1152/jn.00004.2022
pubmed: 35320026
pmcid: 9054256
Coudé D, Parent A, Parent M. Single-axon tracing of the corticosubthalamic hyperdirect pathway in primates. Brain Struct Funct. 2018;223:3959–73. https://doi.org/10.1007/s00429-018-1726-x .
doi: 10.1007/s00429-018-1726-x
pubmed: 30109491
Pulliam CL, Heldman DA, Brokaw EB, et al. Continuous assessment of levodopa response in Parkinson’s disease using wearable motion sensors. IEEE Trans Biomed Eng. 2018;65:159–64. https://doi.org/10.1109/TBME.2017.2697764 .
doi: 10.1109/TBME.2017.2697764
pubmed: 28459677
Evers LJW, Krijthe JH, Meinders MJ, et al. Measuring Parkinson’s disease over time: the real-world within-subject reliability of the MDS-UPDRS. Mov Disord. 2019;34:1480–7. https://doi.org/10.1002/mds.27790 .
doi: 10.1002/mds.27790
pubmed: 31291488
pmcid: 6851993