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Erschienen in: Neurological Sciences 8/2021

07.01.2021 | Original Article

Changes in corticomotor pathway excitability after exercise training in Parkinson’s disease

verfasst von: Federica Ginanneschi, Luca Valerio Messa, Carla Battisti, Alessandro Rossi

Erschienen in: Neurological Sciences | Ausgabe 8/2021

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Abstract

Background

Altered corticospinal excitability in Parkinson’s disease (PD) is related to many of the motor signs.

Objective

We examined whether the recruitment properties of the corticospinal pathway to hand muscles are changed after 8 weeks of specialized upper limbs exercise in PD.

Methods

Seven PD subjects were enrolled. Upper limb exercise was achieved by using a specially designed device. The input–output (I–O) curves were obtained by transcranial magnetic stimulation (TMS). The conduction of peripheral axons and H reflex was also recorded. UPDRS scale, part-III motor examination was used to assess the motor symptom. Clinical and neurophysiological data were obtained before and after 2-month exercise training.

Results

After 2-month exercise training, the UPDRS score was significantly improved. Threshold, slope, and V50 (i.e., the stimulus intensity required to obtain a response 50% of the maximum) of the I–O curve were unchanged, whereas the plateau value was significantly higher.

Conclusions

Exercise training affects the larger motoneurons, that is those activated at higher TMS stimulation intensity. These motoneurones are related to the large, type II motor units. Clinical improvement after exercise may depend upon restoration of the recruitment of the large motor unit, i.e., those necessary to perform rapid and strong movements, known to be deficient in PD.
Literatur
1.
Zurück zum Zitat Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375PubMedCrossRef Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375PubMedCrossRef
2.
Zurück zum Zitat DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends in Neurosciences 13:281–285PubMedCrossRef DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends in Neurosciences 13:281–285PubMedCrossRef
3.
Zurück zum Zitat Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271PubMedCrossRef Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271PubMedCrossRef
4.
Zurück zum Zitat Wichmann T, DeLong MR (2003) Functional neuroanatomy of the basal ganglia in Parkinson's disease. Adv Neurol 91:9–18PubMed Wichmann T, DeLong MR (2003) Functional neuroanatomy of the basal ganglia in Parkinson's disease. Adv Neurol 91:9–18PubMed
5.
Zurück zum Zitat Parr-Brownlie LC, Hyland BI (2005) Bradykinesia induced by dopamine D2 receptor blockade is associated with reduced motor cortex activity in the rat. J Neurosci 25:5700–5709PubMedPubMedCentralCrossRef Parr-Brownlie LC, Hyland BI (2005) Bradykinesia induced by dopamine D2 receptor blockade is associated with reduced motor cortex activity in the rat. J Neurosci 25:5700–5709PubMedPubMedCentralCrossRef
6.
Zurück zum Zitat Pasquereau B, Turner RS (2011) Primary motor cortex of the parkinsonian monkey: differential effects on the spontaneous activity of pyramidal tract-type neurons. Cereb Cortex 21:1362–1378PubMedCrossRef Pasquereau B, Turner RS (2011) Primary motor cortex of the parkinsonian monkey: differential effects on the spontaneous activity of pyramidal tract-type neurons. Cereb Cortex 21:1362–1378PubMedCrossRef
7.
Zurück zum Zitat Cantello R, Tarletti R, Civardi C (2002) Transcranial magnetic stimulation and Parkinson’s disease. Brain Res Rev 38:309–327PubMedCrossRef Cantello R, Tarletti R, Civardi C (2002) Transcranial magnetic stimulation and Parkinson’s disease. Brain Res Rev 38:309–327PubMedCrossRef
8.
Zurück zum Zitat Leon-Sarmiento FE, Rizzo-Sierra CV, Bayona EA, Bayona-Prieto J, Doty RL, Bara-Jimenez W (2013) Novel mechanisms underlying inhibitory and facilitatory transcranial magnetic stimulation abnormalities in Parkinson's disease. Arch Med Res 44:221–228PubMedCrossRef Leon-Sarmiento FE, Rizzo-Sierra CV, Bayona EA, Bayona-Prieto J, Doty RL, Bara-Jimenez W (2013) Novel mechanisms underlying inhibitory and facilitatory transcranial magnetic stimulation abnormalities in Parkinson's disease. Arch Med Res 44:221–228PubMedCrossRef
9.
Zurück zum Zitat Tomlinson CL, Patel S, Meek C, Herd CP, Clarke CE, Stowe R, Shah L, Sackley C, Deane KH, Wheatley K, Ives N (2012) Physiotherapy intervention in Parkinson's disease: systematic review and meta-analysis. BMJ 345:e5004PubMedPubMedCentralCrossRef Tomlinson CL, Patel S, Meek C, Herd CP, Clarke CE, Stowe R, Shah L, Sackley C, Deane KH, Wheatley K, Ives N (2012) Physiotherapy intervention in Parkinson's disease: systematic review and meta-analysis. BMJ 345:e5004PubMedPubMedCentralCrossRef
10.
Zurück zum Zitat Messa LV, Ginanneschi F, Momi D, Monti L, Battisti C, Cioncoloni D, Pucci B, Santarnecchi E, Rossi A (2019) Functional and brain activation changes following specialized upper-limb exercise in Parkinson’s disease. Front Hum Neurosci 13:350PubMedPubMedCentralCrossRef Messa LV, Ginanneschi F, Momi D, Monti L, Battisti C, Cioncoloni D, Pucci B, Santarnecchi E, Rossi A (2019) Functional and brain activation changes following specialized upper-limb exercise in Parkinson’s disease. Front Hum Neurosci 13:350PubMedPubMedCentralCrossRef
11.
Zurück zum Zitat Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W (1998) Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 511:181–190PubMedPubMedCentralCrossRef Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W (1998) Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 511:181–190PubMedPubMedCentralCrossRef
12.
Zurück zum Zitat Cavaleri R, Schabrun SM, Chipchase LS (2017) The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev 6:48PubMedPubMedCentralCrossRef Cavaleri R, Schabrun SM, Chipchase LS (2017) The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev 6:48PubMedPubMedCentralCrossRef
13.
Zurück zum Zitat Ginanneschi F, Mondelli M, Dominici F, Rossi A (2006) Changes in motor axon recruitment in the median nerve in mild carpal tunnel syndrome. Clin Neurophysiol 117:2467–2472PubMedCrossRef Ginanneschi F, Mondelli M, Dominici F, Rossi A (2006) Changes in motor axon recruitment in the median nerve in mild carpal tunnel syndrome. Clin Neurophysiol 117:2467–2472PubMedCrossRef
14.
Zurück zum Zitat Messa LV, Biffi A, Fernando F, Ginanneschi F, Rossi A (2016) Tailored exercise with an innovative mechanical device: effects on cervical-dorsal rachis. J Funct Morphol Kinesiol 1:183–189CrossRef Messa LV, Biffi A, Fernando F, Ginanneschi F, Rossi A (2016) Tailored exercise with an innovative mechanical device: effects on cervical-dorsal rachis. J Funct Morphol Kinesiol 1:183–189CrossRef
15.
Zurück zum Zitat Alberts JL, Phillips M, Lowe MJ, Frankemolle A, Thota A, Beall EB, Feldman M, Ahmed A, Ridgel AL (2016) Cortical and motor responses to acute forced exercise in Parkinsons disease. Parkinsonism Relat Disord 24:56–62PubMedPubMedCentralCrossRef Alberts JL, Phillips M, Lowe MJ, Frankemolle A, Thota A, Beall EB, Feldman M, Ahmed A, Ridgel AL (2016) Cortical and motor responses to acute forced exercise in Parkinsons disease. Parkinsonism Relat Disord 24:56–62PubMedPubMedCentralCrossRef
16.
Zurück zum Zitat Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338PubMedCrossRef Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338PubMedCrossRef
17.
Zurück zum Zitat Capaday C (1997) Neurophysiological methods for studies of the motor system in freely moving human subjects. J Neurosci Methods 74:201–218PubMedCrossRef Capaday C (1997) Neurophysiological methods for studies of the motor system in freely moving human subjects. J Neurosci Methods 74:201–218PubMedCrossRef
18.
Zurück zum Zitat Carroll TJ, Riek S, Carson RG (2001) Reliability of the input-output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation. J Neurosci Methods 112:193–202PubMedCrossRef Carroll TJ, Riek S, Carson RG (2001) Reliability of the input-output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation. J Neurosci Methods 112:193–202PubMedCrossRef
19.
Zurück zum Zitat Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200PubMedCrossRef Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200PubMedCrossRef
20.
Zurück zum Zitat Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633PubMedPubMedCentralCrossRef Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633PubMedPubMedCentralCrossRef
21.
Zurück zum Zitat Burciu RG, Vaillancourt DE (2018) Imaging of motor cortex physiology in Parkinson’s disease. MovDisord 33:1688–1699 Burciu RG, Vaillancourt DE (2018) Imaging of motor cortex physiology in Parkinson’s disease. MovDisord 33:1688–1699
22.
Zurück zum Zitat Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146PubMedCrossRef Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146PubMedCrossRef
23.
Zurück zum Zitat Wu T, Wang L, Hallett M, Chen Y, Li K, Chan P (2011) Effective connectivity of brain networks during self-initiated movement in Parkinson’s disease. Neuroimage 55:204–215PubMedCrossRef Wu T, Wang L, Hallett M, Chen Y, Li K, Chan P (2011) Effective connectivity of brain networks during self-initiated movement in Parkinson’s disease. Neuroimage 55:204–215PubMedCrossRef
24.
Zurück zum Zitat Bologna M, Paparella G, Fasano A, Hallett M, Berardelli A (2020) Evolving concepts on bradykinesia. Brain 143:727–750PubMedCrossRef Bologna M, Paparella G, Fasano A, Hallett M, Berardelli A (2020) Evolving concepts on bradykinesia. Brain 143:727–750PubMedCrossRef
25.
Zurück zum Zitat Bologna M, Guerra A, Paparella G, Giordo L, Alunni Fegatelli D, Vestri AR, Rothwell JC, Berardelli A (2018) Neurophysiological correlates of bradykinesia in Parkinson’s disease. Brain 141:2432–2444PubMedCrossRef Bologna M, Guerra A, Paparella G, Giordo L, Alunni Fegatelli D, Vestri AR, Rothwell JC, Berardelli A (2018) Neurophysiological correlates of bradykinesia in Parkinson’s disease. Brain 141:2432–2444PubMedCrossRef
26.
Zurück zum Zitat Kojovic M, Bologna M, Kassavetis P, Murase N, Palomar FJ, Berardelli A, Rothwell JC, Edwards MJ, Bhatia KP (2010) Functional reorganization of sensorimotor cortex in early Parkinson disease. Neurology 78:1441–1448CrossRef Kojovic M, Bologna M, Kassavetis P, Murase N, Palomar FJ, Berardelli A, Rothwell JC, Edwards MJ, Bhatia KP (2010) Functional reorganization of sensorimotor cortex in early Parkinson disease. Neurology 78:1441–1448CrossRef
27.
Zurück zum Zitat Kimiskidis VK, Papayiannopoulos S, Sotirakoglou K, Karakasis H, Katsarou Z, Kazis DA, Papaliagkas V, Gatzonis S, Papadimitriou A, Hadjigeorgiou G, Bostanjopoulou S (2018) The cortical excitability profile of patients with the G209A SNCA mutation versus patients with sporadic Parkinson’s disease: a transcranial magnetic stimulation study. Neurophysiol Clin 48:203–206PubMedCrossRef Kimiskidis VK, Papayiannopoulos S, Sotirakoglou K, Karakasis H, Katsarou Z, Kazis DA, Papaliagkas V, Gatzonis S, Papadimitriou A, Hadjigeorgiou G, Bostanjopoulou S (2018) The cortical excitability profile of patients with the G209A SNCA mutation versus patients with sporadic Parkinson’s disease: a transcranial magnetic stimulation study. Neurophysiol Clin 48:203–206PubMedCrossRef
28.
Zurück zum Zitat Kačar A, Filipović SR, Kresojević N, Milanović SD, Ljubisavljević L, Kostić SV, Rothwell JC (2013) History ofexposure to dopaminergic medication does not affect motor cortex plasticity and excitability in Parkinson’s disease. Clin Neurophysiol 124:697–707PubMedCrossRef Kačar A, Filipović SR, Kresojević N, Milanović SD, Ljubisavljević L, Kostić SV, Rothwell JC (2013) History ofexposure to dopaminergic medication does not affect motor cortex plasticity and excitability in Parkinson’s disease. Clin Neurophysiol 124:697–707PubMedCrossRef
29.
Zurück zum Zitat Wickens J, Hyland B, Anson G (1994) Cortical cell assemblies: a possible mechanism for motor programs. J Mot Behav 26:66–82PubMedCrossRef Wickens J, Hyland B, Anson G (1994) Cortical cell assemblies: a possible mechanism for motor programs. J Mot Behav 26:66–82PubMedCrossRef
30.
Zurück zum Zitat Poliakov AV, Miles TS (1992) Quantitative analysis of reflex responses in the averaged surface electromyogram. J Neurosci Methods 43:195–200PubMedCrossRef Poliakov AV, Miles TS (1992) Quantitative analysis of reflex responses in the averaged surface electromyogram. J Neurosci Methods 43:195–200PubMedCrossRef
31.
Zurück zum Zitat Magistris MR, Rosler KM, Truffert A, Myers JP (1998) Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 121:437–450PubMedCrossRef Magistris MR, Rosler KM, Truffert A, Myers JP (1998) Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 121:437–450PubMedCrossRef
32.
Zurück zum Zitat Paparella G, Rocchi L, Bologna M, Berardelli A, Rothwell J (2020) Differential effects of motor skill acquisition on the primary motor and sensory cortices in healthy humans. J Physiol 598:4031–4045PubMedCrossRef Paparella G, Rocchi L, Bologna M, Berardelli A, Rothwell J (2020) Differential effects of motor skill acquisition on the primary motor and sensory cortices in healthy humans. J Physiol 598:4031–4045PubMedCrossRef
33.
Zurück zum Zitat Berghuis KMM, Semmler JG, Opie GM, Post AK, Hortobágyi T (2017) Age-related changes in corticospinal excitability and intracortical inhibition after upper extremity motor learning: a systematic review and meta-analysis. Neurobiol Aging 55:61–71PubMedCrossRef Berghuis KMM, Semmler JG, Opie GM, Post AK, Hortobágyi T (2017) Age-related changes in corticospinal excitability and intracortical inhibition after upper extremity motor learning: a systematic review and meta-analysis. Neurobiol Aging 55:61–71PubMedCrossRef
34.
Zurück zum Zitat Edström L (1970) Selective changes in the sizes of red and white muscle fibres in upper motor lesions and Parkinsonism. J Neurol Sci 11:537–550PubMedCrossRef Edström L (1970) Selective changes in the sizes of red and white muscle fibres in upper motor lesions and Parkinsonism. J Neurol Sci 11:537–550PubMedCrossRef
35.
Zurück zum Zitat Rossi B, Siciliano G, Carboncini MC, Manca ML, Massetani R, Viacava P, Muratorio A (1996) Muscle modifications in Parkinson'sdisease: myoelectric manifestations. Electroencephalogr Clin Neurophysiol 101:211–218PubMedCrossRef Rossi B, Siciliano G, Carboncini MC, Manca ML, Massetani R, Viacava P, Muratorio A (1996) Muscle modifications in Parkinson'sdisease: myoelectric manifestations. Electroencephalogr Clin Neurophysiol 101:211–218PubMedCrossRef
36.
Zurück zum Zitat Mu L, Sobotka S, Chen J, Su H, Sanders I, Adler CH, Shill HA, Caviness JN, Samanta JE, Beach TG (2012) Arizona Parkinson’s Disease Consortium. Altered pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol 71:520–530PubMedCrossRef Mu L, Sobotka S, Chen J, Su H, Sanders I, Adler CH, Shill HA, Caviness JN, Samanta JE, Beach TG (2012) Arizona Parkinson’s Disease Consortium. Altered pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol 71:520–530PubMedCrossRef
37.
Zurück zum Zitat Kelly NA, Hammond KG, Bickel CS, Windham ST, Tuggle SC, Bamman MM (1985) Effects of aging and Parkinson’s disease on motor unit remodeling: influence of resistance exercise training. J Appl Physiol 124:888–898CrossRef Kelly NA, Hammond KG, Bickel CS, Windham ST, Tuggle SC, Bamman MM (1985) Effects of aging and Parkinson’s disease on motor unit remodeling: influence of resistance exercise training. J Appl Physiol 124:888–898CrossRef
38.
Zurück zum Zitat Glendinning DS, Enoka RM (1994) Motor unit behavior in Parkinson’s disease. Phys Ther 74:61–70PubMedCrossRef Glendinning DS, Enoka RM (1994) Motor unit behavior in Parkinson’s disease. Phys Ther 74:61–70PubMedCrossRef
39.
Zurück zum Zitat Rose MH, Løkkegaard A, Sonne-Holm S, Jensen BR (2013) Effects of training and weight support on muscle activation in Parkinson’s disease. J Electromyogr Kinesiol 23:1499–1504PubMedCrossRef Rose MH, Løkkegaard A, Sonne-Holm S, Jensen BR (2013) Effects of training and weight support on muscle activation in Parkinson’s disease. J Electromyogr Kinesiol 23:1499–1504PubMedCrossRef
40.
41.
Zurück zum Zitat Calancie B, Nordin M, Wallin U, Hagbarth KE (1987) Motor-unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli. J Neurophysiol 58:1168–1185PubMedCrossRef Calancie B, Nordin M, Wallin U, Hagbarth KE (1987) Motor-unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli. J Neurophysiol 58:1168–1185PubMedCrossRef
42.
Zurück zum Zitat Colebatch JG, Rothwell JC, Day BL, Thompson PD, Marsden CD (1990) Cortical outflow to proximal arm muscles in man. Brain 113:1843–1856PubMedCrossRef Colebatch JG, Rothwell JC, Day BL, Thompson PD, Marsden CD (1990) Cortical outflow to proximal arm muscles in man. Brain 113:1843–1856PubMedCrossRef
43.
Zurück zum Zitat Boniface SJ, Mills KR, Schubert M (1991) Responses of single spinal motoneurons to magnetic brain stimulation in healthy subjects and patients with multiple sclerosis. Brain 114:643–662PubMedCrossRef Boniface SJ, Mills KR, Schubert M (1991) Responses of single spinal motoneurons to magnetic brain stimulation in healthy subjects and patients with multiple sclerosis. Brain 114:643–662PubMedCrossRef
Metadaten
Titel
Changes in corticomotor pathway excitability after exercise training in Parkinson’s disease
verfasst von
Federica Ginanneschi
Luca Valerio Messa
Carla Battisti
Alessandro Rossi
Publikationsdatum
07.01.2021
Verlag
Springer International Publishing
Erschienen in
Neurological Sciences / Ausgabe 8/2021
Print ISSN: 1590-1874
Elektronische ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-020-04960-y

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