Pediatric Slow-Progressive, but Not Non-Progressive Cerebellar Ataxia Delays Intra-Limb Anticipatory Postural Adjustments in the Upper Arm
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample
2.2. Experimental Procedure
2.3. Data Collection and Analysis
2.4. Statistics
3. Results
3.1. EMG and Kinematics Recordings
3.2. Occurrences of Inhibitory APAs
3.3. APA Latencies
3.4. Index Finger Kinematics Parameters
4. Discussion
4.1. Intra-Limb APAs in SlowP and NonP Children: Role of Disease Progression
4.2. Intra-Limb APAs in NonP and H Children: Putative Compensatory Mechanisms
4.3. Intra-Limb APAs in Children and Adults: Role of Cerebellum in APA Ontogenesis
4.4. Are Inhibitory APAs Really Missing in Cerebellar Patients?
4.5. May APA Timing Be Affected by Bradykinesia?
4.6. Limitations and Methodological Considerations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bouisset, S.; Do, M. Posture, Dynamic Stability, and Voluntary Movement. Neurophysiol. Clin. 2008, 38, 345–362. [Google Scholar] [CrossRef] [PubMed]
- Bouisset, S.; Zattara, M. A Sequence of Postural Movements Precedes Voluntary Movement. Neurosci. Lett. 1981, 22, 263–270. [Google Scholar] [CrossRef]
- Massion, J. Postural Control Systems in Developmental Perspective. Neurosci. Biobehav. Rev. 1998, 22, 465–472. [Google Scholar] [CrossRef] [PubMed]
- Bouisset, S.; Zattara, M. Biomechanical Study of the Programming of Anticipatory Postural Adjustments Associated with Voluntary Movement. J. Biomech. 1987, 20, 735–742. [Google Scholar] [CrossRef]
- Cavallari, P.; Bolzoni, F.; Bruttini, C.; Esposti, R. The Organization and Control of Intra-Limb Anticipatory Postural Adjustments and Their Role in Movement Performance. Front. Hum. Neurosci. 2016, 10, 525. [Google Scholar] [CrossRef] [Green Version]
- Belen’kii, V.Y.; Gurfinkel’, V.S.; Pal’tsev, Y.I. Elements of Control of Voluntary Movements. Biophysics 1967, 12, 154–161. [Google Scholar]
- Friedli, W.G.; Cohen, L.; Hallett, M.; Stanhope, S.; Simon, S.R. Postural Adjustments Associated with Rapid Voluntary Arm Movements. II. Biochemical Analysis. J. Neurol. Neurosurg. Psychiatry 1988, 51, 232–243. [Google Scholar] [CrossRef]
- Honeine, J.; Schieppati, M.; Crisafulli, O.; Do, M. The Neuro-Mechanical Processes That Underlie Goal-Directed Medio-Lateral APA during Gait Initiation. Front. Hum. Neurosci. 2016, 10, 445. [Google Scholar] [CrossRef] [Green Version]
- Crenna, P.; Frigo, C. A Motor Programme for the Initiation of Forward-oriented Movements in Humans. J. Physiol. 1991, 437, 635–653. [Google Scholar] [CrossRef]
- Almeida, G.L.; Hong, D.A.; Corcos, D.; Gottlieb, G.L. Organizing Principles for Voluntary Movement: Extending Single-Joint Rules. J. Neurophysiol. 1995, 74, 1374–1381. [Google Scholar] [CrossRef]
- Gribble, P.L.; Ostry, D.J. Compensation for Interaction Torques During Single- and Multijoint Limb Movement. J. Neurophysiol. 1999, 82, 2310–2326. [Google Scholar] [CrossRef] [Green Version]
- Hopf, H.C.; Hufschmidt, H.J. Coordination of Adjoining Muscles in Simple Voluntary Movements. Dtsch. Z. Nervenheilkd. 1963, 185, 191–202. [Google Scholar]
- Aoki, F. Activity Patterns of Upper Arm Muscles in Relation to Direction of Rapid Wrist Movement in Man. Exp. Brain Res. 1991, 83, 679–682. [Google Scholar] [CrossRef]
- Caronni, A.; Cavallari, P. Anticipatory Postural Adjustments Stabilise the Whole Upper-Limb Prior to a Gentle Index Finger Tap. Exp. Brain Res. 2009, 194, 59–66. [Google Scholar] [CrossRef]
- Asaka, T.; Wang, Y. Feedforward Postural Muscle Modes and Multi-Mode Coordination in Mild Cerebellar Ataxia. Exp. Brain Res. 2011, 210, 153–163. [Google Scholar] [CrossRef]
- Timmann, D.; Horak, F.B. Perturbed Step Initiation in Cerebellar Subjects: 2. Modification of Anticipatory Postural Adjustments. Exp. Brain Res. 2001, 141, 110–120. [Google Scholar] [CrossRef]
- Ivry, R.B.; Spencer, R.M.; Zelaznik, H.N.; Diedrichsen, J. The Cerebellum and Event Timing. Ann. N. Y. Acad. Sci. 2002, 978, 302–317. [Google Scholar] [CrossRef]
- D’Angelo, E. Rebuilding Cerebellar Network Computations from Cellular Neurophysiology. Front. Cell. Neurosci. 2010, 4, 131. [Google Scholar] [CrossRef] [Green Version]
- Cerri, G.; Esposti, R.; Locatelli, M.; Cavallari, P. Coupling of Hand and Foot Voluntary Oscillations in Patients Suffering Cerebellar Ataxia: Different Effect of Lateral or Medial Lesions on Coordination. Prog. Brain Res. 2005, 148, 227–241. [Google Scholar] [CrossRef]
- Ivry, R.B.; Keele, S.W. Timing Functions of the Cerebellum. J. Cogn. Neurosci. 1989, 1, 136–152. [Google Scholar] [CrossRef]
- Diedrichsen, J.; Verstynen, T.; Lehman, S.L.; Ivry, R.B. Cerebellar Involvement in Anticipating the Consequences of Self-Produced Actions During Bimanual Movements. J. Neurophysiol. 2005, 93, 801–812. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bruttini, C.; Esposti, R.; Bolzoni, F.; Vanotti, A.; Mariotti, C.; Cavallari, P. Temporal Disruption of Upper-Limb Anticipatory Postural Adjustments in Cerebellar Ataxic Patients. Exp. Brain Res. 2015, 233, 197–203. [Google Scholar] [CrossRef] [PubMed]
- Farinelli, V.; Palmisano, C.; Marchese, S.M.; Strano, C.M.M.; D’Arrigo, S.; Pantaleoni, C.; Ardissone, A.; Nardocci, N.; Esposti, R.; Cavallari, P. Postural Control in Children with Cerebellar Ataxia. Appl. Sci. 2020, 10, 1606. [Google Scholar] [CrossRef] [Green Version]
- Romani, M.; Micalizzi, A.; Valente, E.M. Joubert Syndrome: Congenital Cerebellar Ataxia with the Molar Tooth. Lancet Neurol. 2013, 12, 894–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hermens, H.J.; Freriks, B. SENIAM 9: European Reccommendations for Surface ElectroMyoGraphy; Roessingh Research and Development: Enschede, The Netherlands, 1999; ISBN 90-75452-14-4. [Google Scholar]
- Caronni, A.; Cavallari, P. Supra-Spinal Circuits Shape Inhibitory Postural Adjustments Anticipating Voluntary Index-Finger Flexion. Exp. Brain Res. 2009, 198, 19–28. [Google Scholar] [CrossRef]
- Azevedo, F.A.C.; Carvalho, L.R.B.; Grinberg, L.T.; Farfel, J.M.; Ferretti, R.E.L.; Leite, R.E.P.; Filho, W.J.; Lent, R.; Herculano-Houzel, S. Equal Numbers of Neuronal and Nonneuronal Cells Make the Human Brain an Isometrically Scaled-up Primate Brain. J. Comp. Neurol. 2009, 513, 532–541. [Google Scholar] [CrossRef]
- Lemon, R.N.; Edgley, S.A. Life without a Cerebellum. Brain 2010, 133, 652–654. [Google Scholar] [CrossRef] [Green Version]
- Combettes, M. Absence Complète Du Cervelet, Des Pédoncules Postérieurs et de La Protubérance Cérébrale Chez Une Jeune Fille Morte Dans Sa Onzième Année. Bull. Soc. Anat. Paris 1831, 5, 1. [Google Scholar]
- Timmann, D.; Dimitrova, A.; Hein-Kropp, C.; Wilhelm, H.; Dörfler, A. Cerebellar Agenesis: Clinical, Neuropsychological and MR Findings. Neurocase 2003, 9, 402–413. [Google Scholar] [CrossRef]
- Titomanlio, L.; Romano, A.; Del Giudice, E. Cerebellar Agenesis. Neurology 2005, 64, E21. [Google Scholar] [CrossRef] [Green Version]
- Arrigoni, F.; Romaniello, R.; Nordio, A.; Gagliardi, C.; Borgatti, R. Learning to Live without the Cerebellum. Neuroreport 2015, 26, 809–813. [Google Scholar] [CrossRef]
- Yu, F.; Jiang, Q.-J.; Sun, X.-Y.; Zhang, R.-W. A New Case of Complete Primary Cerebellar Agenesis: Clinical and Imaging Findings in a Living Patient. Brain 2015, 138, e353. [Google Scholar] [CrossRef] [Green Version]
- Ashraf, O.; Jabeen, S.; Khan, A.; Shaheen, F. Primary Cerebellar Agenesis Presenting as Isolated Cognitive Impairment. J. Pediatr. Neurosci. 2016, 11, 150–152. [Google Scholar] [CrossRef]
- Mormina, E.; Briguglio, M.; Morabito, R.; Arrigo, A.; Marino, S.; Di Rosa, G.; Micalizzi, A.; Valente, E.M.; Salpietro, V.; Vinci, S.L.; et al. A Rare Case of Cerebellar Agenesis: A Probabilistic Constrained Spherical Deconvolution Tractographic Study. Brain Imaging Behav. 2016, 10, 158–167. [Google Scholar] [CrossRef]
- Mummel, P.; Timmann, D.; Krause, U.W.H.; Boering, D.; Thilmann, A.F.; Diener, H.C.; Horak, F.B. Postural Responses to Changing Task Conditions in Patients with Cerebellar Lesions. J. Neurol. Neurosurg. Psychiatry 1998, 65, 734–742. [Google Scholar] [CrossRef]
- Müller, F.; Dichgans, J. Impairments of Precision Grip in Two Patients with Acute Unilateral Cerebellar Lesions: A Simple Parametric Test for Clinical Use. Neuropsychologia 1994, 32, 265–269. [Google Scholar] [CrossRef]
- Babin-Ratté, S.; Sirigu, A.; Gilles, M.; Wing, A. Impaired Anticipatory Finger Grip-Force Adjustments in a Case of Cerebellar Degeneration. Exp. Brain Res. 1999, 128, 81–85. [Google Scholar] [CrossRef]
- Krishnamoorthy, V.; Latash, M.L.; Scholz, J.P.; Zatsiorsky, V.M. Muscle Synergies during Shifts of the Center of Pressure by Standing Persons. Exp. Brain Res. 2003, 152, 281–292. [Google Scholar] [CrossRef]
- Krishnamoorthy, V.; Goodman, S.; Zatsiorsky, V.; Latash, M.L. Muscle Synergies during Shifts of the Center of Pressure by Standing Persons: Identification of Muscle Modes. Biol. Cybern. 2003, 89, 152–161. [Google Scholar] [CrossRef] [PubMed]
- Krishnamoorthy, V.; Latash, M.L.; Scholz, J.P.; Zatsiorsky, V.M. Muscle Modes during Shifts of the Center of Pressure by Standing Persons: Effect of Instability and Additional Support. Exp. Brain Res. 2004, 157, 18–31. [Google Scholar] [CrossRef] [PubMed]
- Klous, M.; Mikulic, P.; Latash, M.L. Two Aspects of Feedforward Postural Control: Anticipatory Postural Adjustments and Anticipatory Synergy Adjustments. J. Neurophysiol. 2011, 105, 2275–2288. [Google Scholar] [CrossRef] [Green Version]
- Bruttini, C.; Esposti, R.; Bolzoni, F.; Cavallari, P. Higher Precision in Pointing Movements of the Preferred vs. Non-Preferred Hand Is Associated with an Earlier Occurrence of Anticipatory Postural Adjustments. Front. Hum. Neurosci. 2016, 10, 365. [Google Scholar] [CrossRef] [Green Version]
- Caronni, A.; Bolzoni, F.; Esposti, R.; Bruttini, C.; Cavallari, P. Accuracy of Pointing Movements Relies upon a Specific Tuning between Anticipatory Postural Adjustments and Prime Mover Activation. Acta Physiol. 2013, 208, 111–124. [Google Scholar] [CrossRef] [PubMed]
- Wu, T.; Hallett, M. The Cerebellum in Parkinson’s Disease. Brain 2013, 136, 696–709. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bostan, A.C.; Strick, P.L. The Cerebellum and Basal Ganglia Are Interconnected. Neuropsychol. Rev. 2010, 20, 261–270. [Google Scholar] [CrossRef]
- Caligiore, D.; Pezzulo, G.; Baldassarre, G.; Bostan, A.C.; Strick, P.L.; Doya, K.; Helmich, R.C.; Dirkx, M.; Houk, J.; Jörntell, H.; et al. Consensus Paper: Towards a Systems-Level View of Cerebellar Function: The Interplay Between Cerebellum, Basal Ganglia, and Cortex. Cerebellum 2017, 16, 203–229. [Google Scholar] [CrossRef] [Green Version]
- Marchese, S.M.; Farinelli, V.; Bolzoni, F.; Esposti, R.; Cavallari, P. Overview of the Cerebellar Function in Anticipatory Postural Adjustments and of the Compensatory Mechanisms Developing in Neural Dysfunctions. Appl. Sci. 2020, 10, 5088. [Google Scholar] [CrossRef]
- Marchese, S.M.; Palesi, F.; Bruzzone, M.; Nigri, A.; Pantaleoni, C.M.; Wheeler-kingshott, C.A.M.G.; D’Arrigo, S.; D’Angelo, E.; Cavallari, P. Whole-Brain Connectivity in Patients with Pediatric Cerebellar Ataxia. In Proceedings of the ISMRM & ISMRT 2023, Toronto, Canada, 3–8 June 2023; Available online: https://www.ismrm.org/23m/ (accessed on 15 March 2023).
- Bruttini, C.; Esposti, R.; Bolzoni, F.; Cavallari, P. Ischemic Block of the Forearm Abolishes Finger Movements but Not Their Associated Anticipatory Postural Adjustments. Exp. Brain Res. 2014, 232, 1739–1750. [Google Scholar] [CrossRef]
- Forssberg, H.; Eliasson, A.-C.; Kinoshita, H.; Johansson, R.; Westling, G. Development of Human Precision Grip I: Basic Coordination of Force. Exp. Brain Res. 1991, 85, 451–457. [Google Scholar] [CrossRef]
- Schmitz, C.; Martin, N.; Assaiante, C. Building Anticipatory Postural Adjustment during Childhood: A Kinematic and Electromyographic Analysis of Unloading in Children from 4 to 8 Years of Age. Exp. Brain Res. 2002, 142, 354–364. [Google Scholar] [CrossRef]
- Horak, F.B.; Esselman, P.; Anderson, M.E.; Lynch, M.K. The Effects of Movement Velocity, Mass Displaced, and Task Certainty on Associated Postural Adjustments Made by Normal and Hemiplegic Individuals. J. Neurol. Neurosurg. Psychiatry 1984, 47, 1020–1028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shiratori, T.; Aruin, A. Modulation of Anticipatory Postural Adjustments Associated with Unloading Perturbation: Effect of Characteristics of a Motor Action. Exp. Brain Res. 2007, 178, 206–215. [Google Scholar] [CrossRef]
- Lee, W.A.; Buchanan, T.S.; Rogers, M.W. Effects of Arm Acceleration and Behavioral Conditions on the Organization of Postural Adjustments during Arm Flexion. Exp. Brain Res. 1987, 66, 257–270. [Google Scholar] [CrossRef]
- Esposti, R.; Bruttini, C.; Bolzoni, F.; Cavallari, P. Intended Rather than Actual Movement Velocity Determines the Latency of Anticipatory Postural Adjustments. Exp. Brain Res. 2015, 233, 397–403. [Google Scholar] [CrossRef]
- Bolzoni, F.; Esposti, R.; Marchese, S.M.; Pozzi, N.G.; Ramirez-Pasos, U.E.; Isaias, I.U.; Cavallari, P. Disrupt of Intra-Limb APA Pattern in Parkinsonian Patients Performing Index-Finger Flexion. Front. Physiol. 2018, 9, 1745. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Marchese, S.M.; Esposti, R.; Farinelli, V.; Ciaccio, C.; De Laurentiis, A.; D’Arrigo, S.; Cavallari, P. Pediatric Slow-Progressive, but Not Non-Progressive Cerebellar Ataxia Delays Intra-Limb Anticipatory Postural Adjustments in the Upper Arm. Brain Sci. 2023, 13, 620. https://doi.org/10.3390/brainsci13040620
Marchese SM, Esposti R, Farinelli V, Ciaccio C, De Laurentiis A, D’Arrigo S, Cavallari P. Pediatric Slow-Progressive, but Not Non-Progressive Cerebellar Ataxia Delays Intra-Limb Anticipatory Postural Adjustments in the Upper Arm. Brain Sciences. 2023; 13(4):620. https://doi.org/10.3390/brainsci13040620
Chicago/Turabian StyleMarchese, Silvia Maria, Roberto Esposti, Veronica Farinelli, Claudia Ciaccio, Arianna De Laurentiis, Stefano D’Arrigo, and Paolo Cavallari. 2023. "Pediatric Slow-Progressive, but Not Non-Progressive Cerebellar Ataxia Delays Intra-Limb Anticipatory Postural Adjustments in the Upper Arm" Brain Sciences 13, no. 4: 620. https://doi.org/10.3390/brainsci13040620