Advertisement

The Cerebellum

, Volume 18, Issue 2, pp 203–211 | Cite as

Collaboration of Cerebello-Rubral and Cerebello-Striatal Loops in a Motor Preparation Task

  • Chama BelkhiriaEmail author
  • Eya Mssedi
  • Christophe Habas
  • Tarak Driss
  • Giovanni de Marco
Original Paper

Abstract

In this study, we used fMRI to identify brain regions associated with concentration (sustained attention) during a motor preparation task. In comparison with a non-concentration task, increased activities were observed (P < 0.05, FWE-corrected P values) in cerebellar lobules VI and VII, motor cortex, pre-supplementary motor area (pre-SMA), thalamus, red nucleus (RN), and caudate nucleus (CN). Moreover, analysis of effective connectivity inter-areal (psychophysiological interactions) showed that during preparation, concentration-related brain activity increase was dependent on Cerebello-thalamo-pre-SMA-RN and Pre-SMA-CN-thalamo-M1 loops. We postulate that, while pre-SMA common to both loops is specifically involved in the movement preparation and readiness for voluntary movement through the striatum, the cerebellar lobule VI in conjunction with RN, likely through a cerebellar-rubro-olivary-cerebellar loop, might be implicated in concentration-related optimization of upcoming motor performances.

Keywords

Cerebellum Red nucleus Pre-SMA Caudate nucleus Motor preparation 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Cunnington R, Windischberger C, Deecke L, Moser E. The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. NeuroImage. 2003;20(1):404–12.Google Scholar
  2. 2.
    Nguyen VT, Breakspear M, Cunnington R. Reciprocal interactions of the SMA and cingulate cortex sustain premovement activity for voluntary actions. J Neurosci. 2014;34(49):16397–407.Google Scholar
  3. 3.
    Thickbroom G, Byrnes M, Sacco P, Ghosh S, Morris I, Mastaglia F. The role of the supplementary motor area in externally timed movement: the influence of predictability of movement timing. Brain Res. 2000;874(2):233–41.Google Scholar
  4. 4.
    Rizzolatti G, Fadiga L, Gallese V, Fogassi L. Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res. 1996;3(2):131–41.Google Scholar
  5. 5.
    Yazawa S, Ikeda A, Kunieda T, Ohara S, Mima T, Nagamine T, et al. Human presupplementary motor area is active before voluntary movement: subdural recording of Bereitschaftspotential from medial frontal cortex. Exp Brain Res. 2000;131(2):165–77.Google Scholar
  6. 6.
    Purzner J, Paradiso GO, Cunic D, Saint-Cyr JA, Hoque T, Lozano AM, et al. Involvement of the basal ganglia and cerebellar motor pathways in the preparation of self-initiated and externally triggered movements in humans. J Neurosci. 2007;27(22):6029–36.Google Scholar
  7. 7.
    Weilke F, Spiegel S, Boecker H, von Einsiedel HG, Conrad B, Schwaiger M, et al. Time-resolved fMRI of activation patterns in M1 and SMA during complex voluntary movement. J Neurophysiol. 2001;85(5):1858–63.Google Scholar
  8. 8.
    Lee K-M, Chang K-H, Roh J-K. Subregions within the supplementary motor area activated at different stages of movement preparation and execution. NeuroImage. 1999;9(1):117–23.Google Scholar
  9. 9.
    MacKinnon C, Bissig D, Chiusano J. Preparation of anticipatory postural adjustments prior to stepping. J Neurophysiol. 2007;97(6):4368–79.Google Scholar
  10. 10.
    Akkal D, Dum RP, Strick PL. Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci. 2007;27(40):10659–73.Google Scholar
  11. 11.
    Sussman D, Leung R, Chakravarty M. The developing human brain: age-related changes in cortical, subcortical, and cerebellar anatomy. Brain Behav. 2016;6(4):e00457.Google Scholar
  12. 12.
    Rondi-Reig L, Paradis A-L, Lefort JM, Babayan BM, Tobin C. How the cerebellum may monitor sensory information for spatial representation. Front Syst Neurosci. 2014;8:205.Google Scholar
  13. 13.
    Richard A, Van Hamme A, Drevelle X, Golmard J-L, Meunier S, Welter M-L. Contribution of the supplementary motor area and the cerebellum to the anticipatory postural adjustments and execution phases of human gait initiation. Neuroscience. 2017;358:181–9.Google Scholar
  14. 14.
    D’Angelo E, Mazzarello P, Prestori F, Mapelli J, Solinas S, Lombardo P, et al. The cerebellar network: from structure to function and dynamics. Brain Res Rev. 2011;66(1–2):5–15.Google Scholar
  15. 15.
    Shadmehr R, Krakauer JW. A computational neuroanatomy for motor control. Exp Brain Res. 2008;185(3):359–81.Google Scholar
  16. 16.
    Proudfoot M, Rohenkohl G, Quinn A, Colclough GL, Wuu J, Talbot K, et al. Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis. Hum Brain Mapp. 2017;38(1):237–54.Google Scholar
  17. 17.
    Fekete T, Zach N, Mujica-Parodi L, Turner M. Multiple kernel learning captures a systems-level functional connectivity biomarker signature in amyotrophic lateral sclerosis. PLoS One. 2013;8(12):e85190.Google Scholar
  18. 18.
    Habas C, Kamdar N, Nguyen D, Prater K. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29(26):8586–94.Google Scholar
  19. 19.
    Manto M, Jissendi P. Cerebellum: links between development, developmental disorders and motor learning. Front Neuroanat. 2012;6:1.Google Scholar
  20. 20.
    Nioche C, Cabanis E. Functional connectivity of the human red nucleus in the brain resting state at 3T. AJNR Am J Neuroradiol. 2009;30(2):396–403.Google Scholar
  21. 21.
    Liu Y, Pu Y, Gao J, Parsons L, Xiong J. The human red nucleus and lateral cerebellum in supporting roles for sensory information processing. Hum Brain Mapp. 2000;10(4):147–59.Google Scholar
  22. 22.
    Penhune V, Steele C. Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behav Brain Res. 2012;226(2):579–91.Google Scholar
  23. 23.
    Albouy G, King B, Maquet P, Doyon J. Hippocampus and striatum: dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus. 2013;23(11):985–1004.Google Scholar
  24. 24.
    Grahn J, Parkinson J, Owen A. The cognitive functions of the caudate nucleus. Prog Neurobiol. 2008;86(3):141–55.Google Scholar
  25. 25.
    Belkhiria C, Driss T, Habas C, Jaafar H, Guillevin R, de Marco G. Exploration and identification of cortico-cerebellar-brainstem closed loop during a motivational-motor task: an fMRI study. Cerebellum. 2017;16(2):326–39.Google Scholar
  26. 26.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage. 2002;15(1):273–89.Google Scholar
  27. 27.
    Satoshi H, Koji J, Akira K, Osamu A, Kuni O, Yasushi M, et al. Changes in cerebro-cerebellar interaction during response inhibition after performance improvement. NeuroImage. 2014;99:142–8.Google Scholar
  28. 28.
    Stephan K, Marshall J, Friston K, Rowe J. Lateralized cognitive processes and lateralized task control in the human brain. Science. 2003;301(5631):384–6.Google Scholar
  29. 29.
    Padoa-Schioppa C, Li CSR, Bizzi E. Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron. 2002;36(4):751–65.Google Scholar
  30. 30.
    Smith AM, Bourbonnais D, Blanchette G. Interaction between forced grasping and a learned precision grip after ablation of the supplementary motor area. Brain Res. 1981;222(2):395–400.Google Scholar
  31. 31.
    Cramer SC, Weisskoff RM, Schaechter JD, Nelles G, Foley M, Finklestein SP, et al. Motor cortex activation is related to force of squeezing. Hum Brain Mapp. 2002;16(4):197–205.Google Scholar
  32. 32.
    Luppino G, Rizzolatti G. The organization of the frontal motor cortex. News Physiol Sci. 2000;15:219–24.Google Scholar
  33. 33.
    Kendall FP, Kendall FP. Muscles: testing and function with posture and pain: Lippincott Williams & Wilkins; 2005.Google Scholar
  34. 34.
    Visser JE, Bloem BR. Role of the basal ganglia in balance control. Neural Plast. 2005;12(2–3):161–74.Google Scholar
  35. 35.
    Habas C, Cabanis E. Cortical projections to the human red nucleus: a diffusion tensor tractography study with a 1.5-T MRI machine. Neuroradiology. 2006;48(10):755–62.Google Scholar
  36. 36.
    Ghez C, Vicario D. The control of rapid limb movement in the cat. II. Scaling of isometric force adjustments. Exp Brain Res. 1978;33(2):191–202.Google Scholar
  37. 37.
    Ishikawa T, Tomatsu S, Izawa J, Kakei S. The cerebro-cerebellum: could it be loci of forward models? Neurosci Res. 2016;104:72–9.Google Scholar
  38. 38.
    Cerasa A, Hagberg GE, Peppe A, Bianciardi M, Gioia MC, Costa A, et al. Functional changes in the activity of cerebellum and frontostriatal regions during externally and internally timed movement in Parkinson’s disease. Brain Res Bull. 2006;71(13):259–69.Google Scholar
  39. 39.
    Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32(1):413–34.Google Scholar
  40. 40.
    Schmahmann JD. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev. 2010;20(3):236–60.Google Scholar
  41. 41.
    Leiner HC. Solving the mystery of the human cerebellum. Neuropsychol Rev. 2010;20(3):229–35.Google Scholar
  42. 42.
    Boecker H, Jankowski J, Ditter P, Scheef L. A role of the basal ganglia and midbrain nuclei for initiation of motor sequences. NeuroImage. 2008;39(3):1356–69.Google Scholar
  43. 43.
    Stoodley CJ, Valera EM, Schmahmann JD. Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. NeuroImage. 2012;59(2):1560–70.Google Scholar
  44. 44.
    Ng THB, Sowman PF, Brock J, Johnson BW. Neuromagnetic brain activity associated with anticipatory postural adjustments for bimanual load lifting. NeuroImage. 2013;66:343–52.Google Scholar
  45. 45.
    Bradfield LA, Balleine BW. Thalamic control of dorsomedial striatum regulates internal state to guide goal-directed action selection. J Neurosci. 2017;37(13):3721–33.Google Scholar
  46. 46.
    Sang L, Qin W, Liu Y, Han W, Zhang Y, Jiang T, et al. Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. NeuroImage. 2012;61(4):1213–25.Google Scholar
  47. 47.
    Sege CT, Bradley MM, Lang PJ. Startle modulation during emotional anticipation and perception. Psychophysiology. 2014;51(10):977–81.Google Scholar
  48. 48.
    Chudasama Y, Robbins TW. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol Psychol. 2006;73(1):19–38.Google Scholar
  49. 49.
    Redgrave P, Gurney K. The short-latency dopamine signal: a role in discovering novel actions? Nat Rev Neurosci. 2006;7(12):967–75.Google Scholar
  50. 50.
    Bar-Gad I, Morris G, Bergman H. Information processing, dimensionality reduction and reinforcement learning in the basal ganglia. Prog Neurobiol. 2003;71(6):439–73.Google Scholar
  51. 51.
    Frank MJ. Computational models of motivated action selection in corticostriatal circuits. Curr Opin Neurobiol. 2011;21(3):381–6.Google Scholar
  52. 52.
    Gurney KN, Humphries M, Wood R, Prescott TJ, Redgrave P. Testing computational hypotheses of brain systems function: a case study with the basal ganglia. Network. 2004;15(4):263–90.Google Scholar
  53. 53.
    Humphries MD, Stewart RD, Gurney KN. A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J Neurosci. 2006;26(50):12921–42.Google Scholar
  54. 54.
    Kawagoe R, Takikawa Y, Hikosaka O. Expectation of reward modulates cognitive signals in the basal ganglia. Nat Neurosci. 1998;1(5):411–6.Google Scholar
  55. 55.
    Kawaguchi Y, Wilson CJ, Emson PC. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J Neurosci. 1990;10(10):3421–38.Google Scholar
  56. 56.
    Smith AD, Bolam JP. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci. 1990;13(7):259–65.Google Scholar
  57. 57.
    Schultz W, Apicella P, Ljungberg T, Romo R, Scarnati E. Reward-related activity in the monkey striatum and substantia nigra. Prog Brain Res. 1993;99:227–35.Google Scholar
  58. 58.
    Ness V, Beste C. The role of the striatum in goal activation of cascaded actions. Neuropsychologia. 2013;51(13):2562–71.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Chama Belkhiria
    • 1
    Email author
  • Eya Mssedi
    • 1
  • Christophe Habas
    • 2
  • Tarak Driss
    • 1
  • Giovanni de Marco
    • 1
  1. 1.Centre de Recherches sur le Sport et le Mouvement, (CeRSM - EA 2931)UFR STAPS, UPL, Université Paris NanterreNanterreFrance
  2. 2.Service de Neuro-Imagerie, Hôpital des Quinze-VingtsUPMC Paris 6ParisFrance

Personalised recommendations