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Processing of Limb Kinematics in the Interpositus Nucleus

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Abstract

Neural representations of limb movement kinematic parameters are common among central nervous system structures involved in motor control, such as the interpositus nucleus of the cerebellum. Much experimental evidence indicates that neurons in the interpositus may encode limb kinematic parameters both during active, voluntary actions and during limb motion imposed passively, which entrains only sensory afferents. With respect to the sensory processing of information related to movement kinematics, we show that interpositus neuronal activity can parse out the directional from the scalar component (i.e., the movement speed) of the velocity vector. Moreover, a differential role for the anterior and posterior portion of interpositus in encoding these parameters emerged from these data, since the activity of the posterior interpositus was specifically associated to changes of movement speed. Limb movement representations in the interpositus nucleus may be instrumental for the control of goal-directed movements such as shaping hand during grasping or precise foot placement during gait. Finally, we discuss the idea that sensory information about the movement kinematics contribute to both feedback and anticipatory processes for limb movement control.

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References

  1. Brooks VB, Thach WT (1981) Cerebellar control of posture and movement. In: Brookhart JM, Mountcastle VB (eds) Handbook of Physiology, Neurophysiology, vol. II. American Physiological Society, Bethesda, pp 877–946

    Google Scholar 

  2. Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15:403–442

    Article  CAS  PubMed  Google Scholar 

  3. Milak MS, Shimansky Y, Bracha V, Bloedel JR (1997) Effects of inactivating individual cerebellar nuclei on the performance and retention of an operantly conditioned forelimb movement. J Neurophysiol 78:939–959

    CAS  PubMed  Google Scholar 

  4. Martin JH, Cooper SE, Hacking A, Ghez C (2000) Differential effects of deep cerebellar nuclei inactivation on reaching and adaptive control. J Neurophysiol 83:1886–1899

    CAS  PubMed  Google Scholar 

  5. Harvey RJ, Porter R, Rawson JA (1979) Discharges of intracerebellar nuclear cells in monkeys. J Physiol 297:559–580

    CAS  PubMed  Google Scholar 

  6. Cody FW, Moore RB, Richardson HC (1981) Patterns of activity evoked in cerebellar interpositus nuclear neurones by natural somatosensory stimuli in awake cats. J Physiol 317:1–20

    CAS  PubMed  Google Scholar 

  7. Thach WT (1968) Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J Neurophysiol 31:785–797

    CAS  PubMed  Google Scholar 

  8. Thach WT (1970) Discharge of cerebellar neurons related to two maintained postures and two prompt movements. II. Purkinje cell output and input. J Neurophysiol 33:537–547

    CAS  PubMed  Google Scholar 

  9. Fortier PA, Kalaska JF, Smith AM (1989) Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J Neurophysiol 62:198–211

    CAS  PubMed  Google Scholar 

  10. Schieber MH, Thach WT Jr (1985) Trained slow tracking. II. Bidirectional discharge patterns of cerebellar nuclear, motor cortex, and spindle afferent neurons. J Neurophysiol 54:1228–1270

    CAS  PubMed  Google Scholar 

  11. MacKay WA (1988) Unit activity in the cerebellar nuclei related to arm reaching movements. Brain Res 442:240–254

    Article  CAS  PubMed  Google Scholar 

  12. MacKay WA (1988) Cerebellar nuclear activity in relation to simple movements. Exp Brain Res 71:47–58

    Article  CAS  PubMed  Google Scholar 

  13. Gibson AR, Horn KM, Stein JF, Van Kan PL (1996) Activity of interpositus neurons during a visually guided reach. Can J Physiol Pharmacol 74:499–512

    Article  CAS  PubMed  Google Scholar 

  14. van Kan PL, Houk JC, Gibson AR (1993) Output organization of intermediate cerebellum of the monkey. J Neurophysiol 69:57–73

    PubMed  Google Scholar 

  15. van Kan PL, Horn KM, Gibson AR (1994) The importance of hand use to discharge of interpositus neurones of the monkey. J Physiol 480:171–190

    PubMed  Google Scholar 

  16. Mason CR, Miller LE, Baker JF, Houk JC (1998) Organization of reaching and grasping movements in the primate cerebellar nuclei as revealed by focal muscimol inactivations. J Neurophysiol 79:537–554

    CAS  PubMed  Google Scholar 

  17. Casabona A, Valle MS, Bosco G, Garifoli A, Lombardo SA, Perciavalle V (2003) Anisotropic representation of forelimb position in the cerebellar cortex and nucleus interpositus of the rat. Brain Res 972:127–136

    Article  CAS  PubMed  Google Scholar 

  18. Casabona A, Valle MS, Bosco G, Perciavalle V (2004) Cerebellar encoding of limb position. Cerebellum 3:172–177

    Article  PubMed  Google Scholar 

  19. Casabona A, Valle MS, Bosco G, Perciavalle V (2008) Comparison of neuronal activities of external cuneate nucleus, spinocerebellar cortex and interpositus nucleus during passive movements of the rat's forelimb. Neuroscience 157:271–279

    Article  CAS  PubMed  Google Scholar 

  20. Valle MS, Bosco G, Casabona A, Garifoli A, Perciavalle V, Coco M, Perciavalle V (2009) Representation of movement velocity in the rat's interpositus nucleus during passive forelimb movements. European Workshop on Movement Science. Lisbon 102

  21. Burton JE, Onoda N (1978) Dependence of the activity of interpositus and red nucleus neurons on sensory input data generated by movement. Brain Res 152:41–63

    Article  CAS  PubMed  Google Scholar 

  22. Soechting JF, Burton JE, Onoda N (1978) Relationships between sensory input, motor output and unit activity in interpositus and red nuclei during intentional movement. Brain Res 152:65–79

    Article  CAS  PubMed  Google Scholar 

  23. Garifoli A, Caserta C, Bosco G, Lombardo SA, Casabona A, Perciavalle V (2002) Kinematic features of passive forelimb movements and rat cuneate neuron discharges. NeuroReport 13:267–271

    Article  PubMed  Google Scholar 

  24. Bosco G, Poppele RE (2000) Reference frames for spinal proprioception: kinematics based or kinetics based? J Neurophysiol 83:2946–2955

    CAS  PubMed  Google Scholar 

  25. Bosco G, Poppele RE (1997) Representation of multiple kinematic parameters of the cat hindlimb in spinocerebellar activity. J Neurophysiol 78:1421–1432

    CAS  PubMed  Google Scholar 

  26. MacKay WA, Murphy JT (1974) Responses of interpositus neurons to passive muscle stretch. J Neurophysiol 37:1410–1423

    CAS  PubMed  Google Scholar 

  27. Kawaguchi S, Ono T (1974) Responses of interpositus neurones to inputs from muscle receptors. Exp Brain Res 21:375–386

    Article  CAS  PubMed  Google Scholar 

  28. Eccles JC, Rosen I, Scheid P, Taborikova H (1972) Cutaneous afferent responses in interpositus neurones of the cat. Brain Res 42:207–211

    Article  CAS  PubMed  Google Scholar 

  29. Rowland NC, Jaeger D (2005) Coding of tactile response properties in the rat deep cerebellar nuclei. J Neurophysiol 94:1236–1251

    Article  PubMed  Google Scholar 

  30. Soteropoulos DS, Baker SN (2008) Bilateral representation in the deep cerebellar nuclei. J Physiol 586:1117–1136

    Article  CAS  PubMed  Google Scholar 

  31. Zackowski KM, Thach WT Jr, Bastian AJ (2002) Cerebellar subjects show impaired coupling of reach and grasp movements. Exp Brain Res 146:511–522

    Article  CAS  PubMed  Google Scholar 

  32. Thach WT, Bastian AJ (2004) Role of the cerebellum in the control and adaptation of gait in health and disease. Prog Brain Res 143:353–366

    Article  PubMed  Google Scholar 

  33. Cooper SE, Martin JH, Ghez C (2000) Effects of inactivation of the anterior interpositus nucleus on the kinematic and dynamic control of multijoint movement. J Neurophysiol 84:1988–2000

    CAS  PubMed  Google Scholar 

  34. Bastian AJ, Martin TA, Keating JG, Thach WT (1996) Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol 76:492–509

    CAS  PubMed  Google Scholar 

  35. Miall RC, Weir DJ, Stein JF (1987) Visuo-motor tracking during reversible inactivation of the cerebellum. Exp Brain Res 65:455–464

    Article  CAS  PubMed  Google Scholar 

  36. Giaquinta G, Valle MS, Caserta C, Casabona A, Bosco G, Perciavalle V (2000) Sensory representation of passive movement kinematics by rat's spinocerebellar Purkinje cells. Neurosci Lett 285:41–44

    Article  CAS  PubMed  Google Scholar 

  37. Fu QG, Flament D, Coltz JD, Ebner TJ (1997) Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. J Neurophysiol 78:478–491

    CAS  PubMed  Google Scholar 

  38. Coltz JD, Johnson MTV, Ebner TJ (1999) Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J Neurosci 19:1782–1803

    CAS  PubMed  Google Scholar 

  39. Roitman AV, Pasalar S, Johnson MT, Ebner TJ (2005) Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J Neurosci 25:9244–9257

    Article  CAS  PubMed  Google Scholar 

  40. Tarnecki R, Morrison AR, Rajkowski J (1974) Neuronal activity in normal and cortically deprived interpositus neurons of the cat. Brain Res 73(3):534–539

    Article  CAS  PubMed  Google Scholar 

  41. Holdefer RN, Houk JC, Miller LE (2005) Movement-related discharge in the cerebellar nuclei persists after local injections of GABA(A) antagonists. J Neurophysiol 93(1):35–43

    Article  CAS  PubMed  Google Scholar 

  42. Apps R, Garwicz M (2005) Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6:297–311

    Article  CAS  PubMed  Google Scholar 

  43. van Kan PL, McCurdy ML (2001) Role of primate magnocellular red nucleus neurons in controlling hand preshaping during reaching to grasp. J Neurophysiol 85:1461–1478

    PubMed  Google Scholar 

  44. van Kan PL, McCurdy ML (2002) Discharge of primate magnocellular red nucleus neurons during reaching to grasp in different spatial locations. Exp Brain Res 142:151–157

    Article  PubMed  Google Scholar 

  45. van Kan PL, McCurdy ML (2002) Contribution of primate magnocellular red nucleus to timing of hand preshaping during reaching to grasp. J Neurophysiol 87:1473–1487

    PubMed  Google Scholar 

  46. Miller LE, Sinkjaer T (1998) Primate red nucleus discharge encodes the dynamics of limb muscle activity. J Neurophysiol 80:59–70

    CAS  PubMed  Google Scholar 

  47. Johnson MT, Ebner TJ (2000) Processing of multiple kinematic signals in the cerebellum and motor cortices. Brain Res Brain Res Rev 33:155–168

    Article  CAS  PubMed  Google Scholar 

  48. Johnson MT, Coltz JD, Ebner TJ (1999) Encoding of target direction and speed during visual instruction and arm tracking in dorsal premotor and primary motor cortical neurons. Eur J NeuroSci 81:4433–4445

    Article  Google Scholar 

  49. Prud'homme MJ, Kalaska JF (1994) Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. J Neurophysiol 72:2280–2301

    PubMed  Google Scholar 

  50. Thach WT (1978) Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. J Neurophysiol 41:654–676

    CAS  PubMed  Google Scholar 

  51. Gordon J, Ghilardi MF, Ghez C (1995) Impairments of reaching movements in patients without proprioception. I. Spatial errors. J Neurophysiol 73:347–360

    CAS  PubMed  Google Scholar 

  52. Allen GI, Tsukahara N (1974) Cerebrocerebellar communication systems. Physiol Rev 54:957–1006

    CAS  PubMed  Google Scholar 

  53. Allen GI, Gilbert PF, Marini R, Schultz W, Yin TC (1977) Integration of cerebral and peripheral inputs by interpositus neurons in monkey. Exp Brain Res 27:81–99

    Article  CAS  PubMed  Google Scholar 

  54. Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16:645–649

    Article  CAS  PubMed  Google Scholar 

  55. Blakemore SJ, Frith CD, Wolpert DM (2001) The cerebellum is involved in predicting the sensory consequences of action. NeuroReport 12:1879–1884

    Article  CAS  PubMed  Google Scholar 

  56. Schweighofer N, Spoelstra J, Arbib MA, Kawato M (1998) Role of the cerebellum in reaching movements in humans. II. A neural model of the intermediate cerebellum. Eur J NeuroSci 10:95–105

    Article  CAS  PubMed  Google Scholar 

  57. Ebner TJ, Pasalar S (2008) Cerebellum predicts the future motor state. Cerebellum 7:583–588

    Article  PubMed  Google Scholar 

  58. Miall RC, King D (2008) State estimation in the cerebellum. Cerebellum 7:572–576

    Article  PubMed  Google Scholar 

  59. Wolpert DM, Ghahramani Z, Flanagan JR (2001) Perspectives and problems in motor learning. Trends Cogn Sci 5:487–494

    Article  PubMed  Google Scholar 

  60. Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26:9107–9116

    Article  CAS  PubMed  Google Scholar 

  61. Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J Neurophysiol 93:2809–2821

    Article  PubMed  Google Scholar 

  62. Lang CE, Bastian AJ (1999) Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82:2108–2119

    CAS  PubMed  Google Scholar 

  63. Diedrichsen J, Verstynen T, Lehman SL, Ivry RB (2005) Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol 93:801–812

    Article  PubMed  Google Scholar 

  64. Monzee J, Drew T, Smith AM (2004) Effects of muscimol inactivation of the cerebellar nuclei on precision grip. J Neurophysiol 91:1240–1249

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Physiological Sciences, University of Catania, viale Andrea Doria 6, 95125, Catania, Italy

    Antonino Casabona, Vincenzo Perciavalle & Maria Stella Valle

  2. Department of Neuromotor Physiology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy

    Gianfranco Bosco

  3. Department of Neuroscience and Center for Space Biomedicine, University of Tor Vergata, 00173, Rome, Italy

    Gianfranco Bosco

Authors
  1. Antonino Casabona
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  2. Gianfranco Bosco
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  3. Vincenzo Perciavalle
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  4. Maria Stella Valle
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Correspondence to Vincenzo Perciavalle.

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Casabona, A., Bosco, G., Perciavalle, V. et al. Processing of Limb Kinematics in the Interpositus Nucleus. Cerebellum 9, 103–110 (2010). https://doi.org/10.1007/s12311-009-0149-x

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