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In Vivo Structural and Functional Imaging of the Human Rubral and Inferior Olivary Nuclei: A Mini-review

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Abstract

Few imaging studies have been devoted to the structural and functional connectivity of the red and inferior olivary nuclei although these two nuclei represent two main targets of the cerebellum within the brainstem. However, the RN is anatomically and functionally related to a widespread sensorimotor, limbic, and executive brain network. It projects massively onto the principal olive with which it contributes to a cerebello-rubro-olivo-cerebellar loop modulated by cortical and subcortical afferents. Despite a minor role in planning and execution of rhythmic movements, the red nucleus in conjunction with the inferior olive, more specifically involved in the detection of “unexpected” events, contributes to sensorimotor, sensory and, likely, cognitive higher functions.

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References

  1. Massion J (1967) The mammalian red nucleus. Physiol Rev 47:383–436

    CAS  PubMed  Google Scholar 

  2. Azizi SA (2007) ...And the olive said to the cerebellum: organization and functional significance of the olivo-cerebellar system. Neuroscientist 13:646–625

    Google Scholar 

  3. Nieuwenhuys R, Voogt J, vanHuijzen C (eds) (2008) The human central nervous system. A synopsis and atlas, 4th revised edn. Springer, Berlin Heidelberg New York

  4. ten Donkelaar HJ (1988) Evolution of the red nucleus and the rubrospinal tract. Behav Brain Res 28:9–20

    Article  PubMed  Google Scholar 

  5. Lapresle J (1979) Rhythmic palatal myoclonus and the dentate-olivary pathway. J Neurol 200:223–230

    Article  Google Scholar 

  6. Larochelle L, Bedard P, Boucher R, Poirier LJ (1970) The rubro-olivo-cerebello-rubral loop and postural tremor in the monkey. J Neurol Sci 11:53–64

    Article  CAS  PubMed  Google Scholar 

  7. Lavezzi AM, Corna M, Matturri L, Santoro F (2009) Neuropathology of the Guillain–Mollaret Triangle (dentate-rubro-olivary network) in sudden unexplained perinatal death and SIDS. Open Neurol J 3:48–53

    Article  PubMed  Google Scholar 

  8. Miller LE, van Kan PL, Sinjjaer T, Andersen T, Harris GD, Houk JC (1993) Correlation of primate red nucleus discharge with muscle activity during free-form arm movements. J Physiol 469:213–243

    CAS  PubMed  Google Scholar 

  9. Lefebvre V, Josien E, Pasquier F, Steinling M, Petit H (1993) Infarctus du noyau rouge et diaschisis cérébelleux croisé. Rev Neurol (Paris) 149:294–296

    CAS  Google Scholar 

  10. Ito M (2005) Bases and implications of learning in the cerebellum—adaptative control and internal model mechanism. Prog Brain Res 148:95–109

    Article  PubMed  Google Scholar 

  11. Llinas RR (2009) Inferior olive oscillation as the temporal basis for motricity and oscillatory reset as the basis for motor error correction. Neuroscience 162:797–804

    Article  CAS  PubMed  Google Scholar 

  12. Thompson RF, Steinmetz JE (2009) The role of cerebellum in classical conditioning of discrete behavioural responses. Neurosci 162:732–755

    Article  CAS  Google Scholar 

  13. Jacobson GA, Rokni D, Yarom Y (2008) A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci 31:617–625

    Article  CAS  PubMed  Google Scholar 

  14. Schmahmann JD, Pandya DN (1997) The cerebrocerebellar system. Int Rev Neurobiol 41:31–60

    Article  CAS  PubMed  Google Scholar 

  15. Kelly RM, Strick PL (2003) Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci 23:8432–8444

    CAS  PubMed  Google Scholar 

  16. Ralston DD (1994) Corticorubral synaptic organization in Macaca fascicularis: a study utilizing degeneration, anterograde transport of WGA-HRP, and combined immuno-GABA-gold technique and computer-assisted reconstruction. J Comp Neurol 50:657–673

    Article  Google Scholar 

  17. Humphrey DR, Gold R, Reed DJ (1984) Sizes, laminar and topographical origins of cortical projections to the major divisions of the red nucleus in the monkey. J Comp Neurol 225:75–94

    Article  CAS  PubMed  Google Scholar 

  18. Stanton GB (1980) Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: an anterograde degeneration study. J Comp Neurol 190:699–731

    Article  CAS  PubMed  Google Scholar 

  19. Miller RA, Strominger NL (1973) Efferent connections of the red nucleus in the brainstem and spinal cord of the rhesus monkey. J Comp Neurol 152:327–346

    Article  CAS  PubMed  Google Scholar 

  20. Ito M (1984) The cerebellum and neural control. Raven, New York

    Google Scholar 

  21. Von Monakow C (1895) Experimentelle und pathologisch-anatomische Untersuchungen über die Haubenregion, den Schlügel und die Regio subthalamica nebst Beiträge zur Kenntnis früh erworbener Gross- und Kleinhirndefecte. Arch Psychiatr Nervenkr 27:1–128 386-478

    Article  Google Scholar 

  22. Archambault L (1914-1915) Les connexions corticales du noyau rouge. Nouvelle Iconographie Salpêtrière 27:188–225

    Google Scholar 

  23. Meyer M (1949) Study of efferent connections of the frontal lobe in the human brain after leucotomy. Brain 72:265–296

    Article  CAS  PubMed  Google Scholar 

  24. Kanki S, Ban T (1952) Corticofugal connections of the frontal lobe in man. Med J Osaka Univ 3:201–222

    Google Scholar 

  25. Habas C, Cabanis EA (2006) Cortical projections to the human red nucleus: a diffusion tensor tractography study with a 1.5-T machine. Neuroradiology 48:755–762

    Article  PubMed  Google Scholar 

  26. Habas C, Cabanis EA (2007) Cortical projections to the human red nucleus: complementary results with probabilistic tractography at 3 T. Neuroradiology 49:777–784

    Article  PubMed  Google Scholar 

  27. Habas C, Cabanis EA (2007) Anatomical parcellation of the brainstem and cerebellar white matter: a preliminary probabilistic tractography study at 3 T. Neuroradiology 49:849–863

    Article  PubMed  Google Scholar 

  28. Granziera C, Schmahmann JD, Hadjikhani N, Meyer H, Meuli R, Wedeen V, Krueger G (2009) Diffusion spectrum imaging shows the structural basis of functional cerebellar circuits in the human cerebellum system in vivo. PLOSone 4

  29. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting brain using echo-planar MRI. Magn Reson Med 34:537–541

    Article  CAS  PubMed  Google Scholar 

  30. Fox MD, Raischle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711

    Article  CAS  PubMed  Google Scholar 

  31. Nioche C, Cabanis EA, Habas C (2009) Functional connectivity of the human red nucleus in the brain resting state at 3 T. AJNR Am J Neuroradiol 30:396–403

    Article  CAS  PubMed  Google Scholar 

  32. Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, Greicius MD (2009) Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci 29:8586–8594

    Article  CAS  PubMed  Google Scholar 

  33. Liu Y, Pu Y, Gao JH, Parsons LM, Xiong J, Liotti M, Bower JM, Fox PT (2000) The human red nucleus and lateral cerebellum in supporting roles for sensory information processing. Hum Brain Mapp 10:147–159

    Article  CAS  PubMed  Google Scholar 

  34. Habas C, Cabanis EA (2007) The neural network involved in a bimanual tactile-tactile matching discrimination task: a functional imaging study at 3 T. Neuroradiology 49:681–688

    Article  PubMed  Google Scholar 

  35. Xu D, Liu T, Ashe J, Bushara KO (2006) Role of the olivo-cerebellar system in timing. J Neurosci 26:5990–5995

    Article  CAS  PubMed  Google Scholar 

  36. Cunnington R, Windischberger C, Deecke L, Moser E (2002) The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. NeuroImage 15:373–385

    Article  CAS  PubMed  Google Scholar 

  37. Boecker H, Jankowski J, Ditter P, Scheef L (2008) A role of the basal ganglia and midbrain nuclei for initiation of motor sequences. NeuroImage 39:1356–1369

    Article  CAS  PubMed  Google Scholar 

  38. Wetter TC, Eisensehr I, Trenkwalder C (2004) Functional neuroimaging studies in restless legs syndrome. Sleep Med 5:401–406

    Article  PubMed  Google Scholar 

  39. Boecker H, Kleinschmidt A, Weindl A, Conrad B, Hänicke W, Frahm J (1994) Dysfunctional activation of subcortical nuclei in palatal myoclonus detected by high-resolution MRI. NMR Biomedecin 7:327–329

    Article  CAS  Google Scholar 

  40. Bingel U, Quante M, Knab R, Bromm B, Weiller C, Büchel C (2003) Single fMRI reveals significant contralateral bias in responses to laser pain within thalamus and somatosensory cortices. NeuroImage 18:740–748

    Article  CAS  PubMed  Google Scholar 

  41. Dunckley P, Wise RG, Fairhurst M, Hobden P, Aziz Q, Chang L, Tracey I (2005) A comparison of visceral and somatic pain processing in the human brainstem using functional magnetic resonance imaging. J Neurosci 25:7333–7341

    Article  CAS  PubMed  Google Scholar 

  42. Bhatt S, Mbwana J, Adeymo A, Sawyer A, Hailu A, VanMeter J (2009) Lying about facial recognition: an fMRI study. Brain Cogn 69:382–390

    Article  CAS  PubMed  Google Scholar 

  43. Sörös P, Sokoloff LG, Bose A, McIntosh AR, Graham SJ, Stuss DT (2006) Clustered functional of overt speech production. NeuroImage 32:376–387

    Article  PubMed  Google Scholar 

  44. Alain C, Reinke K, McDonald KL, Chau W, Tam F, Pacucar A, Graham S (2005) Left thalamo-cortical network implicated in successful speech separation and identification. NeuroImage 26:592–599

    Article  PubMed  Google Scholar 

  45. Desmond JE, Gabrieli JDE, Wagner AD, Ginier BL, Glover GH (1997) Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci 17:9675–9685

    CAS  PubMed  Google Scholar 

  46. Pu Y, Liu Y, JH GAO, Parsons LM, Xiong J, Liotti M, Qin YL, Bower JM, Fox PT (1998) Implication of human inferior olive in sensory discrimination, a fMR study (Abstract). Society of Neurosci 24:1150

    Google Scholar 

  47. Liu T, Xu D, Ashe J, Bushara K (2008) The specificity of inferior olive response to stimulus timing. J Neurophysiol 100:1557–1561

    Article  CAS  PubMed  Google Scholar 

  48. Gautier JC, Blackwood W (1961) Enlargement of the inferior olivary nucleus in association with lesions of the central tegmental tract or dentate nucleus. Brain 84:341

    Article  CAS  PubMed  Google Scholar 

  49. Jellinger K (1973) Hypertrophy of the inferior olives: report on 29 cases. Z Neurol 205:153

    Article  CAS  PubMed  Google Scholar 

  50. Gotto N, Kakimi S, Kaneko M (1988) Olivary enlargement: stage of initial astrocytic changes. Clin Neuropathol 7:39–43

    Google Scholar 

  51. Goyal M, Versnick E, Tuite P, Saint Cyr J, Kucharczyk W, Montanera W, Willinsky R, Mikulis D (2000) Hypertrophic olivary degeneration: metaanalysis of the temporal evolution of MR findings. AJNR Am J Neuroradiol 21:1073–1077

    CAS  PubMed  Google Scholar 

  52. Guillain G, Mollaret P (1931) Deux cas de myoclonies synchrones et rythmées vélo-pharyngo-laryngo-oculo-diaphragmatiques. Rev Neurol (Paris) 2:545

    Google Scholar 

  53. Duvelleroy Hommet C, de Toffol B, Cottier JP, Autret A (1998) Bilateral olivary hypertrophy and palatal myoclonus. Surg Neurol 49:215–216

    Article  Google Scholar 

  54. Wu JC, Lu CS, Ng SH (2000) Limb myorhythmia in association with hypertrophy of the inferior olive: report of two cases. Chang Gung Med J 23:630–635

    CAS  PubMed  Google Scholar 

  55. Boecker H, Kleinschmidt A, Weindl A, Conrad B, Hänicke W, Frahm J (1994) Dysfunctional activation of subcortical nuclei in palatal myoclonus detected by high-resolution MRI. NMR Biomed 7:327–329

    Article  CAS  PubMed  Google Scholar 

  56. Nitschke MF, Kruger G, Bruhn H, Klein C, Gehrking E, Wessel K, Frahm J, Vieregge P (2001) Voluntary palatal tremor is associated with hyperactivation of the inferior olive: a functional magnetic resonance imaging study. Mov Disord 16:1193–1195

    Article  CAS  PubMed  Google Scholar 

  57. Hong S, Leigh RJ, Zee DS, Optican LM (2008) Inferior olive hypertrophy and cerebellar learning are both needed to explain ocular oscillations in oculopalatal tremor. Prog Brain Res 171:219–226

    Article  PubMed  Google Scholar 

  58. Ramnani N, Behrens TEJ, Johansen-Berg H, Richter MC, Pinsk MA, Andersson JLR, Rudebeck P, Ciccarelli et al (2005) The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from macaque monkeys and humans. Cereb Cortex 16:811–818

    Article  PubMed  Google Scholar 

  59. Habas C (2009) Functional imaging of the deep cerebellar nuclei: a review. Cerebellum Jun 10 [Epub ahead of print]

  60. Stoodley CJ, Schmahmann JD (2008) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage 44:489–501

    Article  PubMed  Google Scholar 

  61. Schmahmann (2004) Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsych Clin Neurosci 16:367–378

    Google Scholar 

  62. Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058

    Article  CAS  PubMed  Google Scholar 

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Habas, C., Guillevin, R. & Abanou, A. In Vivo Structural and Functional Imaging of the Human Rubral and Inferior Olivary Nuclei: A Mini-review. Cerebellum 9, 167–173 (2010). https://doi.org/10.1007/s12311-009-0145-1

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