Hierarchical Aspects of Eye Movement Disorders

  • C. Kennard
Part of the Clinical Medicine and the Nervous System book series (CLIN.MED.NERV.)


Although John Hughlings Jackson often referred to ocular motor control in relation to his general hypothesis of the hierarchical control of movement, he appears only to have written one paper specifically on the subject. It was written in 1909, and was entitled “On some abnormalities of ocular movements”. In this paper he recapitulated his concept of different representations of movements in centres at various levels of the nervous system, this time specifically applied to eye movements. The first level comprised a direct representation of eye movements in the ocular motor nuclei of the brain stem. A second, indirect representation or re-representation of ocular muscles as they are involved in more complex movements was encoded in centres of the middle level, which he interpreted as the motor region of the cerebral cortex. Finally, a third, “doubly indirect” and still more complex representation occurred at the highest level, the prefrontal lobe, containing, as he termed them, the “mental centres”. Thus he suggested a hierarchical control system in which motor impulses depart from the prefrontal lobe and reach the ocular motor periphery via the middle and lowest levels.


Superior Colliculus Ocular Motor Medial Longitudinal Fasciculus Voluntary Saccade Cerebral Blood Flow Study 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adamuk E (1870) Ubere die Innervation der Augenbewegungen. Zentralbi Med Wiss 8: 65Google Scholar
  2. Albano JE, Mishkin M, Westbrook LE, Wurtz RM (1982) Visuomotor deficits following ablation of monkey superior colliculus. J Neurophysiol 48: 338–350PubMedGoogle Scholar
  3. Baker R, Highstem SM (1975) Physiological identification of interneurons and motorneurons in the abducens nucleus. Brain Res 91: 292–298PubMedCrossRefGoogle Scholar
  4. Becker W, Hoehne O, Iwase K, Kornhuber HH (1972) Bereitshaft potential, pramotorische Positivierung and andere Hirnpotentiate bei sakkadischen Augenbewegungen. Vis Res 12: 421–436PubMedCrossRefGoogle Scholar
  5. Bizzi E (1968) Discharge of frontal eye field neurons during saccadic and following eye movements in unanaesthetised monkeys. Exp Brain Res 6: 69–80PubMedCrossRefGoogle Scholar
  6. Bizzi E, Schiller PH (1970) Neuronal activity in the frontal eye fields of unanaesthetised monkeys during head and eye movement. Exp Brain Res 10: 151–158CrossRefGoogle Scholar
  7. Brinkman C, Porter R (1979) Supplementary motor area in the monkey: activity of neurons during performance of a learned motor task. J Neurophysiol 42: 681–709PubMedGoogle Scholar
  8. Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603–635PubMedGoogle Scholar
  9. Bruce CJ, Goldberg ME, Bushnell MC, Stanton GB (1985) Primate frontal eye fields II. Physiological and anatomical correlates of electrically evoked eye movements. J Neurophysiol 54: 714–734PubMedGoogle Scholar
  10. Büttner-Ennever JA, Akert K (1981) Medial rectus subgroups of the oculomotor nucleus and their abducens internuclear input in the monkey. J Comp Neurol 197: 17–27PubMedCrossRefGoogle Scholar
  11. Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57: 1383–1409PubMedGoogle Scholar
  12. Distel H, Fries W (1982) Contralateral cortical projections to the superior colliculus in the macaque monkey. Exp Brain Res 48: 157–162PubMedCrossRefGoogle Scholar
  13. Ferrier D (1874) The localisation of function in the brain. Proc R Soc Lond (Series B) 22: 229–232Google Scholar
  14. Ferrier D (1986) Functions of the brain. Smith, Elder, LondonGoogle Scholar
  15. Fox PT, Fox JM, Raichle ME, Burder RM (1985) The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. J Neurophysiol 54: 348–369PubMedGoogle Scholar
  16. Fuchs AF, Kaneko CRS, Scudder CA (1985) Brainstem control of saccadic eye movements. Annu Rev Neurosci 8: 307–337PubMedCrossRefGoogle Scholar
  17. Gibson JM, Pimlott R, Kennard C (1987) Ocular motor and manual tracking in Parkinson’s disease and the effect of treatment. J Neurol Neurosurg Psychiatry 50: 853–860PubMedCrossRefGoogle Scholar
  18. Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp Brain Res 58: 455–472PubMedCrossRefGoogle Scholar
  19. Hikosaka O, Wurtz RH (1983a) Visual and oculomotor functions of monkey substantia nigra pars reticulata. I Relation of visual and auditory responses to saccades. J Neurophysiol 49: 1230–1253Google Scholar
  20. Hikosaka O, Wurtz RT (1983b) Visual and oculomotor functions of monkey substantia nigra pars reticulata. II Visual responses related to fixation of gaze. J Neurophysiol 49: 1254–1267Google Scholar
  21. Hikosaka O, Wurtz RH (1983c) Visual and oculomotor functions of monkey substantia nigra pars reticulata. III Memory contingent visual and saccade responses. J Neurophysiol 49: 1269–1284Google Scholar
  22. Hikosaka O, Wurtz RH (1983d) Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV Relation of substantia nigra to superior colliculus. J Neurophysiol 49: 1285–1301Google Scholar
  23. Hikosaka, O, Wurtz RH (1985a) Modification of saccadic eye movements by GABA-related substances. I Effect of muscimol and bicuculline in monkey superior colliculus. J Neurophysiol 53: 266–291Google Scholar
  24. Hikosaka O, Wurtz RH (1985b) Modification of saccadic eye movements by GABA-related substances. II Effects of muscimol in monkey substantia nigra pars reticulata. J Neurophysiol 53: 292–308Google Scholar
  25. Holmes G (1938) The cerebral integration of the ocular movements. Br Med J II: 107–112PubMedCrossRefGoogle Scholar
  26. Jackson JH (1909) On some abnormalities of ocular movements. Lancet I: 900–912CrossRefGoogle Scholar
  27. Jayaraman A, Batton RR III, Carpenter MB (1977) Nigrotectal projections in the monkey: an autoradiographic study. Brain Res 135: 147–152PubMedCrossRefGoogle Scholar
  28. Keating EG, Gooley SG, Pratt SE, Kelsey JE (1983) Removing the superior colliculus silences eye movements normally evolved from stimulation of the parietal and occipital eye fields. Brain Res 269: 145–148PubMedCrossRefGoogle Scholar
  29. Keller EL (1974) Participation of medial pontine reticular formation in eye movement generation in monkey. J Neurophysiol 37: 316–332PubMedGoogle Scholar
  30. King WM, Precht W, Dieringer N (1980) Afferent and efferent connections of cat omnipause neurons. Exp Brain Res 38: 395–403PubMedCrossRefGoogle Scholar
  31. Leichnetz GR, Spencer RF, Smith DJ (1984) Cortical projections to nuclei adjacent to the oculomotor complex in the medial dienmesencephalic tegmentum in the monkey. J Comp Neurol 228: 359–387PubMedCrossRefGoogle Scholar
  32. Leigh RJ, Newman SA, Folstein SE, Lasker AG, Jensen BA (1983) Abnormal ocular motor control in Huntington’s disease. Neurology 33: 1268–1275PubMedGoogle Scholar
  33. Lesser RP, Leigh RJ, Dinner DS, Luden H, Morris HH, Tomsak RL, Lockwood KI (1985) Preservation of voluntary saccades after intracarotid injection of barbiturates. Neurology 35: 1108–1112PubMedGoogle Scholar
  34. Luria AR (1966) Higher cortical functions in man. Translated by Haigh B. Basic Books, New York, pp 293–327Google Scholar
  35. Lynch JC, Graybiel AM, Lobeck LJ (1985) The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. J Comp Neurol 235: 241–254PubMedCrossRefGoogle Scholar
  36. Mays LE, Sparks DL (1980) Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol 43: 207–231PubMedGoogle Scholar
  37. Melamed E, Larson B (1979) Cortical activation pattern during saccadic eye movements in humans: localisation by focal cerebral blood flow increases. Ann Neurol 5: 79–88PubMedCrossRefGoogle Scholar
  38. Penfield W, Jasper H (1954) Epilepsy and the functional anatomy of the human brain. Little, Brown, BostonGoogle Scholar
  39. Robinson DA, Fuchs AF (1969) Eye movements evoked by stimulation of frontal eye fields. J Neurophysiol 32: 637–648PubMedGoogle Scholar
  40. Schiller PH, Stryker M (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35: 915–924PubMedGoogle Scholar
  41. Schiller PH, True SD, Conway JL (1980) Deficits in eye movements following frontal eye-field and superior colliculus ablations. J Neurophysiol 44: 1175–1189PubMedGoogle Scholar
  42. Schlag J, Schalg-Rey M (1987) Evidence for a supplementary eye field. J Neurophysiol 57: 179–200PubMedGoogle Scholar
  43. Schnyder H, Reisine H, Hepp K, Henn V (1985) Frontal eye field projection to the paramedian pontine reticular formation traced with wheat germ agglutinin in the monkey. Brain Res 329: 151–160PubMedCrossRefGoogle Scholar
  44. Shibutani H, Sakata H, Hyvarinen J (1984) Saccade and blinking evoked by microstimulation of the posterior parietal association cortex of the monkey. Exp Brain Res 55: 1–8PubMedCrossRefGoogle Scholar
  45. Steiner I, Melamed E (1984) Conjugate eye deviation after acute hemispheric stroke: delayed recovery after previous contralateral frontal lobe damage. Ann Neurol 16: 509–511PubMedCrossRefGoogle Scholar
  46. Wagman IH, Krieger HP, Papatheodorou CA, Bender MB (1961) Eye movements elicited by surface and depth stimulation of the frontal lobe of Macaque mulatta. J Comp Neurol 117: 179–188PubMedCrossRefGoogle Scholar
  47. White OB, Saint-Cyr JA, Tomlinson RD, Sharpe JA (1983) Ocular motor deficits in Parkinson’s disease. II. Control of the saccadic and smooth pursuit systems. Brain 106: 571–587PubMedCrossRefGoogle Scholar
  48. Woolsey CN, Settlage PH, Meyer DR, Spencer W, Hamuy TP, Travis AM (1952) Patterns of location in the precentral and `supplementary’ motor area and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis 30: 238–264PubMedGoogle Scholar
  49. Wurtz RH, Albano JE (1980) Visual-motor functions of the primate superior colliculus. Annu Rev Neurosci 3: 189–226PubMedCrossRefGoogle Scholar
  50. Zee DS (1984) Ocular motor control: the cerebral control of saccadic eye movements. In: Lessell S, van Dalen JTW (eds) Neuropathalmology 1984, vol 3, Elsevier, Amsterdam, pp 141–156Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • C. Kennard

There are no affiliations available

Personalised recommendations