A review of current concepts in ocular motor neurophysiology is presented. Four separate subsystems of eye movements are recognized: saccadic, smooth pursuit, vergence, and vestibular. Each subsystem is characterized by different physiologic characteristics and different anatomic substrates which may be selectively affected in different pathologic states. A further eye movement response, optokinetic nystagmus, is complex and may be considered a separate system. To regard the horizontal optokinetic response as merely a combination of pursuit and saccades is an oversimplification but one which may be useful in clinical localization.
Get full access to this article
View all access options for this article.
References
1.
PedersenRAAbelLATroostBT. Anatomy of eye movements. In: JacobiecFBiomedical foundations in ophthalmology. Hagerstown: Harper and Row (in press).
2.
DaroffRBTroostBT. Supranuclear disorders of eye movements. In: GlaserJSNeuro-ophthalmology.Hagerstown: Harper and Row, 1978: 201–18.
3.
TroostBTDell'OssoLF. Fast eye movements (saccades): Basic science and clinical correlations. In: ThompsonHSTopics in neuro-ophthalmology.Baltimore: Williams and Wilkins, 1979: 246–65.
4.
BahillATTroostBT. Types of saccadic eye movements. Neurology1979; 29:1150–2.
5.
CarpenterRHS. Movements of the eyes. London: Pion Press, 1977.
6.
BakerRBerthozA.Control of gaze by brain stem neurons, developments in neuroscience. New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977.
7.
BrooksBABajandasFJ. Eye movements, ARVO symposium. New York: Plenum Press, 1977.
8.
ThompsonH.Topics in neuro-ophthalmology. Baltimore: Williams and Wilkins, 1979.
9.
BeckerWJurgensR.An analysis of the saccadic system by means of double step stimuli. Vision Res1979; 19:967–83.
10.
HouRLFenderDH. Processing of direction and magnitude by the saccadic eye-movements system. Vision Res1979; 19:1421–6.
11.
AbelLASchmidtD.Dell'OssoLFDaroffRB. Saccadic system plasticity in humans. Ann Neurol1978; 4:313–8.
12.
BahillATClarkMRStarkL.The main sequence, a tool for studying human eye movements. Math Biosciences1975; 24:191–204.
13.
BoghenDATroostBTDaroffRBDell'OssoLFBirkettJE. Velocity characteristics of normal human saccadic eye movements. Invest Ophthalmol1974; 13:619–23.
14.
TroostBTDaroffRBDell'OssoLF. Hemispheric control of eye movements. II. Quantitative analysis of smooth pursuit in a hemispherectomy patient. Arch Neurol1972; 27:449–52.
15.
BrandtTDichgansJKoenigE.Differential effect of central versus peripheral vision on egocentric and exocentric motion perception. Exp Brain Res1973; 16:476–91.
16.
RaphanTCohenBMatsuoV.A velocity-storage mechanism responsible for optokinetic nystagmus (OKN), optokinetic afternystagmus (OKAN), and vestibular nystagmus. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 37–47.
17.
SharpeJADeckH.Destruction of the internal sagittal stratum and normal smooth pursuit. Ann Neurol1978; 4:473–6.
18.
SharpeJALoAWRabinovitchHE. Control of the saccadic and smooth pursuit systems after cerebral hemidecortication. Brain1979; 102:387–403.
19.
HartjeWKerschensteinerM.A quantitative analysis of saccadic pursuit eye movements in patients with unilateral hemispheric lesions. Z Neurol1973; 203:299–310.
20.
RashbassC.The relationship between saccadic and smooth tracking eye movements. J Physiol1961; 159:326–38.
21.
NorrisH.The action of sedatives on brain stem oculomotor systems in man. Neuropharmacology1971; 10: 181–91.
22.
YasuiS.Nystagmus generation, oculomotor tracking and visual motion perception. PhD thesis, Massachusetts Institute of Technology, 1976.
23.
YasuiSYoungLR. Perceived visual motion as effective stimulus to pursuit eye movement system. Science1975; 190:906–8.
24.
YasuiSYoungLR. Eye movements during after-image tracking under sinusoidal and random vestibular stimulation. In: LennerstrandGBach-y-RitaPBasic mechanism of ocular motility and their clinical implications.New York: Pergamon Press, 1975b:509–13.
25.
CookGStarkL.Horizontal eye movements studied with the online computer. Arch Ophthalmol1966; 76:589–96.
26.
BahillATStarkL.Overlapping saccades and glissades are produced by fatigue in the saccadic eye movement system. Exp Neurol1975; 48:95–106.
27.
BahillATStarkL.The trajectories of saccadic eye movements. Sci Am1979; 240:108–17.
28.
BalohRWSillsAWKumleyWEHonrubiaV.Quantitative measurement of saccadic amplitude, duration, and velocity. Neurology1975; 25:1065–70.
BenitzJT. Eye-tracking and optokinetic tests: Diagnostic significance in peripheral and central vestibular disorders. Laryngoscope1970; 80:834–48.
31.
Von NoordenGKPreziosiTJ. Eye movement recordings in neurological disorders. Arch Ophthalmol1966; 76:162–71.
32.
CorveraJTorres-CourtneyGLopez-RiosG.The neurotological significance of alterations of pursuit eye movements and the pendular eye tracking test. Ann Otol Rhinol Laryngol1973; 82:1–13.
33.
LarmandeAMDelplaceMP. L'epreuve de poursuite pendulaire. Principe et technique. Arch Ophthalmol1973; 33:269–78.
BogaczJMendilaharsuCDe MendilaharsuSA. Electro-oculographic study of saccadic pursuit eye movements in patients with brain lesions. Electroencephalogr Clin Neurophysiol1977; 42:23–30.
FrankMCKuhloW.Die Wirkung des Alkohols auf die raschen Blickzielbewegungen (Saccaden) beim Menschen. Arch Psychiatr Nervenkr1970; 213:238–45.
38.
WilkinsonIMSKimeRPurnellM.Alcohol and human eye movement. Brain1974; 97:785–92.
39.
YamazakiA.Electrophysiological study on saccades during fixation and small smooth pursuit movement in neurological disorders. Acta Soc Ophthalmol Jpn1970; 74:244–52.
HartjeWSteinhauserDKerschensteinerM.Diagnostic value of saccadic pursuit eye movement in screening for organic cerebral dysfunction. J Neurol1978; 217:253–60.
42.
HolzmanPSProctorLRHughesDW. Eye-tracking patterns in schizophrenia. Science1973; 181:179–81.
43.
HolzmanPSLevyDLProctorLR. Smooth pursuit eye movements, attention, and schizophrenia. Arch Gen Psychiatry1976; 33:1415–20.
44.
ShagrassCRoemerRAAmadeoM.Eye-tracking performance and engagement of attention. Arch Gen Psychiatry1976; 33:121–5.
45.
TroostBTDaroffRBDell'OssoLF. Eye tracking patterns in schizophrenia. Science1974; 184:1202–3.
46.
TroostBTWeberRBDaroffRB. Hemispheric control of eye movements. I. Quantitative analysis of refixation saccades in a hemispherectomy patient. Arch Neurol1972; 27:441–8.
47.
TroostBTDaroffRB. The ocular motor defects in progressive supranuclear palsy (PSP). Ann Neurol1977; 2:397–403.
48.
BalohRWKumleyWESillsAWHonrubiaVKonradHR. Quantitative analysis of smooth pursuit eye movements. Ann Otol Rhinol Laryngol1976; 85:111–8.
49.
StarkLVossiusGYoungLR. Predictive control of eye tracking movement. Inst Radio Eng Trans Hum Factors Electron1962; 3:52–7.
50.
ShirachiDKMonkDLBlackJH. Head rotational spectral characteristics during two dimensional smooth pursuit tasks. IEEE Trans Systems, Man and Cybernetics1978; SMC-8:332–41.
51.
DallosPJJonesRW. Learning behaviour of the eye fixation control system. IEEE Trans on Automatic Control1963; AC-8:218–27.
52.
YoungLR. Pursuit eye movement – what is being pursued? In: BakerRBerthozAThe control of gaze by brainstem neurons.New York: Elsevier/North-Holland Biomedical Press, 1977: 29–36.
53.
SteinbackMJ. Pursuing the perceptual rather than the retinal stimulus. Vision Res1976; 16:1371–6.
54.
IandoloMJBahillATTroostBT. Quantitative study of human smooth pursuit tracking. Soc Neurosc Abs1978; 4:163.
55.
BahillATIandoloMJTroostBT. Smooth pursuit eye movements in response to unpredictable target waveforms. Vision Res1980; 20:923–31.
56.
KunzleH.AkertK.Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J Comp Neurol1977; 173: 147–53.
57.
OgrenMHendricksonA.Pathways between striate cortex and subcortical regions in Macaca mulatta and Saimiri sciureus: Evidence for a reciprocal pulvinar connection. Exp Neurol1976; 53:780–800.
58.
GuittonDMandlGR. The frontal eye field in cat. In: BakerRBerthozAControl of gaze by brain stem neurons.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 463–7.
59.
LynchJCMountcastleVBTalbotWHYinTCT. Parietal lobe mechanisms for directed visual attention. I. J Neurophysiol1977; 40:362–70.
60.
LynchJCMountcastleVBTalbotWHYinTCT. Parietal lobe mechanisms for directed visual attention. II. J Neurophysiol1977; 40:371–89.
61.
LynchJC. The functional organization of posterior parietal association cortex. Behav Brain Sci1980; 3:485–534.
62.
GoldbergMERobinsonDL. Visual mechanisms underlying gaze: Function of the cerebral cortex. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 469–76.
63.
BalohRWHonrubiaVSillsA.Eye-tracking and optokinetic nystagmus. Results of quantitative testing in patients with well-defined nervous system lesions. Ann Otol Rhinol Laryngol1977; 86:108–14.
64.
UpdykeBV. Topographic organization of the projections from cortical areas 17, 18, and 19 onto the thalmus, pretectum, and superior colliculus in the cat. J Comp Neurol1977; 173:81–7.
65.
UngerleiderLGChristensenCA. Pulvinar lesions in monkeys produce abnormal eye movements during visual discrimination training. Brain Res1977; 136:189–91.
66.
SchlagJSchlag-ReyM.Visuomotor properties of cells in cat thalmic internal medullary lamina. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 453–62.
67.
Schlag-ReyMSchlagJ.Visual and presaccadic neuronal activity in thalamic internal medulary lamina of cat: A study of targeting. J Neurophysiol1977; 40:156–73.
68.
GraybielAM. Organization of oculomotor pathways in the cat and rhesus monkey. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 79–88.
69.
KompfDPasikTPasikPDownward gaze in monkeys. Stimulation and lesion studies. Brain1979; 102:527–58.
70.
Van GisenbergenJAMRobinsonDA. Generation of micro- and macrosaccades by burst neurons in the monkey. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977:301–8.
71.
ButtnerUHeppKHennV.Neurons in the rostral mesencephalic and paramedian pontine reticular formation generating fast eye movements. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 309–18.
72.
KingWMFuchsAF. Neuronal activity in the mesencephalon related to vertical eye movements. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 319–26.
73.
KellerEL. Control of saccadic eye movements by midline brain stem neurons. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 327–36.
74.
FuchsAF. Role of the vestibular and reticular nuclei in the control of gaze. B: Reticular prepositus and other internuclear neuronal activity. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 341–8.
75.
RaphanTCohenB.Brainstem mechanisms for rapid and slow eye movements. Ann Rev Physiol1978; 40:527–44.
76.
AshPRKeltnerJL. Neuro-ophthalmic signs in pontine lesions. Medicine1979; 58:304–15.
77.
PedersenRATroostBT. Abnormalities of gaze in cerebrovascular disease. Stroke1981 (in press).
78.
AkagiY.The localization of the motor neurons innervating the extraocular muscles in the oculomotor nuclei of the cat and rabbit, using horseradish peroxidase. J Comp Neurol1978; 181:745–55.
79.
MaciewiczRJSpencerRF. Oculomotor and abducens internuclear pathways in the cat. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 99–108.
80.
HighsteinSM. Abducens and oculomotor internuclear neurons: Relation to gaze. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 153–62.
81.
GraybielAM. Direct and indirect preoculomotor pathways of the brainstem: An autoradiographic study of the pontine reticular formation in the cat. J Comp Neurol1977; 175:37–45.
82.
Buttner-EnneverJA. Pathways from the pontine reticular formation structures controlling horizontal and vertical eye movements in the monkey. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.Now York: Elsevier/North-Holland Biomedical Press: vol 1, 89–98.
83.
SteigerHJButtner-EnneverJ.Relationship between motoneurons and internuclear neurons in the abducens nucleus: A double retrograde tracer study in the cat. Brain Res1978; 148:181–9.
84.
KingWMLisbergerSGFuchsAF. Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli. J Neurophysiol1976; 39:1135–49.
85.
HighsteinS.Abducens to medial rectus pathway in the MLF: A possible cellular basis for the syndrome of internuclear ophthalmoplegia. In: BrooksBABahandasFJEye movements, ARVO symposium.New York: Plenum Press, 1977: 127–35.
86.
BakerRBerthozADelgado-GarciaJ.Monosynaptic excitation of trochlear motoneurons following electrical stimulation of the prepositus hypoglossi nucleus. Brain Res1977; 121:157–60.
BalohRWHonrubiaV.Clinical neurophysiology of the vestibular systems. Philadelphia: FA Davis, 1979.
89.
RobinsonDA. Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp Brain Res1977; 30:447–50.
90.
BarrCCSchultheisLWRobinsonDA. Voluntary, nonvisual control of the human vestibulo-ocular reflex. Acta Otolaryngol (Stockh)1976; 81:365–70.
91.
ZeeDS. The organization of the brainstem ocular motor subnuclei. Ann Neurol1978; 4:384.
92.
LlinasRWolfeJW. Functional linkage between the electrical activity in the vermal cerebellar cortex and saccadic eye movements. Exp Brain Res1977; 29:1–4.
93.
LisbergerSGFuchsAF. Role of the primate flocculus in smooth pursuit eye movements and rapid behavioral modification of the vestibulo-ocular reflex. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977; 381–9.
94.
AlleyK.Anatomical basis for interaction between cerebellar flocculus and brainstem. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 109–17.
95.
MackawaKTakedaT.Afferent pathways from the visual systems to the cerebellar flocculus of the rabbit. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Press: vol 1, 1977: 187–95.
96.
GonshorAMelvill JonesG.Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol1976; 256:381–92.
97.
RobinsonDA. Adaptive gain control of the vestibulo-ocular reflex by the cerebellum. J Neurophysiol1976; 39:954–65.
98.
CollewijnH.The modifiability of the adult vestibulo-ocular reflex. Trends Neurosc1979; 1:98–105.
PurkinjiJ.Beobachtungen und Versuche zur Physiologie der Sinne. Neue Beitrage zur Kenntnis des Sehens in subjectiver Hinischt. Berlin: G. Reimer, 1825; 2:60–1.
101.
BaranyR.Zur Klinik und Theorie des Eisenbahn-Nystagmus. Arch Augenheilk1921; 88:139–42.
102.
Ter BraakeJWC. Untersuchungen uber optokinetischen Nystagmus. Arch Neurol Physiol1936; 21:309–76.
103.
HoodJD. Observations upon the neurological mechanism of optokinetic nystagmus with special reference to the contribution of peripheral vision. Acta Otolaryngol (Stockh)1967; 63:208–15.
104.
HonrubiaVScottBJWardPH. Experimental studies on optokinetic nystagmus. I. Normal cats. Acta Otolaryngol (Stockh)1967; 64:388–402.
105.
HonrubiaVJenkinsHDowneyWExperimental studies on optokinetic nystagmus. III. Modifications produced by labyrinthectomy and cerebral hemidecortication in cats. Ann Otol Rhinol Laryngol1971; 80:97–110.
106.
HonrubiaVDowneyWMitchellDPExperimental studies on optokinetic nystagmus. II. Normal humans. Acta Otolaryngol (Stockh)1968; 65:441–8.
107.
DichgansJ.Optokinetic nystagmus as dependent on the retinal periphery via the vestibular nuclei. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neurosciece.New York: Elsevier/North-Holland Biomedical Press, vol 1, 1977: 261–7.
108.
CohenBMatsuoVRaphanT.Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic afternystagmus. J Physiol1977; 270:321–44.
109.
BalohRWYeeRDHonrubiaV.Optokinetic nystagmus and parietal lobe lesions. Ann Neurol1980; 7:269–76.
110.
WallaceMBlairSMWestheimerG.Neural pathways common to vestibular and optokinetic eye movements. Exp Brain Res1978; 33:19–25.
DuboisMFCollewijnH.Optokinetic reactions in man elicited by localized retinal motion stimuli. Vision Res1979; 19:1105–15.
113.
ZeeDSYeeRDRobinsonDA. Optokinetic responses in labyrinthine-defective human beings. Brain Res1976; 113:423–8.
114.
HennVYoungLRFinleyC.Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brain Res1974; 71:144–9.
115.
AllumJHJGrafWDichgansJVisual-vestibular interactions in the vestibular nuclei of goldfish. Exp Brains Res1976; 26:463–85.
116.
WaespeWHennV.Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res1977a; 27:523–39.
117.
WaespeWHennV.Vestibular nuclei activity during optokinetic after-nystagmus (OKAN) in the alert monkey. Exp Brain Res1977b; 30:323–30.
118.
RobinsonDA. Vestibular and optokinetic symbiosis: An example of explaining by modelling. In: BakerRBerthozAControl of gaze by brain stem neurons, developments in neuroscience.New York: Elsevier/North-Holland Biomedical Pres: vol 1, 1977: 49–58.
