Top

Published in:

01-09-2006 | Research Article

Brainstem and cerebellar fMRI-activation during horizontal and vertical optokinetic stimulation

Authors: Sandra Bense, Barbara Janusch, Goran Vucurevic, Thomas Bauermann, Peter Schlindwein, Thomas Brandt, Peter Stoeter, Marianne Dieterich

Published in: Experimental Brain Research | Issue 2/2006

Abstract

Animal studies have shown that not only cortical, but also brainstem and cerebellar areas are involved in the initiation and generation of optokinetic nystagmus (OKN), e.g., cortico-(pretecto)pontine-olivo-cerebellar pathways. The aim of this fMRI study was to identify and differentiate brainstem and cerebellar areas involved in horizontal and vertical OKN (h/vOKN) in humans. In a group of nine healthy volunteers, hOKN and vOKN were statistically compared with a stationary control condition. There were common activated regions for hOKN and vOKN directions located in the transition zone between the posterior thalamus and the mesencephalon bilaterally covering the pretectal nucleus complex, which is known to be a major structure within the afferent branch of the optokinetic system. Furthermore, during hOKN, activation occurred bilaterally in the mediodorsal and dorsolateral ponto-medullary brainstem, which could be best attributed to the reticular formation, especially the paramedian pontine reticular formation (PPRF). For vOKN, additional activated areas in the dorsal mesencephalic brainstem could be best localized to the ocular motor nuclei and the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). For both OKN directions, the cerebellar activation was localized in the oculomotor vermis (declive VI, folium and tuber VIIA/B, in part pyramis VIIIA), and the flocculus bilaterally as well as widespread in the cerebellar hemispheres. In conclusion, fMRI allowed first attributions of neuronal substrates in the cerebellum and brainstem to hOKN and vOKN in humans. Consistent with the animal data, the dorsal ponto-medullary routes were involved bilaterally for hOKN, whereas the rostral mesencephalic routes were involved for vOKN.

Angelaki DE, Hess BJ (1994) The cerebellar nodulus and ventral uvula control the torsional vestibulo-ocular reflex. J Neurophysiol 72:1443–1447PubMed

Angelaki DE, Hess BJ (1995) Inertial representation of angular motion in the vestibular system of the rhesus monkey. II Otolith-controlled transformation that depends on an intact cerebellar nodulus. J Neurophysiol 73:1729–1751PubMed

Barmack NH, Baugham RW, Errico P, Shojaku H (1993) Vestibular primary afferent projection to the cerebellum of the rabbit. J Comp Neurol 327:521–534PubMedCrossRef

Bense S, Janusch B, Schlindwein P, Bauermann T, Vucurevic G, Brandt T, Stoeter P, Dieterich M (2006) Direction-dependent visual cortex activation during horizontal optokinetic stimulation (fMRI study). Human Brain Mapp 27:296–305CrossRef

Boileau I, Beauregar M, Beuter A, Breault C, Lecours AR (2002) Optokinetic stimulation and the egocentred midsagittal plane: an fMRI study. Neuroreport 13:61–65PubMedCrossRef

Bucher SF, Dieterich M, Seelos KC, Brandt T (1997) Sensorimotor cerebral activation during optokinetic nystagmus. A functional MRI study. Neurology 49:1370–1377PubMed

Büttner U (1989) The role of the cerebellum in smooth pursuit eye movements and optokinetic nystagmus in primates. Rev Neurol (Paris) 145:560–566

Büttner-Ennever JA, Cohen B, Horn AKE, Reisine H (1996a) Efferent pathways of the nucleus of the optic tract in the monkey and their role in eye movements. J Comp Neurol 373:90–107CrossRef

Büttner-Ennever JA, Cohen B, Horn AKE, Reisine H (1996b) Pretectal projections to the oculomotor complex of the monkey, and their role in eye movements. J Comp Neurol 366:348–359CrossRef

Büttner-Ennever JA, Gerrits NM (eds) (2004) The vestibular system. The human nervous system, 2nd edn. Elsevier, USA, pp 1212–1240

Büttner-Ennever JA, Horn AKE (eds) (2004) Reticular formation: eye movements, gaze, and blinks. The human nervous system, 2nd edn. Elsevier, USA, pp 479–509

Carleton SC, Carpenter MB (1984) Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey. Brain Res 294:281–298PubMedCrossRef

Cohen B, Reisine H, Yokota JI, Raphan T (1992) The nucleus of the optic tract. Ann NY Acad Sci 656:277–296PubMedCrossRef

Collewijn H (1981) The oculomotor system of the rabbit and its plasticity. Springer, Berlin Heidelberg New York

Cooper HM, Baleydier C, Magnin M (1990) Macaque accessory optic system: I definition of the medial terminal nucleus. J Comp Neurol 302:294–404CrossRef

Dejardin S, Dubois S, Bodart JM, Schiltz C, Delinte A, Michel C, Roucoux A, Crommelinck M (1998) PET study in human voluntary saccadic eye movements in darkness: effect of task repetition on the activation pattern. Eur J Neurosci 10:2328–2336PubMedCrossRef

Desmurget M, Pellison D, Urquizar C, Prablanc C, Alexander GE, Grafton ST (1998) Functional anatomy of saccadic adaptation in humans. Nat Neurosci 1:524–528PubMedCrossRef

Dicke PW, Barash S, Ilg U, Thier P (2004) single-neuron evidence for a contribution of the dorsal pontine nuclei to both types of target-directed eye movements, saccades and smooth pursuit. Eur J Neurosci 19:609–624PubMedCrossRef

Dieterich M, Bucher SF, Seelos KC, Brandt T (1998) Horizontal or vertical optokinetic stimulation activates visual motion-sensitive, ocular motor and vestibular cortex areas with right hemispheric dominance. An fMRI study. Brain 121:1479–1495PubMedCrossRef

Dieterich M, Bucher SF, Seelos KC, Brandt T (2000) Cerebellar activation during optokinetic stimulation and saccades. Neurology 54:148–155PubMed

Dieterich M, Bense S, Stephan T, Yousry TA, Brandt T (2003) FMRI cortical increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation. Exp Brain Res 148:117–127PubMedCrossRef

Duvernoy HM (1995) The human brain stem and cerebellum. Surface, structure, vascularization, and three-dimensional sectional anatomy with MRI. Springer, Wien, New York

Frison L, Popcock S (1992) Repeated measures in clinical trials: analysis using mean summary statistics and its implications for design. Stat Med 11:1685–1704PubMedCrossRef

Friston KJ, Asburner J, Frith CD, Poline JB, Heather JD, Frackowiak RSJ (1995a) Spatial registration and normalization of images. Hum Brain Mapp 2:165–189CrossRef

Friston KJ, Holms AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ (1995b) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRef

Galati G, Pappata S, Pantano P, Lenzi GL, Samson Y, Pizzamiglio L (1999) Cortical control of optokinetic nystagmus in humans: a positron emission tomography study. Exp Brain Res 126:149–159PubMedCrossRef

Giolli RA (1963) An experimental study of the accessory optic system in the cynomologus monkey. J Comp Neurol 121:89–107PubMedCrossRef

Glasauer S, Hoshi M, Kempermann U, Eggert T, Büttner U (2003) Three-dimensional eye position and slow phase velocity in humans with downbeat nystagmus. J Neurophysiol 89:338–354PubMedCrossRef

Hayakawa Y, Nakajima T, Takagi M, Fukuhara N, Abe H (2002) Human cerebellar activation in relation to saccadic eye movements: a functional magnetic resonance imaging study. Ophthalmologica 216:399–405PubMedCrossRef

Heinen SJ, Keller EL (1996) The function of the cerebellar uvula in monkey during optokinetic and smooth pursuit eye movements: single-unit responses and lesion effects. Exp Brain Res 110:1–14PubMedCrossRef

Helmchen CH, Büttner U (1995) Saccade-related Purkinje cell activity in the oculomotor vermis during spontaneous eye movements in light and darkness. Exp Brain Res 103:198–208PubMedCrossRef

Hoffmann KP (1988) Responses of single neurons in the pretectum of monkeys to visual stimuli in the three-dimensional space. Ann NY Acad Sci 545:180–186PubMedCrossRef

Hoffmann KP, Distler C, Erickson R, Mader W (1988). Physiological and anatomical identification of the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in monkeys. Exp Brain Res 69:635–644PubMedCrossRef

Hoffmann KP, Fischer WH (2001) Directional effect of inactivation of the nucleus of the optic tract on optokinetic nystagmus in the cat. Vision Res 41:3389–3398PubMedCrossRef

Ilg UJ (1997) Slow eye movements. Prog Neurobiol 53:293–329PubMedCrossRef

Ilg UJ, Koffmann KP (1996) Responses of neurons of the nucleus of the optic tract and the dorsal terminal nucleus of the accessory optic tract in the awake monkey. Eur J Neurosci 8:92–105PubMedCrossRef

Kato I, Harada K, Hasegawa T, Igarashi T, Koike Y, Kawasaki T (1986) Role of the nucleus of the optic tract in monkeys in relation to optokinetic nystagmus. Brain Res 365:12–22CrossRef

Kato I, Harada K, Hasegawa T, Ikarashi T (1988) The role of the nucleus of the optic tract of monkey optokinetic nystagmus and after-nystagmus. Brain Res 474:16–26PubMedCrossRef

Kawano K, Shidara M, Yamane S (1992) Neural activity in the dorsolateral pontine nucleus of alert monkey during ocular following responses. J Neurophysiol 67:680–703PubMed

Konen CS, Kaiser R, Seitz RJ, Bremmer F (2005) An fMRI study of optokinetic nystagmus and smooth pursuit eye movements in humans. Exp Brain Res 165:203–216PubMedCrossRef

Leigh RJ, Kennard C (2004) Using saccades as a research tool in the clinical neurosciences. Brain 127:460–477PubMedCrossRef

Leigh RJ, Zee DS (eds) (1999) The neurology of eye movements, 3rd edn. Oxford University Press, New York, pp 19–89

Lisberger SG, Miles FA, Zee DS (1984) Signals used to compute errors in monkey vestibuloocular reflex: a possible role of the flocculus. J Neurophysiol 52:1140–1153PubMed

Magnin M, Kennedy H, Hoffmann KP (1990) A double-labeling investigation of the pretectal visuo-vestibular pathways. Vis Neurosci 3:53–58CrossRef

Markert G, Büttner U, Straube A, Boyle R (1988) Neuronal activity in the flocculus of the alert monkey during sinusoidal optokinetic stimulation. Exp Brain Res 70:134–144PubMed

Mustari MJ, Fuchs AF (1989) Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate. J Neurophysiol 61:1207–1220PubMed

Mustari MJ, Fuchs AF (1990) Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. J Neurophysiol 64:77–90PubMed

Mustari MJ, Fuchs AF, Kaneko CRS, Robinson RF (1994) Anatomical connections of the primate pretectal nucleus of the optic tract. J Comp Neurol 349:111–128PubMedCrossRef

Naito Y, Tateya I, Hirano S, Inoue M, Funabiki K, Toyoda H, Ueno M, Ishizu K, Nagahama Y, Fukuyama H, Ito J (2003) Cortical correlates of vestibulo-ocular reflex modulation: a PET study. Brain 126:1562–1578PubMedCrossRef

Nitschke MF, Binkofski F, Buccino G, Posse S, Erdmann C, Kömpf D, Seitz RJ, Heide W (2004) Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: an fMRI study. Hum Brain Mapp 22:155–164PubMedCrossRef

Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRef

Precht W, Simpson JI, Llinas R (1976) Responses of Purkinje cells in rabbit nodulus and uvula to natural vestibular and visual stimuli. Pflugers Arch 367:1–6PubMedCrossRef

Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG (2002) Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J Neurophysiol 87:912–924PubMed

Salmaso D, Longoni AM (1985) Problems in the assessment of hand preference. Cortex 21:533–549PubMed

Schaltenbrandt G, Wahren W (1977) Atlas for Stereotaxy of the Human brain. Georg Thieme Verlag, Stuttgart

Schiff D, Cohen B, Büttner-Ennever J, Matsuo V (1990) Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey. Exp Brain Res 79:225–239PubMedCrossRef

Schiff D, Cohen B, Raphan T (1988) Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Exp Brain Res 70:1–14PubMed

Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI atlas of the human cerebellum. Academic Press, San Diego

Simpson JI, Soodak RE, Hess R (1979) The accessory optic system and its relation to the vestibulocerebellum. Prog Brain Res 50:715–724PubMedCrossRef

Simpson JI. Giollo RA, Blanks RHI (1988) The pretectal nuclear complex and the accessory optic system. In: Büttner-Ennever JA (eds) Neuroanatomy of the ocular motor system. Elsevier Science Publisher BV (Biomedical Division), Amsterdam, pp 335–364

Stephan T, Mascolo A, Yousry TA, Bense S, Brandt T, Dieterich M (2002) Changes in cerebellar activation pattern during two successive sequences of saccades. Hum Brain Mapp 16:63–70PubMedCrossRef

Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, Dieterich M (2005) Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. NeuroImage 26:721–732PubMedCrossRef

Suzuki DA, Keller EL (1988) The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. I. Eye and head-movement-related activity. J Neurophysiol 59:1–18PubMed

Takeda T, Maekawa K (1989) Olivary projections to the flocculus, nodulus and uvula in the rabbit. I. An electrophysiological study. Exp Brain Res 74:47–62PubMedCrossRef

Talairach J, Tournoux P (1988) Co-Planar stereotaxic atlas of the human brain, Thieme, Stuttgart

Tanabe J, Tregellas J, Miller D, Ross RG, Freedmann R (2002) Brain activation during smooth pursuit. NeuroImage 17:1315–1324PubMedCrossRef

Walley RE (1967) Receptive fields in the accessory optic system of the rabbit. Exp Neurol 17:27–43PubMedCrossRef

Woods RP (1996) Modeling for intergroup comparisons of imaging data. NeuroImage 4:84–94CrossRef

Wylie DR, De Zweeuw CI, Di Giori PL, Simpson JI (1994) Projections of individual cell of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol 349:448–463PubMedCrossRef

Yakushin S, Gizzi M, Reisine H, Cohen B (1994) Lesion of the nucleus of the optic tract (NOT) impair smooth pursuit. Soc Neurosci Abstr 20:772

Zee DS, Yamazaki A, Butler PH (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol 46:878–899PubMed

Title: Brainstem and cerebellar fMRI-activation during horizontal and vertical optokinetic stimulation
Authors: Sandra Bense
Barbara Janusch
Goran Vucurevic
Thomas Bauermann
Peter Schlindwein
Thomas Brandt
Peter Stoeter
Marianne Dieterich
Publication date: 01-09-2006
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 2/2006
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-006-0464-0

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Brainstem and cerebellar fMRI-activation during horizontal and vertical optokinetic stimulation

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2006

The coalition of constraints during coordination of the ipsilateral and heterolateral limbs

Threshold control of motor actions prevents destabilizing effects of proprioceptive delays

Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability

Changing plans: neural correlates of executive control in monkey and human frontal cortex

The mirror antisaccade task: direction–amplitude interaction and spatial accuracy characteristics

Activation of α2-adrenoreceptors suppresses the excitability of C1 spinal neurons having convergent inputs from tooth pulp and superior sagittal sinus in rats