Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: An fMRI study

What mechanisms allow us to direct a precise saccade to a remembered target position in space? The cerebellum has been proposed to be involved not only in motor and oculomotor control, but also in perceptual and cognitive functions. We used functional MRI (Echoplanar imaging at 1.5 T) to investigate the role of the cerebellum in the control of externally triggered and internally generated saccadic eye movements of high and low memory impact, in six healthy volunteers. Memory‐guided saccades to remembered locations of 3 targets (triple‐step saccades) in contrast to either central fixation or to visually guided saccades activated the cerebellar hemispheres predominantly within lobuli VI‐crus I. The same areas were activated when an analogous visuospatial working memory task was contrasted to the triple‐step saccades. Visually guided saccades activated the posterior vermis and the triple‐step saccades, contrasted to the working memory task, activated predominantly the posterior vermis and paravermal regions. Our data confirm the primary involvement of the posterior vermis for visually‐triggered saccadic eye movements and present novel evidence for a role of the cerebellar hemispheres in the mnemonic and visuospatial control of memory‐guided saccades. Hum. Brain Mapp. 22:155–164, 2004. © 2004 Wiley‐Liss, Inc.

[1]  P E Roland,et al.  Metabolic mapping of sensorimotor integration in the human brain. , 1987, Ciba Foundation symposium.

[2]  Nick Fogt,et al.  The Neurology of Eye Movements, 3rd ed. , 2000 .

[3]  D. Pandya,et al.  Anatomic Organization of the Basilar Pontine Projections from Prefrontal Cortices in Rhesus Monkey , 1997, The Journal of Neuroscience.

[4]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[5]  M Westerfield,et al.  Spatial Attention Deficits in Patients with Acquired or Developmental Cerebellar Abnormality , 1999, The Journal of Neuroscience.

[6]  H. Deubel,et al.  Current Oculomotor Research , 1999, Springer US.

[7]  C. Svarer,et al.  Parieto-occipital cortex activation during self-generated eye movements in the dark. , 1998, Brain : a journal of neurology.

[8]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[9]  K Ugurbil,et al.  Activation of visuomotor systems during visually guided movements: a functional MRI study. , 1998, Journal of magnetic resonance.

[10]  A. L. Leiner,et al.  Cognitive and language functions of the human cerebellum , 1993, Trends in Neurosciences.

[11]  Massimo Pandolfo,et al.  The Cerebellum and its Disorders: SPORADIC DISEASES , 2001 .

[12]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[13]  H. Deubel,et al.  Differential Effect of a Bilateral Deep Cerebellar Nuclei Lesion on Externally and Internally Triggered Saccades in Humans , 1995 .

[14]  Karl J. Friston,et al.  Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  J V Haxby,et al.  Dissociation of saccade-related and pursuit-related activation in human frontal eye fields as revealed by fMRI. , 1997, Journal of neurophysiology.

[16]  M. Takagi,et al.  Human Cerebellar Activation in Relation to Saccadic Eye Movements: A Functional Magnetic Resonance Imaging Study , 2002, Ophthalmologica.

[17]  H. Noda,et al.  Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation , 1980, The Journal of physiology.

[18]  D. A. Suzuki,et al.  The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity. , 1988, Journal of neurophysiology.

[19]  K. Ohtsuka,et al.  Discharge properties of Purkinje cells in the oculomotor vermis during visually guided saccades in the macaque monkey. , 1995, Journal of neurophysiology.

[20]  C. Michel,et al.  PET study of human voluntary saccadic eye movements in darkness: effect of task repetition on the activation pattern , 1998, The European journal of neuroscience.

[21]  P. Strick,et al.  Dentate output channels: motor and cognitive components. , 1997, Progress in brain research.

[22]  P. Thier,et al.  Encoding of movement time by populations of cerebellar Purkinje cells , 2000, Nature.

[23]  S. Mann,et al.  Ciba Foundation Symposium , 1997 .

[24]  W. T. Thach Motor Learning and Synaptic Plasticity in the Cerebellum: On the specific role of the cerebellum in motor learning and cognition: Clues from PET activation and lesion studies in man , 1997 .

[25]  M Dieterich,et al.  Cerebellar activation during optokinetic stimulation and saccades , 2000, Neurology.

[26]  J. Harbison,et al.  The Neurology of Eye Movements, 3rd ed , 2000 .

[27]  Emile Godaux,et al.  The Cerebellum and its Disorders: Neuroanatomy of the cerebellum , 2001 .

[28]  M. Mintun,et al.  Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. , 1996, Journal of neurophysiology.

[29]  Jan G. Bjaalie,et al.  Organization of the pontine nuclei , 1992, Neuroscience Research.

[30]  P. Thier,et al.  Absence of a common functional denominator of visual disturbances in cerebellar disease. , 1999, Brain : a journal of neurology.

[31]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[32]  U. Büttner Eye Movement Deficits in Cerebellar Disease , 1999 .

[33]  B. Cohen,et al.  Changes in saccadic eye movements produced by cerebellar cortical lesions. , 1971, Experimental neurology.

[34]  R. Passingham,et al.  The cerebellum and cognition: cerebellar lesions do not impair spatial working memory or visual associative learning in monkeys , 1999, The European journal of neuroscience.

[35]  P. Thier,et al.  Saccadic Dysmetria and Adaptation after Lesions of the Cerebellar Cortex , 1999, The Journal of Neuroscience.

[36]  A. Straube,et al.  The Effect of Cerebellar Midline Lesions on Eye Movements , 1995 .

[37]  N. Minshew,et al.  Neocortical system abnormalities in autism: An fMRI study of spatial working memory , 2002, Neurology.

[38]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

[39]  S. Stone-Elander,et al.  Motor learning in man: a positron emission tomographic study. , 1990, Neuroreport.

[40]  P. Strick,et al.  Chapter 32 Dentate output channels: motor and cognitive components , 1997 .

[41]  Scott T. Grafton,et al.  Genetic dissection of Alzheimer's disease and related dementias: amyloid and its relationship to tau , 1998, Nature Neuroscience.

[42]  H. Deubel Separate adaptive mechanisms for the control of reactive and volitional saccadic eye movements , 1995, Vision Research.

[43]  M. Raichle,et al.  The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. , 1985, Journal of neurophysiology.

[44]  J P Donoghue,et al.  Motor Areas of the Cerebral Cortex , 1994, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[45]  P. Strick,et al.  Activation of a cerebellar output nucleus during cognitive processing. , 1994, Science.

[46]  R. J. Seitz,et al.  Activation of frontoparietal cortices during memorized triple‐step sequences of saccadic eye movements: an fMRI study , 2001, The European journal of neuroscience.

[47]  Thomas Stephan,et al.  Changes in cerebellar activation pattern during two successive sequences of saccades , 2002, Human brain mapping.

[48]  T. Mergner,et al.  Relationship between saccadic eye movements and cortical activity as measured by fMRI: quantitative and qualitative aspects , 2001, Experimental Brain Research.

[49]  Alan C. Evans,et al.  Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space , 1999, NeuroImage.

[50]  N. Shimizu [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[51]  J. Bower,et al.  Cerebellum Implicated in Sensory Acquisition and Discrimination Rather Than Motor Control , 1996, Science.

[52]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. I. Neuronal discharge pattern. , 1993, Journal of neurophysiology.

[53]  U. Büttner,et al.  Saccade-related Purkinje cell activity in the oculomotor vermis during spontaneous eye movements in light and darkness , 2004, Experimental Brain Research.

[54]  W. Heide,et al.  Cortical control of double‐step saccades: Implications for spatial orientation , 1995, Annals of neurology.