PHYSIOLOGICAL REVIEWS Vol 80 No 3 July 2000 Printed in U S A Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements OKIHIDE HIKOSAKA YORIKO TAKIKAWA AND REIKO KAWAGOE Department of Physiology Juntendo University School of Medicine Tokyo Japan I Introduction II Concept of the Basal Ganglia III General Scheme of Saccadic Eye Movement A Hierarchy of oculomotor mechanisms B Superior colliculus a key station for saccade control IV Mechanisms of the Basal Ganglia Disinhibition A Visuo oculomotor activities in the substantia nigra pars reticulata B Substantia nigra pars reticulata superior colliculus projection and its experimental manipulation C Caudate nucleus as an input station in the basal ganglia D Visuo oculomotor activities in the caudate nucleus E Caudate nucleus substantia nigra pars reticulata projection F Disinhibition a key feature of basal ganglia function G Reversible blockade of substantia nigra pars reticulata V Mechanisms of the Basal Ganglia Enhancement of Inhibition A Subthalamic nucleus as a mechanism for motor suppression B Neural activity in the subthalamic nucleus C Globus pallidus external segment as a mediator for enhancement of inhibition D Neural activity in the globus pallidus external segment E Focusing and sequencing of basal ganglia signals VI Mechanisms of the Basal Ganglia Role of Dopamine VII Context Dependency of Neural Activity in the Basal Ganglia A Relation to attention B Relation to working memory C Relation to expectation D Relation to sequential procedural learning VIII Reinforcement A Key Factor for Decision Making in the Basal Ganglia A Experimental approach to motivation and oculomotor action B Modulation of caudate nucleus neural activity by expectation of reward C Possible role of dopamine neurons D Scheme of reinforcement learning IX Clinical Application X Conclusions 954 954 955 955 957 957 958 958 958 959 959 959 960 960 961 961 962 962 962 963 964 964 964 965 965 966 966 967 967 968 969 970 Hikosaka Okihide Yoriko Takikawa and Reiko Kawagoe Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements Physiol Rev 80 953 978 2000 In addition to their well known role in skeletal movements the basal ganglia control saccadic eye movements saccades by means of their connection to the superior colliculus SC The SC receives convergent inputs from cerebral cortical areas and the basal ganglia To make a saccade to an object purposefully appropriate signals must be selected out of the cortical inputs in which the basal ganglia play a crucial role This is done by the sustained inhibitory input from the substantia nigra pars reticulata SNr to the SC This inhibition can be removed by another inhibition from the caudate nucleus CD to the SNr which results in a disinhibition of the SC The basal ganglia have another mechanism involving the external segment of the globus pallidus and the subthalamic nucleus with which the SNr SC inhibition can further be enhanced The sensorimotor signals carried by the basal ganglia neurons are strongly modulated depending on the behavioral context which reflects working memory expectation and attention Expectation of reward is a critical determinant in that the saccade that has been rewarded is facilitated subsequently The interaction between cortical and dopaminergic inputs to CD neurons may underlie the behavioral adaptation toward purposeful saccades www physrev physiology org 0031 9333 00 15 00 Copyright 2000 the American Physiological Society 953 954 HIKOSAKA TAKIKAWA AND KAWAGOE I INTRODUCTION Animals lacking the striatum always display a certain fatuous expressionless facies from which the eyes stare vacantly and with morbid intentness Mettler 212 Patients with basal ganglia disorders suffer from excessive or retarded movements of the trunk arms or legs Such movement deficits are so disabling that deficits in eye movements if present may remain unnoticed during clinical tests Notably however one of the diagnostic signs of Parkinson s disease is the expressionless face often called parkinsonian mask 283 which is due partly to the paucity of spontaneous gaze shifts saccadic eye movements Parkinsonian patients may make a saccade on command to a visual object with little difficulty yet their voluntary saccades are rare These facts suggest that the basal ganglia are involved in the control of saccades but in an intricate manner Recent studies on trained animals and humans have suggested that the basal ganglia are related to both initiation and suppression of saccades in complex behavioral contexts which we summarize in this review Clinical studies have indicated that smooth pursuit is also impaired in basal ganglia disorders 75 326 However because to our knowledge there has been no study that suggests how the basal ganglia contribute to the control of smooth pursuit we do not make further comments on this issue This article may be divided roughly into three parts First we introduce you to the present topic by speculating how the basal ganglia evolved to control spatial orienting sects II and III In the second part we summarize the experimental evidence for the specific relation of the basal ganglia to saccadic eye movement sects IV VI The second part will hopefully be continued into the third part smoothly where we describe the results of recent studies on cognitive or motivational aspects of motor control sects VII and VIII The issues dealt with in the third part are not limited to the control of eye movement but are of more global importance for brain function in general II CONCEPT OF THE BASAL GANGLIA The basal ganglia are considered to be necessary for voluntary control of body movements 53 This idea is derived mainly from the clinical observations that lesions in the basal ganglia lead to movement disorders ranging from the inability to initiate a movement to the inability to suppress involuntary movements Anatomically the basal ganglia are the aggregate of nerve cell nuclei located at the base of the cerebrum 39 Although there are differ Volume 80 ent opinions on the definition 106 the basal ganglia as a functional entity are composed of the caudate nucleus CD and putamen PUT collectively called striatum globus pallidus substantia nigra and subthalamic nucleus STN 1 The globus pallidus is further divided into the external segment GPe and the internal segment GPi the substantia nigra is divided into the pars reticulata SNr and pars compacta SNc The CD and PUT are the two
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