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How the Brain Moves Your Eyes About C. Casanova and M. Ptito (Eds.) Progress in Brain Research, Vol. 134 2001 Elsevier Science B.V. All rights reserved CHAPTER 9 Look and see: how the brain moves your eyes about Peter H. Schiller Ł and Edward J. Tehovnik Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA Abstract: Two major cortical streams are involved in the generation of visually guided saccadic eye movements: the anterior and the posterior. The anterior stream from the frontal and medial eye fields has direct access to brainstem oculomotor centers. The posterior stream from the occipital cortices reaches brainstem oculomotor centers through the superior colliculus. The parietal cortex interconnects with both streams. Our findings suggest that the posterior stream plays an unique role in the execution of rapid, short latency eye movements called ‘express saccades’. Both the anterior and posterior streams play a role in the selection of targets to which saccades are to be generated, but do so in different ways. Areas V1, V2 and LIP contribute to decisions involved in where to look as well as where not to look. In addition, area LIP is involved in decisions about how long to maintain fixation prior to the execution of a saccade. Area V4 does not appear to be directly involved in eye-movement generation. In the anterior stream, the frontal eye fields, and to a lesser extent the medial eye fields, are involved in the correct execution of saccades subsequent to decisions made about where to look and where not to look. Introduction studied quite a number of brain areas that include V1, V2, V4, the lateral intraparietal sulcus (LIP), the Our eyes are on the move most of the time during frontal eye fields (FEF), the medial eye fields (MEF), our waking hours. We make about three saccadic and the superior colliculus (SC). eye movements per second, some 170,000 a day, These were carried out on trained rhesus monkeys and about 5 billion in an average life time. With because their eye movements are similar to those each shift in gaze, the numerous stimuli in the vi- of humans. Fig. 1 shows records of eye movements sual scene impinge on new retinal locations, to only made by one of our animals while he was restrained one of which can the eye be shifted subsequently. and looked at the displays shown on the left. The This process of target selection necessitates the dis- monkey received periodic juice reward. The eye crimination of objects, the assessment of temporal movements are similar to those generated by humans order and the determination of spatial location. In as shown by Yarbus (1967). this presentation, some of the neural systems that are involved in the generation of visually guided sac- Neural structures involved in the generation of cadic eye movements are described. We have used saccadic eye movements several methods in our effort that include single-cell recordings, lesions and microstimulation. We have The exploration of the neural mechanisms of visually guided saccade generation is begun by demonstrat- ing, schematically, the central structures from which Ł Corresponding author: P.H. Schiller, Department of saccadic eye movements can be elicited by electrical Brain and Cognitive Sciences, Massachusetts Institute of microstimulation. As shown in Fig. 2, such saccades Technology, Cambridge, MA 02139, USA. can be elicited from quite a number of brain areas Tel.: C1-617-253-5754; Fax: C1-617-253-8943; at relatively low currents. As indicated by the arrows E-mail: [email protected] in the circles, stimulation of regions of the occipital CICERO/GALAYAA B.V. / CASANOVA 9: pp. 1-16 2 Fig. 1. Saccadic eye movements of a monkey, shown in the right panels, while the animal was viewing the stimulus displays shown on the left. cortex, such as V1 and V2, elicits saccades whose A different coding operation takes place in the me- vectors are constant, and are independent of starting dial eye fields where stimulation elicits a saccade eye position (Schiller, 1972, 1977, 1998). The vector that takes at the center of gaze to a particular lo- and amplitude of the saccade elicited depends on cation in craniotopic space (Schlag and Schlag-Rey, where one stimulates within the structure. When one 1987; Tehovnik and Lee, 1993). Different subregions records as well and finds the location of the recep- code for different spatial locations. In the parietal tive fields, stimulation takes the eye to the receptive lobe, in different subregions one can find either one field location prior to the eye movement. These areas or the other of these coding operations (Shibutani therefore carry a vector code. What is computed is et al., 1984; Kurylo and Skavenski, 1991; Thier and a retinal error signal between the center of gaze and Andersen, 1998). the location of the receptive field activated by the Although it was thought that cortical signals for target; the eye movement nulls this error. Like visual the generation of saccadic eye movements are con- cortex, the superior colliculus and the frontal eye veyed entirely through the superior colliculus, more fields also carry a vector code (Robinson and Fuchs, recent evidence indicates that this is not the case. 1969; Robinson, 1972; Schiller and Stryker, 1972). When the colliculus is removed, monkeys still make CICERO/GALAYAA B.V. / CASANOVA 9: pp. 1-16 3 Fig. 2. Eye movements elicited by electrical stimulation of five areas. Stimulation of the superior colliculus, the visual cortex, regions of the parietal cortex, and the frontal eye fields produces saccades whose amplitude and direction depends on the subregion stimulated in each of these areas. Stimulation of the medial eye fields and some regions of the parietal cortex elicits saccades that take the eye to a particular orbital location. pretty good visually guided eye movements (Schiller cortex and the colliculus (Lynch et al., 1985; Huerta et al., 1980; Keating and Gooley, 1988a). Further et al., 1987; Huerta and Kaas, 1990), there is one work established that collicular removal has a se- important additional piece of information in support lective effect on electrically triggered saccadic eye of the two-stream hypothesis depicted in Fig. 4. This movements from the cortex. What happens is de- additional evidence is that ablation of both the su- picted in Fig. 3. After ablation of the superior perior colliculus and the frontal eye fields eliminates colliculus, one can still elicit saccadic eye move- all visually guided saccadic eye movements (Schiller ments from the frontal and medial eye fields, but not et al., 1980). This is a deficit from which there is from posterior cortex (Schiller, 1977; Keating et al., virtually no recovery. 1983; Keating and Gooley, 1988b; Tehovnik et al., Given that there are quite a number of cortical 1994). areas involved in visually guided saccadic eye-move- These findings have led to the formulation de- ment control that appear form two major streams to picted in Fig. 4. According to this generalized the brainstem oculomotor centers, the question arises scheme, there are two major streams for the gen- as to what the functional contributions are of the eration of visually guided saccadic eye movements, cortical areas within each of these two streams. To the anterior and the posterior. The posterior stream address this question, in our recent work, we have gains access to the brainstem oculomotor centers concentrated on two methods. The first method ex- through the superior colliculus whereas the anterior amined the effects of selective lesions on the genera- stream from the frontal and medial eye fields has di- tion of visually guided saccadic eye movements. The rect connections to the brainstem. Although cortical second method examined the effects subthreshold areas are extensively interconnected, and the region electrical microstimulation in various cortical areas of the parietal cortex that resides in the lateral intra- on target selection and the execution of saccadic eye parietal sulcus has connections both with the frontal movements. CICERO/GALAYAA B.V. / CASANOVA 9: pp. 1-16 4 Fig. 3. After ablation of the superior colliculus, electrical stimulation no longer elicits saccadic eye movements from the occipital and parietal cortices, but continues to do so in the frontal lobe. Fig. 4. Model of the hypothesized connections involved in visually guided eye-movement control. Two major streams control these eye movements: the anterior and the posterior. The anterior system has direct access to the brainstem oculomotor centers. The posterior stream reaches these centers through the superior colliculus. Lesion studies streams contribute to different aspects of eye-move- ment generation. To block the posterior stream we The aim of our lesion studies was to determine removed the superior colliculus. We then compared how the structures within the anterior and posterior that with lesions of the frontal and medial eye fields. CICERO/GALAYAA B.V. / CASANOVA 9: pp. 1-16 5 The first task to be discussed is depicted in Fig. 5. Next we turn to a different task depicted in Fig. 7, When a central fixation spot comes on, the monkey which we refer to as the sequential task. In this looks at it. Then a single target appears somewhere case, we present two targets in succession and the on the monitor and the monkey has to look at it monkey’s task is to make a corresponding pair of to receive a drop of apple juice for reward. When saccades. The task is shown in Fig. 7. The dura- a monkey performs this task repeatedly, the latency tion of the targets and the interval between them distribution becomes bimodal as first shown by Fis- is systematically varied. We studied performance on cher and Boch (1983).
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