1998 Special IssueNeural mechanisms of selection and control of visually guided eye movements
Introduction
Eye movements are necessary for vision. While this is true for all sighted creatures, it is especially so for primates that possess a focus of high acuity vision called the fovea. Vision is accomplished through an unceasing cycle of fixations and gaze shifts because it is necessary to direct the focus of gaze on different parts of a complex real-world image because visual acuity declines rapidly with increasing distance from the fovea. As a matter of fact, primates make more than 100 000 eye movements every day.
Fig. 1 illustrates the pattern of eye movements made by a monkey searching for a randomly oriented T among randomly oriented Ls. The rapid shifts of gaze from one object to another are called saccades. Saccades tend to direct gaze to conspicuous, informative elements in the image. If subjects are looking for a particular object, then gaze focuses primarily on appropriate elements in the image; otherwise, gaze is dispersed (e.g. Yarbus, 1967, Viviani, 1990). Recent studies in which eye, head and hand movements are recorded while subjects perform simple tasks have shown systematic relationships between gaze behavior and information acquisition for visually guided behavior (e.g. Ballard et al., 1995). Behavior of this sort indicates that before each saccade the brain selects the target for the eye movement. Deciding where to look represents the outcome of visual processing and cognitive guidance. The neural systems responsible for visual processing have been described (Colby and Duhamel, 1991, Merigan and Maunsell, 1993), as have neural correlates of visual perception (Parker and Newsome, 1998) and attention (Desimone and Duncan, 1995, Maunsell, 1995, Schall, 1995, Schall and Bichot, 1998). In the first half of this review, we will discuss the new evidence from our laboratory on neural correlates of saccade target selection in frontal eye field.
During each saccadic eye movement vision is in essence shut down. The reader can be convinced of this by looking in a mirror and shifting gaze from one eye to the other and back again. One will find it effectively impossible to see one's own saccadic eye movements. This saccadic suppression is due in part to image motion and masking effects, but active neural processes play some role (reviewed by Matin (1974)). The influence of saccadic suppression begins as much as 100 ms before and lasts as long as 100 ms after a saccade. So while we must move our eyes to see, if we move them too much, we will be effectively blind. The balance between gaze holding and gaze shifting requires a brain system to regulate the production of eye movements over time. Deciding when to shift gaze is the province of the oculomotor system (Wurtz and Goldberg, 1989, Carpenter, 1991). In the second half of this review, we will discuss new insights into how cortical neural processes regulate the initiation of eye movements.
Why investigate eye movements? Will what is learned about the perceptual and motor decisions associated with visually guided saccades be applicable to other sensory systems and the skeletal motor system? We believe that the knowledge gained about the high level control of eye movements will indeed provide more general insights. In fact, the study of the production of visually guided eye movements provides a number of advantages. In terms of kinematics, the rotation of the eye in Listing's plane is much simpler than movement of multijointed limbs with many degrees of freedom. In terms of dynamics, movements of the eyes floating nimbly in the orbits do not entail the complex torques that occur with limb movements. Moreover, the questions we will address about target selection and the control of movement involve processes that probably generalize across motor systems. In fact, a number of lines of behavioral evidence indicate that the high level control of gaze operates according to similar principles as the high level control of limb movements or speech. For example, when asked to generate a sequence of saccades, the latency of the first saccade increases with the number of movements in the sequence (Zingale and Kowler, 1987) following the same pattern observed for speech and typing (Sternberg et al., 1978). This is just one example among many which demonstrates that the high-level programming and behavioral control of eye movements seems indistinguishable from that of manual movements or even speech.
Section snippets
Frontal eye field (FEF)
The FEF is an area in the prefrontal cortex, located in the rostral bank of the arcuate sulcus of macaques. Broadly considered, this cortical area participates in the transformation of visual signals into saccade motor commands (reviewed by Schall (1997)). As illustrated in Fig. 2, the FEF is innervated in a topographic fashion by areas in both the dorsal and ventral streams of extrastriate visual cortex (e.g. Schall et al., 1995b). The part of the FEF that is responsible for generating short
Target selection in the FEF
To investigate how the brain selects the target for an eye movement, a choice must be provided. This can be accomplished by presenting more than one stimulus at a time, with one being visually distinct from the others. For many years, visual selection and attention in humans have been investigated using the visual search paradigm (reviewed by Treisman (1988)and Egeth and Yantis (1997)). Macaque monkeys also will learn very quickly to direct gaze to the oddball stimulus among similar
Rise to threshold mechanism for reaction time
Over the years many models have been developed to explain the stochastic variability of reaction time (reviewed by Luce (1986)). Most reaction time models incorporate assumptions that are not physiologically plausible, because such was not their aim. One class of models, though, known as accumulator models, does seem appropriate for evaluation in relation to brain function. Accumulator models suppose that in response to a stimulus, a signal in the brain grows until it reaches a threshold,
Conclusion
We have described neural processes that are involved in selecting the target for an eye movement and controlling whether and when the eye movement will be produced. We have also described neural signals that may serve to monitor performance. We expect that the brain signals and processes we have reviewed may provide insights into computational principles that will be useful for non-biological animate systems.
Acknowledgements
We thank N. Bichot and K. Thompson for their contributions to this work. Our research has been supported by NIH grants R01-MH55806, F31-MH11178, R01-EY08890, P30-EY08126. JDS is a Kennedy Center Investigator.
References (97)
- et al.
An analysis of the saccadic system by means of double step stimuli
Vision Res.
(1979) - et al.
Modeling the role of parallel processing in visual search
Cog. Psychol.
(1990) - et al.
Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey
Neuropsychologia
(1991) - et al.
Saccade target selection and object recognition: evidence for a common attentional mechanism
Vision Res.
(1996) - et al.
The role of attention in the programming of saccades
Vision Res.
(1995) - et al.
Effect of mean reaction time on saccadic responses to two-step stimuli with horizontal and vertical components
Vis. Res.
(1975) - et al.
Modern mental chronometry
Biol. Psychol.
(1988) - et al.
Visual receptive fields of frontal eye field neurons
Brain Res.
(1973) - et al.
Neural correlates of visual and motor decision processes
Curr. Opin. Neurobiol.
(1998) Dopamine neurons and their role in reward mechanisms
Curr. Opin. Neurobiol.
(1997)
The discovery of processing stages: extensions of Donders' method
Acta Psychologica
Linking propositions
Vision Res.
Planning sequences of saccades
Vision Res.
Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local–global comparisons of visual motion
Annu. Rev. Neurosci.
Overriding stimulus-driven attentional capture
Percept. Psychophys.
Memory representations in natural tasks
J. Cogn. Neurosci.
Visual feature selectivity in frontal eye fields induced by experience in mature macaques
Nature
Primate frontal eye fields. I. Single neurons discharging before saccades
J. Neurophysiol.
Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements
J. Neurophysiol.
Neural computation of log likelihood in the control of saccadic eye movements
Nature
A neural basis for visual search in inferior temporal cortex
Nature
Spatial attention effects in macaque area V4
J. Neurosci.
Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent or overlapping neural systems?
Proc. Natl. Acad. Sci. USA
Neural mechanisms of selective visual attention
Annu. Rev. Neurosci.
Acute activation and inactivation of macaque frontal eye field with GABA-related drugs
J. Neurophysiol.
Grice-representability of response time distribution families
Psychometrika
Visual attention: control, representation, and time course
Annu. Rev. Psychol.
A neural system for error detection and compensation
Psych. Sci.
Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades
J. Neurophysiol.
The representation of visual salience in monkey parietal cortex
Nature
Pre- and poststimulus activation of response channels: a psychophysiological analysis
J. Exp. Psychol.: Hum. Percept. Perform.
Human reaction time: toward a general theory
J. Exp. Psych.: Gen.
Countermanding saccades in macaque
Vis. Neurosci.
Neural control of voluntary movement initiation
Science
The role of frontal eye field in countermanding saccades: visual, movement and fixation activity
J. Neurophysiol.
Involuntary attentional shifts due to orientation differences
Percept. Psychophys.
Spatial attention in visual search for features and feature conjunctions
Psych. Sci.
Neuronal responses to static texture patterns in area V1 of the alert macaque monkey
J. Neurophysiol.
Changes in neuronal activity of the monkey precentral cortex during preparation for movement
J. Neurophysiol.
Cited by (30)
Biomimetic race model of the loop between the superior colliculus and the basal ganglia: Subcortical selection of saccade targets
2015, Neural NetworksCitation Excerpt :See May, 2006 for a full review of the SC anatomy.) Despite the pivotal position of the SC in these pathways, target selection in the saccadic system has long been thought to occur at the cortical level—mainly involving the Frontal Eye Fields (Fischer, 1987; Schall & Hanes, 1998), while the SC would only serve as a Visual Mapping structure that relays the selection signal and process the saccade metrics for the brainstem. This view has been challenged, firstly by showing the implication of the SC in saccade target selection (Mays & Sparks, 1980; Ottes, Van Gisbergen, & Eggermont, 1987; Schiller, Sandell, & Maunsell, 1987), and secondly by exposing its active role in the selection process (Carello & Krauzlis, 2004; McPeek, 2008 and McPeek & Keller, 2002, 2004, among others).
Reaction time variability and related brain activity in methamphetamine psychosis
2015, Biological PsychiatryBedside saccadometry as an objective and quantitative measure of hemisphere-specific neurological function in patients undergoing cranial surgery
2015, Journal of Clinical NeuroscienceCitation Excerpt :The LATER model (Supp. Fig. 1) aims to define the relationship between saccadic latency and higher cognitive functions. It has been validated both empirically and neurophysiologically, [25–27,10,28,29]. Together, saccadometry and LATER model analysis can objectively quantify neurological deficit and further define the exact change in the cortical decision making process.
fMRI of intrasubject variability in ADHD: Anomalous premotor activity with prefrontal compensation
2008, Journal of the American Academy of Child and Adolescent PsychiatryA neural model of decision-making by the superior colicullus in an antisaccade task
2007, Neural NetworksCitation Excerpt :Such an assumption is consistent with known neurophysiology of saccadic eye movements. In the frontal eye fields of monkeys there are populations of visuomotor neurons that begin to fire in advance of saccades, with their activity rising linearly upon presentation of a suitable target stimulus (Hanes & Schall, 1996; Kim & Shadlen, 1999; Schall & Hanes, 1998). Buildup neurons in the monkey SC begin to linearly build up their activity after the signal to make a saccade is presented (Everling et al., 1998; Munoz & Wurtz, 1995b).
Computational algorithms and neuronal network models underlying decision processes
2006, Neural NetworksCitation Excerpt :Results of recent electrophysiological experiments in behaving monkeys have revealed that the decision variables are represented by activities of parietal and/or prefrontal neurons. For instance, in an experiment, monkeys were asked to make a saccade in one of the two possible directions, when the target direction was instructed by a visual cue (Schall & Hanes, 1998). Activity of some parietal neuron was correlated with the probability that a movement to the cell’s response field was instructed.
- 1
Present address: Laboratory for Sensorimotor Research, NIH, Building 49 Room 2A50, 9000 Rockville Pike, Bethesda, MD 20892, USA.