Elsevier

Neural Networks

Volume 11, Issues 7–8, October–November 1998, Pages 1241-1251
Neural Networks

1998 Special Issue
Neural mechanisms of selection and control of visually guided eye movements

https://doi.org/10.1016/S0893-6080(98)00059-8Get rights and content

Abstract

The selection and control of action is a critical problem for both biological and machine animated systems that must operate in complex real world situations. Visually guided eye movements provide a fruitful and important domain in which to investigate mechanisms of selection and control. Our work has focused on the neural processes that select the target for an eye movement and the neural processes that regulate the production of eye movements. We have investigated primarily an area in the frontal cortex that plays a central role in the production of purposive eye movements which is called the frontal eye field. A fundamental property of biological nervous systems is variability in the time to respond to stimuli. Thus, we have been particularly interested in examining whether the time occupied by perceptual and motor decisions explains the duration and variability of behavioral reaction times. Current evidence indicates that salient visual targets are located through a temporal evolution of retinotopically mapped visually evoked activation. The responses to non-target stimuli become suppressed, leaving the activation representing the target maximal. The selection of the target leads to growth of movement-related activity at a stochastic rate toward a fixed threshold to generate the gaze shift. For a given image, the neural concomitants of perceptual processing occupy a relatively constant interval so that stochastic variability in response preparation introduces additional variability in reaction times. Neural processes in another cortical area, the supplementary eye field, do not participate in the control of eye movements but seem to monitor performance. The signals and processes that have been observed in the cerebral cortex of behaving monkeys may provide useful examples for the engineering problems of robotics.

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)

  • S. Sternberg

    The discovery of processing stages: extensions of Donders' method

    Acta Psychologica

    (1969)
  • D.Y. Teller

    Linking propositions

    Vision Res.

    (1984)
  • C.M. Zingale et al.

    Planning sequences of saccades

    Vision Res.

    (1987)
  • J.M. Allman et al.

    Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local–global comparisons of visual motion

    Annu. Rev. Neurosci.

    (1985)
  • W.F. Bacon et al.

    Overriding stimulus-driven attentional capture

    Percept. Psychophys.

    (1994)
  • D.H. Ballard et al.

    Memory representations in natural tasks

    J. Cogn. Neurosci.

    (1995)
  • Bichot, N.P., & Schall, J.D. (1998). Evidence for parallel feature-based saccade target selection in macaque during...
  • N.P. Bichot et al.

    Visual feature selectivity in frontal eye fields induced by experience in mature macaques

    Nature

    (1996)
  • Boring, E. G. (1950). A history of experimental psychology. New York:...
  • C.J. Bruce et al.

    Primate frontal eye fields. I. Single neurons discharging before saccades

    J. Neurophysiol.

    (1985)
  • C.J. Bruce et al.

    Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements

    J. Neurophysiol.

    (1985)
  • Carpenter, R. H. S. (1981). Oculomotor procrastination. In D. F. Fisher, R. A. Monty, & J. W. Senders (Eds.), Eye...
  • Carpenter, R.H.S. (1988). Movements of the eyes. London:...
  • Carpenter, R.H.S. (1991). Eye movements. London:...
  • R.H.S. Carpenter et al.

    Neural computation of log likelihood in the control of saccadic eye movements

    Nature

    (1995)
  • L. Chelazzi et al.

    A neural basis for visual search in inferior temporal cortex

    Nature

    (1993)
  • Coles, M. G. H., Smid, H. G. O. M., Scheffers, M. K., & Otten, L. J. (1995). Mental chronometry and the study of human...
  • C.E. Connor et al.

    Spatial attention effects in macaque area V4

    J. Neurosci.

    (1997)
  • M. Corbetta

    Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent or overlapping neural systems?

    Proc. Natl. Acad. Sci. USA

    (1998)
  • R. Desimone et al.

    Neural mechanisms of selective visual attention

    Annu. Rev. Neurosci.

    (1995)
  • E.C. Dias et al.

    Acute activation and inactivation of macaque frontal eye field with GABA-related drugs

    J. Neurophysiol.

    (1995)
  • Donders, F. C. (1868). On the speed of mental processes. In W. G. Koster (transl.) (1969) Attention and performance II...
  • E.N. Dzhafarov

    Grice-representability of response time distribution families

    Psychometrika

    (1993)
  • H.E. Egeth et al.

    Visual attention: control, representation, and time course

    Annu. Rev. Psychol.

    (1997)
  • W.J. Gehring et al.

    A neural system for error detection and compensation

    Psych. Sci.

    (1993)
  • M.E. Goldberg et al.

    Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades

    J. Neurophysiol.

    (1981)
  • J.P. Gottlieb et al.

    The representation of visual salience in monkey parietal cortex

    Nature

    (1998)
  • G. Gratton et al.

    Pre- and poststimulus activation of response channels: a psychophysiological analysis

    J. Exp. Psychol.: Hum. Percept. Perform.

    (1988)
  • G.R. Grice et al.

    Human reaction time: toward a general theory

    J. Exp. Psych.: Gen.

    (1982)
  • Hanes, D. P., & Carpenter, R. H. S. (1998). Countermanding saccades in humans: evidence for a race-to-threshold...
  • D.P. Hanes et al.

    Countermanding saccades in macaque

    Vis. Neurosci.

    (1995)
  • D.P. Hanes et al.

    Neural control of voluntary movement initiation

    Science

    (1996)
  • D.P. Hanes et al.

    The role of frontal eye field in countermanding saccades: visual, movement and fixation activity

    J. Neurophysiol.

    (1998)
  • J.S. Joseph et al.

    Involuntary attentional shifts due to orientation differences

    Percept. Psychophys.

    (1996)
  • M-S. Kim et al.

    Spatial attention in visual search for features and feature conjunctions

    Psych. Sci.

    (1995)
  • Klein, R., Kingstone A., & Pontefract, A. (1992). Orienting of visual attention. In K. Rayner (Ed.) Eye movements and...
  • J.J. Knierim et al.

    Neuronal responses to static texture patterns in area V1 of the alert macaque monkey

    J. Neurophysiol.

    (1992)
  • J.-C. Lecas et al.

    Changes in neuronal activity of the monkey precentral cortex during preparation for movement

    J. Neurophysiol.

    (1986)
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    Present address: Laboratory for Sensorimotor Research, NIH, Building 49 Room 2A50, 9000 Rockville Pike, Bethesda, MD 20892, USA.

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