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| Volume 3, Number 11, Introduction i, Pages i-iii |
doi:10.1167/3.11.i |
http://journalofvision.org/3/11/i/ |
ISSN 1534-7362 |
Special Issue Introduction
Linking eye movements and perception
Leland S. Stone |
Human Factors Research and Technology Division, NASA Ames Research Center, Moffett Field, CA, USA |
|
Frederick A. Miles |
Laboratory of Sensorimotor Research, National Eye Institute, Bethesda, MD, USA |
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Martin S. Banks |
Vision Science Program and Department of Psychology, University of California, Berkeley, CA, USA |
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Evolution has endowed primates with a highly
specialized fovea, which allows them to perform detailed and sophisticated
visual processing, albeit restricted to a small fraction of the visual field.
They have also developed many specialized visual cortical areas, that greatly
emphasize the representation of the central visual field and that support an
impressive array of perceptual capabilities. In parallel, primates display a
remarkable repertoire of oculomotor behaviors that take advantage of their
powerful foveal processing and allow them to use their eyes to locate, acquire,
and pursue objects embedded in complex, dynamic visual scenes. Perhaps these
perceptual and eye-movement mechanisms evolved independently. However, it would
seem more likely that the new visual and oculomotor capabilities, unique to
primates, evolved together as integrally linked systems.
The papers in this special issue of the Journal of
Vision examine links between eye movements and visual perception. They focus on
three related questions.
First, how do eye movements affect visual performance?
Eye movements can enhance performance under some circumstances (e.g. performance
in a steering task is improved when drivers’ gaze movements are
unconstrained, Wilkie & Wann, 2003;
fixational eye movements improve visual discrimination performance, Rucci & Desbordes, 2003), yet provide little
or no advantage under other conditions (e.g. direction discrimination judgments
are unaffected by pursuit eye movements, Krukowski, Pirog, Beutter, Brooks, &
Stone, 2003; bisection judgments are virtually unaffected by fixation
shifts, Trommershauser, Maloney, &
Landy, 2003). Perceptual performance appears to depend on the most reliable
signal available, whether the signal is sensory or motor in origin. For
example, eye movements can improve perceptual performance in both slant and
depth estimation tasks when objects are widely separated in space ( Backus & Matza-Brown, 2003; Zhang, Berends, & Schor, 2003), or when
disparity signals are noisy ( Berends, Zhang,
& Schor, 2003). Furthermore, the dependence of oculomotor behavior on
the visual task suggests that eye-movement strategies are tailored to acquire
specific visual information ( Welchman &
Harris, 2003).
Second, to what extent are eye movements limited by raw
sensory signals or by higher-order perceptual signals? Two studies that examine
the pursuit responses to perceptually ambiguous stimuli reveal that pursuit eye
movements are directly related to perceptual choices on a moment-by-moment
basis, even when the stimulus remains completely unchanged ( Madelain & Krauzlis, 2003; Stone & Krauzlis, 2003). Furthermore, pursuit
is subject to the same motion processing limitations as perception ( Watamaniuk & Heinen, 2003). Using
illusions, studies found that both the conjugate ( McCarley, Kramer, DiGirolamo, 2003) and
vergence ( Both, Ee, & Erkelens, 2003; Sheliga & Miles, 2003) components of
voluntary saccades respond to perceived target location and depth even when the
percept is in conflict with the raw retinal images.
Third, to what extent is visual perception driven by
retinal signals versus oculomotor signals? Several studies found that reliable
and precise visual percepts of motion can be driven by an oculomotor signal with
little or no retinal motion ( Freeman,
Sumnall, & Snowden, 2003; Krukowski
et al, 2003) or that depth judgments can be influenced by oculomotor
signals, even when in conflict with retinal disparity ( Backus & Matza-Brown, 2003; Nawrot, 2003). Efference-copy signals can also
foster perceptual mis-localizations, even when the responsible eye movement is
not perceived ( Blohm, Missal, & Lefevre,
2003). Hamker ( 2003) provides a model
mechanism by which motor signals might be fed back from higher-order cortical
areas to influence processing in earlier visual areas.
Although this special issue is not meant to provide a
complete overview of the current status of this field, it does highlight some
interesting and important recent examples of links between oculomotor and visual
behavior. There are, we believe, three take-home messages. First, oculomotor
strategies can affect visual performance either directly by recruitment of
efference-copy information or indirectly by foveation and stabilization of the
retinal image, but performance effects will depend on the salience of the visual
and efference-copy cues, and on the demands of the task (see also e.g., Zelinsky & Sheinberg 1997; Findlay, 1998; Hooge & Erkelens, 1999; Eckstein, Beutter, & Stone, 2001).
Second, saccadic, pursuit, and vergence eye movements are strongly influenced by
higher-order visual processing related to perception and cognition, and cannot
be explained by retinal inputs alone (see also e.g., Steinbach, 1976; Khurana & Kowler, 1987; Ringach, Hawken, & Shapley, 1996; Krauzlis & Stone, 1999). Third,
feedback of motor commands, long known to play a critical role in controlling
oculomotor behavior ( Robinson, 1981), plays
a critical role in visual perception as well (see also e.g., Pola & Wyatt, 1989; Freeman & Banks, 1998; Turano & Heidenreich, 1999).
A major conclusion is that computational models of
primate visual perception need to be extended to incorporate an explicit role
for eye movements, together with their associated attentional shifts and motor
commands. Traditional linear-system models of oculomotor behavior (e.g. Robinson, 1981; Lisberger, Morris, & Tyschen, 1987),
which limit visual processing to subtraction and differentiation of retinal
signals and a few static non-linearities, must incorporate the higher-order,
fundamentally non-linear visual processing associated with perception. In sum,
the two fields of visual psychophysics and oculomotor behavior, and their
associated neurophysiological counterparts, need to coalesce. The picture
emerging is that perception is a sensorimotor process, the final step in an
interactive dance between sensation and action.
Backus
B.T. & Matza-Brown, D. (2003). The contribution of vergence change to the
measurement of relative disparity. Journal of
Vision, 3 (11), (this issue), http://journalofvision.org/3/11/,
doi:10.1167/3.11.
Berends, E.M., Zhang, Z.-L.,
Schor, SM. (2003). Eye movements facilitate stereo-slant discrimination when
horizontal disparity is noisy. Journal of
Vision, 3 (11), (this issue), http://journalofvision.org/3/11/,
doi:10.1167/3.11.
Blohm, G., Missal, M., &
Lefevre, P. (2003). Smooth anticipatory eye movements alter the memorized
position of flashed targets. Journal of
Vision, 3 (11), (this issue), http://journalofvision.org/3/11/,
doi:10.1167/3.11.
Both, M.H., van Ee, R., &
Erkelens, C.J. (2003). Perceived slant from Werner’s illusion affects
binocular saccadic eye movements. Journal of
Vision, 3 (11), (this issue), http://journalofvision.org/3/11/,
doi:10.1167/3.11.
Eckstein, M.P., Beutter,
B.R., & Stone, L.S. (2001). Quantifying the performance limits of human
saccadic targeting during visual search.
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Findlay, J. (1998). Active
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Freeman, T.C. & Banks,
M.S. (1998). Perceived head-centric speed is affected by both extra-retinal and
retinal errors. Vision Research, 38,
941-945. [PubMed]
Freeman, T.C.A., Sumnall,
J.H., & Snowden, R.J. (2003). The extra-retinal motion afteraffect.
Journal of Vision, 3 (11), (this
issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
Hamker, F.H. (2003). The
reentry hypothesis: Linking eye movements to visual perception.
Journal of Vision, 3 (11), (this
issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
Hooge, I.T. & Erkelens,
C.J. (1999). Peripheral vision and oculomotor control during visual search.
Vision Research, 39, 1557-1575. [PubMed]
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E. (1987). Shared attentional control of smooth eye movement and perception.
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Trends in Neuroscience, 22, 544-550. [PubMed]
Krukowski, A.E., Pirog,
K.A., Beutter, B.R., Brooks, K.R., & Stone, L.S. (2003). Human
discrimination of visual direction of motion with and without smooth pursuit eye
movements. Journal of Vision, this
issue
Lisberger,
S.G., Morris, E.J., & Tyschen, L. (1987). Visual motion processing and
sensory-motor integration for smooth pursuit eye movements.
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Krauzlis, R.J. (2003). Pursuit of the ineffable: perceptual and motor reversals
during tracking of apparent motion. Journal of
Vision, this issue
McCarley, J.S., Kramer, A.F.,
& DiGirolamo (2003). Differential effects of the Muller-Lyer illusion on
reflexive and voluntary saccades. Journal of
Vision, 3 (11), (this issue), http://journalofvision.org/3/11/,
doi:10.1167/3.11.
Nawrot, M. (2003). Depth from
motion parallax scales with eye movement gain.
Journal of Vision, 3 (11), (this
issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
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briefly presented stimuli. Journal of Vision,
3 (11), (this issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
Sheliga, B.M. & Miles, F.A.
(2003). Perception can influence the vergence responses associated with
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(this issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
Trommershauser J.,
Maloney, L.T., & Landy, M.S. (2003). The consistency of bisecting judgments
in visual grasp space. Journal of Vision,
3 (11), (this issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
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Welchman, A.E. & Harris,
J.M. (2003). Task demands and binocular eye movements.
Journal of Vision, 3 (11), (this
issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
Wilkie, R.M. & Wann, J.P.
(2003). Eye-movements aid the control of locomotion.
Journal of Vision, 3 (11), (this
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3 (11), (this issue), http://journalofvision.org/3/11/, doi:10.1167/3.11.
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