Saccadic Eye Movements, a Basic Introduction

Zvi Hershel Fishman

The City College of New York
July 23 2009
(slightly revised 5/5/2010)
Contact: hershy.fishman2@gmail.com
Eye movements

Voluntary movement is accomplished through the contraction of muscles. All voluntary

movement is mediated by skeletal muscles except for eye movement. The eye can rotate, to some
extent, with three degrees of freedom: horizontally, vertically, and, to some degree, torsionally.
For each degree of freedom, it can rotate in two directions; thus, it can rotate in six different
directions: right, left, up, down, clockwise, counterclockwise. This is accomplished by six
extraocular, or ocular, muscles which are connected to the eye, rotating it as they contract.
However, except for two of the muscles, the medial and lateral rectus muscles which correspond
to the two horizontal directions, each muscle is not assigned to one direction. With the other four,
the superior and inferior rectus and oblique muscles, there is overlap, all being involved in both
vertical and torsional rotation. Three cranial nuclei; III (oculomotor), IV (trochlear) and VI
(abducens); supply the motor neurons that innervate and control the ocular muscles.
In a paper published in 1903, psychologist R. Dodge divided eye movements into five types:
1) fast jerky movements to change the point of fixation, 2) smooth movement following a
moving object, 3) moving the eyes to fixate on an object while the head is moving, 4) jerky
compensatory eye movement due to spinning of the head, observed in darkness, 5) moving the
two eyes in opposite directions to point them to an object (Dodge 1903). Current understanding
divides the third type into two types: the vestibulo-ocular reflex (VOR), for sudden head
movement, and the optokinetic response for sustained head movement (Goldberg 2000).
Optokinetic response also applies to movement of the visual field with the head stationary
(Sparks 2002). The fourth type, on the other hand, is seen as just part of the VOR, thus the
number of types remains five (Goldberg 2000, Sparks 2002). A sixth, less common, type is the
cervico-ocular reflex (Leigh & Zee 2006).
A seventh and important type of ocular muscle action is the opposite of movement (1),
fixation. The specific amount of tonic firing of ocular motor neurons and in turn the
corresponding amount of contraction in each of the ocular muscles holds the eyes at any specific
position. Thus, each position of the eye corresponds to a different "step" on a recording of
oculomotor neural activity (Goldberg 2000).
Saccades

The first type mentioned by Dodge, the most frequent type of eye movement and the only
gaze shifting type, has been termed saccadic eye movements, or saccades, the French term for
_______
(1) That is on the macro level. In reality, anything that "happens" in the universe (giving meaning to the passage of time) is
movement of matter or energy. Fixation is movement of small molecules, ions and electrical charge preventing
movement of muscle.
jerk. The term was first used for quick eye movements in a French paper in 1879 by E. Javal
(after Leigh & Zee 2006). Humans make saccades more than 100,000 times per day (Wong
2007). Saccadic eye movements are the most widely studied movements due to their simplicity
of function and measurement, among other reasons. They serve as a model for understanding
many aspects of the sensorimotor system. Most animals, even insects, make saccades; however
there are many differences between species (see Land 1999). This paper is about human
saccades, although some data are taken from other primates with the assumption, for simplicity,
that they apply to humans.
The main purpose of saccades is to point the fovea, the center of the retina which senses the
most sharp and focused part of the visual scene, to another point in the scene. Otherwise, without
moving the head, one would constantly be focused on one point, seeing the entire rest of the field
only in the periphery. Researchers term the central two deg of the retina the fovea, the next three
degrees the parafovea, and the rest of the retina the periphery. However, this is just a
simplification; in reality, the resolution of the retina constantly declines in a spectrum starting
from the center point (Liversedge & Findlay 2000).
An even more important purpose of saccades is to change the image on the retina; otherwise,
the image would fade away within seconds. This has been demonstrated both by paralyzing the
ocular muscles and by attaching mirrors to contact lenses to be worn by a subject so that the
image s/he sees moves with the eye, and the eye cannot move off it. In such cases, the image
disappears from sight after a few seconds (Hall & White 2008, Martinez-Conde et al. 2004).
However, for this second purpose, it would suffice to just make small random non-voluntary
saccades. In fact, such “microsaccades” are indeed made for this purpose (Martinez-Conde et al.
2004). This can be observed with concentration when fixating for long on, for example, a letter
in print.
Each of the five types of eye movements has a distinct reaction time, or latency, and velocity.
Although velocity is higher for saccades than for any other type of eye movement—up to about
500 deg/sec (Leigh & Zee 2006) or even 900/sec (Goldberg 2000)—as is their acceleration and
rate of acceleration (“jerk” in physics) (Leigh & Zee 2006), their average reaction time is the
longest of the five types, about 200 ms (Sparks 2002). Under certain laboratory conditions
reaction time could be much faster, as discussed below. Velocity is affected by the type of
saccade, including its direction and target, and decreases under fatigue. However, for any given
condition, a saccade’s velocity, and thus also its duration, depends only on its amplitude and
cannot be controlled voluntarily. Peak velocity increases with amplitude following an asymptotic
curve that starts leveling off at about 20 deg amplitude and the eye’s maximum velocity, about
500 deg/sec (Leigh & Zee 2006). This relationship is referred to as the “main sequence,” and
minimizes the variability in saccade durations, being between 20 and 100 ms. Duration linearly
depends on amplitude for saccades with amplitudes of 1 to 50 degrees (Leigh & Zee 2006).
Saccades end abruptly (Optican 1985).
Saccadic suppression

Vision is a sequence of fixations (which in a broader sense can also include fixating on an
object while the eye is slowly moving due to one of the other types of eye movements) separated
by saccades (Goldberg 2000). At the high velocities of saccades it is impossible to see clearly,
but we do not even see the blur; vision is actively suppressed during saccades by a process called
saccadic suppression. Moreover, we don't experience brownouts or blackouts during saccades;
we experience the fixation images in a smooth sequence with no intervening noise. This is
referred to as saccadic omission (Campbell & Wurtz 1978). A related and more anomalous
phenomenon is watching a pre-digital motion picture, which is a sequence of images on a long
role of film. One doesn't perceive the images passing by, but rather a smooth movie.
Nonetheless, in a report published in June 2009, T. L. Watson and B. Krekelberg discovered that
an image projected during a saccade can still affect visual perception: An optical illusion distorts
a circle presented right after a line as an ellipse elongated orthogonal to the line. They presented
circles to subjects preceded by lines which on many trials fell during a saccade and thus were not
perceived. Yet, the lines still effected the illusion on the circle (Watson & Krekelberg 2009).
Reflexive saccades

Besides for saccades which one constantly makes while volitionally scanning the visual
scene, saccades are elicited reflexively at the appearance of a stimulus in the periphery or in
response to a sudden sound or touch. This is important to help one notice a danger or an
opportunity. When two stimuli appear at the same time, a saccade is made to their center, and a
second saccade goes to one of them. This is termed the "global effect." When one stimulus is
larger or more luminant than the other, the saccade goes toward the "center of gravity" of the two
(summarized in Beauvillain et al. 1995). Similarly, when one stimulus is closer, the saccade is
biased toward the closer one (Edelman et al. 2007 citing Findlay 1982). Interestingly, some
evidence shows that the appearance of stimulus in the visual field may elicit a saccade
independently to the visual perception. This has been investigated through optical illusions
where the perception does not match the actual vision (de'Sperati & Boud-Bovy 2008). This can
be explained by the direct pathway of DSC from SSC from retina, to be discussed bellow.
However, it can also be mediated by cortical regions but bypassing the perceptual pathways.
However, stimuli don't always elicit saccades. Otherwise, it would be impossible to focus on a
task, for example, reading, while stimuli are constantly appearing in the peripheral view. In such
cases, the brain suppresses the reflex, just as all motor reflexes can be suppressed at will by
applying an opposite force. Nevertheless, the stimuli still exhibit an effect on eye movement.
Researchers have found that they inhibit the eye from making saccades for a brief period, 70-100
ms following their appearance. This is termed "saccadic inhibition" (Reingold & Stampe 2004).
Feedback

The visual response time is about 100 ms. Since the duration of saccades is about the same, a
saccade’s size cannot be affected by visual information presented midflight (Leigh & Zee 2006).
If the target’s position moves midflight, a second corrective saccade will be made. However, if
this is repeated a few times, the saccades progressively adapt to land on the target (Optican
1985). However, a saccade can be altered midflight by visual information that was presented
before the saccade onset and was processed midflight (Leigh & Zee 2006). Some researchers
report to have found that saccades can be terminated midflight by suddenly appearing stimuli in
the periphery (that appeared earlier and were processed midflight) (Edelman & Xu 2009).
Neural structure

All five types of eye movement are controlled by the ocular muscles and motor neurons of the
three cranial nerves described earlier, but they differ in the higher pathways controlling the motor
neurons innervating the muscles. For saccades, the motor neurons of the three cranial nerves are
controlled by burst cells of one of two gaze centers in the brain stem reticular formation
depending on axis (horizontal vs. vertical). The paramedian pontine reticular formation (PPRF)
controls horizontal saccades and the horizontal component of oblique (slanted) saccades, while
the rostral interstitial nucleus of the mesencephallic reticular formation in the midbrain controls
the vertical component. The gaze centers in the reticular formation are, in turn, controlled by
upper motor neurons in higher brain centers: most importantly, the superior colliculus (SC) of the
midbrain and the frontal eye fields (FEF) of the premotor cortex. Two other important higher
regions are the supplementary eye fields (SEF), and the lateral intraparietal area (LIP).
The superior colliculus (superior as opposed to the inferior colliculus under it, colliculus,
Latin for hill, denoting its structure: two bumps on each side of the dorsal part of the midbrain)
has multiple layers. The superficial layers (the SSC) code for visual information and the
intermediate and deep layers (DSC) code for motor activity. Axons from magnocellular parts, or
M cells, from the retina project to the SSC, sending it raw eye data, as do higher neurons from
the striate cortex, sending it processed data, supplying the SSC with a topographic map of the
contralateral visual hemifield. The DSC, on the other hand, has a "motor map" which codes for
saccades to every eye position. Neurons for small saccades are found in the rostral region, while
those for large saccades are found in the caudal region (Munoz & Istvan 1998 citing Robinson
1972). The map is revealed to researchers both by recording the DSC areas firing at saccades to
different eye positions and, conversely, by electrically stimulating those areas and causing the
corresponding saccades (Munoz & Istvan 1998). Recent evidence has rejuvenated an earlier view
that each point in the DSC motor map has a direct connection to the corresponding point in the
SSC, enabling the DSC upper motor neurons to respond to visual stimuli (Hall & White 2008).
However, the direct intracullicular connection is not the only one enabling the visumotor
response. The DSC motor map also has direct input from multiple cortical areas; moreover, the
SSC also projects back to the cortex (Goldberg 2000). The DSC motor map is also projected to
by an auditory map and a sensory map of the body enabling saccades to be executed in response
to sound and touch (Hall & White 2008). The command from the DSC is sent to the reticular
formation where the particular desired eye position is translated by interneurons into activity of
particular oculomotor neurons to activate the necessary ocular muscles at the right magnitude.
To better understand how the DSC motor map is coded, D. L. Sparks and colleagues
stimulated the DSC in trained monkeys to induce a saccade in one direction right after the
monkeys were about to make one in another direction. They found that the volitional saccades
had new vectors to compensate for the shift and landed in the correct place, rather than having
the same vector they were supposed to have and landing in the wrong place. This shows that the
motor map codes for end results of eye position rather than simply for particular vectors (Hall &
White 2008 citing Sparks & Mays 1983).
Each step on a recording of motor neuron activity corresponding to a different fixation
position, as mentioned above, is separated by a high spike caused by a "pulse" of neural saccadic
activity. Its height corresponds to the peak velocity. Three areas of the brain, the cerebellar
flocculus, the medial vestibular nucleus and the nucleus prepositus hypoglossi are responsible for
the cooperation of the fixation neurons with pulse neurons by changing the tonic "step" signal to
that of the new landing position. How do they accomplish this task? D. A. Robinson theorized
that they calculate the new position by integrating the velocity (known from the level of the
pulse) (Goldberg 2000). Or, perhaps, in a propreoceptive process, neurons projected from these
areas sense the new landing position similar to the sensing of the position of one's limbs.
Above the SC in the hierarchy are the frontal eye fields in the premotor cortex. Electrical
stimulation in the FEF can also cause saccades. Movement-related neurons in the FEF terminate
at excitatory synapses in the DSC. In addition, other movement-related neurons of the FEF
disinhibit the SC by terminating at excitatory synapses in the caudate nucleus of the basal
ganglia which inhibit the substantia nigra pars reticulata from inhibiting the SC during a saccade.
These neurons that project to the DSC fire only before saccades that are related to behavior. The
FEF also projects directly to the gaze centers of the reticular formation. Thus, monkeys with
lesions to either the FEF or the SC can still recover the ability to make saccades, although some
deficits remain (Goldberg 2000, Hall & White 2008) as will be mentioned below.
The SEF have a unique role. Rather than coding for saccades to specific eye positions, they
code for saccades to the contralateral side of an object (Goldberg 2000). However, the SEF are
not unique to saccades; they also mediate non-saccade-related attention that is object relative
(Olson 2003). The LIP is involved in memory related saccades (Goldberg 2000).
Fixation is stabilized by several systems that inhibit saccades. 1) Omnipause neurons in the
nucleus of the dorsal raphe inhibit the pontine burst cells. 2) The rostral DSC (beside for
containing other neurons causing small saccades, as above) inhibit the excitatory neurons in the
DSC and excite omnipause neurons in the nucleus of the dorsal raphe (Goldberg 2000). 3) The
substantia nigra pars reticulata also inhibit the DSC (as briefly mentioned above). Stimulating
fixation neurons with low-frequency microstimulation increases latency, and stimulating them
during a saccade interrupts the saccade in midflight (Munoz & Istvan 1998 citing Munoz and
Wurtz 1993). The latter is true for both the pontine omnipause neurons as well as for the rostral
SC (Edelman & Xu 2009 citing others). Gandhi & Keller (1995, cited by Walker et al. 1997)
found neurons extending to the more caudal SC which, when stimulated, interrupt saccades only
extending 10 deg of eccentricity, suggesting that the central 10 deg is the limit of the fixation
region (Walker et al. 1997). In fact, saccades land accurately only when their amplitudes are less
than 10 deg; otherwise, a second corrective saccade is usually needed (Optican 1985).
Head movement

Saccades are usually studied having the head fixed in order measure the eye movements, but
in real life, head movements are also part of the “gaze system” (Goldberg 2000). Therefore, the
results of many studies may differ in real life. For example, a reflexive saccade elicited by a
suddenly appearing stimulus may be smaller when it can be complemented with a reflexive head
movement. Freedman et al. (1996, cited in Gilchrist et al. 1997) stimulated areas in the DSC of
rhesus monkeys with their head unrestrained and found that it caused combined head-eye
movements. A notable case demonstrating that the saccadic system is not fundamentally limited
to eye movements is reported in Nature of a woman who has no functional eye muscles and yet
makes “saccadic head movements” very similar to saccadic eye movements (Gilchrist et al.
1997).
Laboratory saccades

In real life, saccades occur with little, if any, awareness. However, researchers have opened
many new sub-fields of saccadic research by investigating saccades executed on command by
humans or trained monkeys. Many of these experiments are purely psychological in nature,
investigating one's behavioral response to various types of saccadic instruction. More
importantly for this discussion, researchers have investigated the interaction of an instruction or
volition conflicting with the reflexive direction of a stimulus. Researchers have found that
subjects can make “anti-saccades,” to the opposite direction at the appearance of a stimulus, or to
volitionally land before or after the target (Optican 1985 citing “Hallet 1978”). Anti-saccades
have, on average, longer latencies increasing with age, and lower velocity than regular (“pro”)
saccades (Leigh & Zee 2006). Patients with lesions in the FEF cannot recover the ability to make
anti-saccades (Hall & White 2008). Another case is when a subject is instructed to make a
saccade to a target as soon as it appears or upon some other cue, and a distracting stimulus
appears somewhere else on the scene. Researchers have found that if it is distant from the target,
it causes the latency to be longer, but its landing point is unaffected. This is called the
"remote-distractor effect." On the other hand, if the distractor is close to the target, the amplitude,
but not the latency, is affected (Walker et al. 1997). The remote-distractor effect demonstrates
that suddenly appearing stimuli, in addition to eliciting attention, directly affect the saccadic
system (Findlay 1999). Researchers investigated this effect in conjunction with saccadic
inhibition (mentioned above): How long does the remote-distracor effect last, or, put differently,
how close, spatially, does a distractor cause saccadic inhibition? They found that inhibition in the
70-100 ms window occurs when the distarctor is 45 deg or more from the target. In contrast,
when it is 22.5 deg or less from the target, saccades are facilitated, yet direction is only
minimally affected, showing that saccades can be initiated by a distractor although they are still
cognitively directed to the target (Edelman & Xu 2009). In analyzing the results of this study,
however, they did not differentiate between saccades on the basis of their latency, i.e. to see
whether or not the likelihood of a saccade to occur at a particular range of time after the
appearance of a distractor depends on its reaction time to the appearance of the target itself or to
the cue to make the saccade.
Subjects may be instructed to saccade to a remembered location with no visible target.
Patients with lesions in the FEF cannot make such saccades (Hall & White 2008), demonstrating
that the FEF works with the LIP in executing memorized saccades.
One of the most important findings investigating commanded saccades has been "express
saccades." Researchers have found that by having subjects saccade to a target as fast as possible
while the fixation system is inactive or weakly active, saccades can be made with as little as
80-110 ms of latency. This is done in a technique called the "gap paradigm," first introduced by
M. G. Saslow in 1967, where the subject fixates on a fixation point and then the target appears
100-200 ms after the fixation point disappeared. Express saccades probably rarely occur in real
life where the scene is more diversified, and the ability to make them improves with practice
(Leigh & Zee 2006). A study on monkeys has shown that the velocity of express saccades is
similar to that of regular saccades (Edelman & Keller 1996); however, another study on humans
showed that it may be higher (Edelman & Xu 2009). However, those were not real express
saccades; they were willed earlier, but facilitated by a proximal distractor. It is disputed whether
express saccades in humans are a unique type or whether they are simply at the far end of a
spectrum (Edelman & Keller 1996). What makes express saccades so interesting is their neural
pathway. While normal-latency saccades show two separate bursts of visumotor neural activity,
first the visual response 40-60 ms after the appearance of the target and then the motor response
20-25 ms before the saccade, M. A. Sommer (1994, cited by Edelman & Keller 1996)
hypothesized, based on the reaction time of express saccades matching the sum of the duration of
these two responses, that in express saccades there is only one burst, the visual acting also as the
motor response. J. A. Edelman and E.L. Keller (1996) tested this hypothesis on two macaque
monkeys and found only one burst in 83% of the visumotor neurons they tested. The standard
deviations of their timing showed that they were equally aligned with the visual appearance as
with the motor response. Furthermore, most of the remaining visumotor neurons that did show
two bursts were distinct from normal-latency bursts. Moreover, the activity of the peaks was
higher than the sum of the expected activities of separate visual and motor peaks, suggesting that
the visual burst of express saccades is unique, reaching a threshold which brings it to make a
saccade (Edelman & Keller 1996). In addition to showing this neural property of express
saccades, this finding and others to follow (Dorris et al., 1997, Sparks et al. 2000), demonstrated
the existence of express saccades, that they are indeed initiated by the target and not earlier, in
anticipation, as some in the psychological field have argued (J. A. Edelman, personal
communication, July 2009. See also Rohrer & Sparks (1993) cited by Sparks et al. (2000) for
additional evidence that they are not anticipatory). However, D. Sparks et al. (2000) hold that
unlike Sommer’s theory, the merged burst is just really two separate busts happening in the same
neuron at the same time. They argue that this is suggested from their results obtained from nine
visumotor neurons of two rhesus monkeys. They recorded the bursts over a range of trials
gradually decreasing from regular to express saccades rather than testing two distinct groups of
regular and express saccades. They found a gradual decrease in the interval between the bursts,
the first always aligned with the visual presentation and the second with the saccade, until they
merged for express saccades.
What is the neural pathway of express saccades? Lesions in the SC abolish the ability to make
express saccades while lesions in the FEF do not. This suggests that the direct retinocollicular
pathway mediates express saccades (Hall & White 2008). However, there are difficulties with
this approach: Express saccades can be made to isoluminant targets which differ from the
background only in color; vision of these targets is mediated by the parvocellular pathway, not
by the M cells which project to the SSC. Furthermore, lesions in the lateral geniculate nucleus of
the thalamus also abolish express saccades. This would suggest that the pathway is from the
retina to the thalamus and cortex and then to the DSC (Edelman and Keller 1996). Additional
evidence for cortical input in the pathway of at least certain express saccades can be deduced
from Edelman et al. (2007), an important finding in its own right: Expanding on the findings of
He & Kowler (1989) that instruction based on color can bias one target over another in the global
effect, similar to the way size and luminance do (see above) (Edelman et al. 2007 citing He &
Kowler 1989), J. A. Edelman et al. (2007) found this effect also in express saccades and when
the instruction is target based, to the right or left target regardless of where they appear in the
visual field (such saccades being mediated by the SEF, as above). Furthermore, they found that
this bias based on instruction completely overrides an opposite bias based on size or luminance.
Summary

There are generally considered to be five types of human eye movements. Saccades are the
only type changing the point of fixation. They serve two main purposes: Small “microsaccades''
are made when fixating for a while to shift the image on the retina—otherwise it would fade
away—and larger saccades are made volitionally when scanning the visual field or reflexively,
elicited by suddenly appearing stimuli, to view clearly with the fovea an area of the peripheral
view. Vision is actively suppressed during a saccade and the experience omitted. However,
evidence suggests that the omitted image can still affect vision as can saccades be elicited by a
stimulus that is not seen. Saccades are stereotyped, all having their velocity and duration
dependant on amplitude, although they can be affected by direction, target, fatigue etc.. Saccades
are the fastest but have the longest average reaction time of all eye movements, about 200 ms,
but in the laboratory, using the gap paradigm where there is a gap of 100-200 ms before the
target appears, “express saccades'' can be as low as 80-110 ms.
The study of saccades is very important in neuroscience. Cranial nerve nuclei III, IV, and VI
innervate the six muscles that control eye movement. Saccades are coded for in the DSC and the
FEF, each of which can work independently of the other. They have topographic maps of the
contralateral visual hemifield and code for every type of eye position which is translated by the
two brainstem gaze centers to the firing of the neurons needed for the horizontal and vertical
components of saccades. Fixation, both inhibiting saccades and keeping the eyes in the correct
position are controlled by multiple brain areas. Saccades show two bursts, the first visually
aligned and the second saccade aligned; however, express saccades show only one, and the
explanation for this is disputed. Express saccades are associated with the SC and not the FEF, but
their exact pathway is still unclear.
There is an infinite amount of experiments that can be made, testing where the eye will
saccade to in the face of various competing stimuli. This can be further complicated by various
instructions, and by examining their velocity, latency, and by many other factors. Many areas of
saccadic research have yet to examine their results in the real-life situation where head
movements, an integral part of the saccadic system, are involved. Most important in the future of
saccadic research is the neuroscience: precisely mapping out all the neural pathways involved,
part of a larger task, of doing the same for all movements and, moreover, for all brain functions.
The genetic revolution further enables researchers to understand the development of these
pathways on the protein and DNA level, the complete picture, an ultimate goal in biology.

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