Voluntary spatial attention has different effects on voluntary and reflexive saccades.

Abstract

Although numerous studies have investigated the relationship between saccadic eye movements and spatial attention, one fundamental issue remains controversial. Some studies have suggested that spatial attention facilitates saccades, whereas others have claimed that eye movements are actually inhibited when spatial attention is engaged. However, these discrepancies may be because previous research has neglected to separate and specify the effects of attention for two distinct types of saccades, namely reflexive (stimulus-directed) and voluntary (antisaccades). The present study explored the effects of voluntary spatial attention on both voluntary and reflexive saccades. Results indicate that voluntary spatial attention has different effects on the two types of saccades. Antisaccades were always greatly facilitated following the engagement of spatial attention by symbolic cues (arrows) informing the subject where the upcoming saccade should be directed. Reflexive saccades showed little or no cueing effects and exhibited significant facilitation only when these cues were randomly intermixed with uncued trials. In addition, the present study tested the effects of fixation condition (gap, step, and overlap) on attentional modulation. Cueing effects did not vary due to fixation condition. Thus, voluntary spatial attention consistently showed different effects on voluntary and reflexive saccades, and there was no evidence in these studies that voluntary cues inhibit reflexive saccades, even in a gap paradigm.

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Research Article
TheScientificWorldJOURNAL (2003) 3, 881-902
ISSN 1537-744X; DOI 10.1100/tsw.2003.72


Voluntary Spatial Attention has Different Effects on
Voluntary and Reflexive Saccades
Stephanie K. Seidlits1,2, Tammi Reza3, Kevin A. Briand1,
and Anne B. Sereno*,1
1Department of Neurobiology and Anatomy and the Keck Center for the Neurobiology of
Learning and Memory, University of Texas – Houston Medical School, 6431 Fannin Street, Houston,
TX 77030; 2Department of Bioengineering, Rice University, Suite 116 Keck Hall,
6100 Main, Houston, TX 77005; 3Microbia, Inc., 320 Bent Street, Cambridge, MA 02141
E-mail: anne.b.sereno@uth.tmc.edu
Received June 16, 2003; Revised August 11, 2003; Accepted August 14, 2003; Published September 15, 2003
Although numerous studies have investigated the relationship between saccadic eye
movements and spatial attention, one fundamental issue remains controversial.
Some studies have suggested that spatial attention facilitates saccades, whereas
others have claimed that eye movements are actually inhibited when spatial attention
is engaged. However, these discrepancies may be because previous research has
neglected to separate and specify the effects of attention for two distinct types of
saccades, namely reflexive (stimulus-directed) and voluntary (antisaccades). The
present study explored the effects of voluntary spatial attention on both voluntary
and reflexive saccades. Results indicate that voluntary spatial attention has different
effects on the two types of saccades. Antisaccades were always greatly facilitated
following the engagement of spatial attention by symbolic cues (arrows) informing
the subject where the upcoming saccade should be directed. Reflexive saccades
showed little or no cueing effects and exhibited significant facilitation only when
these cues were randomly intermixed with uncued trials. In addition, the present
study tested the effects of fixation condition (gap, step, and overlap) on attentional
modulation. Cueing effects did not vary due to fixation condition. Thus, voluntary
spatial attention consistently showed different effects on voluntary and reflexive
saccades, and there was no evidence in these studies that voluntary cues inhibit
reflexive saccades, even in a gap paradigm.
KEYWORDS: spatial attention, prosaccades, antisaccades, voluntary, reflexive
DOMAINS: higher level brain function, cognition


*Corresponding author.
©2003 with author.

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INTRODUCTION

Previous research involving the relationship between spatial attention and saccades has led to
disagreement on the seemingly basic issue of whether or not spatial attention facilitates, inhibits, or
has no effect on saccadic eye movements. The view that voluntary spatial attention facilitates
saccades has been suggested by several studies (e.g., [1]). This facilitation is often interpreted as an
indication that endogenous shifts of attention precede endogenous saccades[2]. Theoretical proposals
such as the “premotor” theory of attention[3,4] are supportive of this view. The premotor theory
asserts that by preparing an attentional shift, one automatically also prepares an oculomotor or
manual response. It assumes that since the spatial maps used to code shifts of attention in space are
also involved in the preparation of oculomotor responses, that preparation to shift attention inevitably
leads to the preparation of a saccade to that location. And, indeed, recent imaging work suggests an
overlap in some cortical regions for attending, looking, and pointing[5].
However, other studies[6] have proposed that spatial attention actually inhibits saccades. For
example, these studies have reported delayed saccadic latencies in a gap task when spatial attention is
activated, even when the cue accurately predicts the target location[7,8,9]. According to Fischer and
colleagues, attention must first be disengaged before an eye movement can be made. Hence, even
attending to the target location should delay the eye movement to the target. Further, they argue that
the “gap” in a gap paradigm allows the subject to disengage spatial attention from the point of
fixation before making a saccade. Hence, there is less of an attentional cost in the uncued gap
paradigm. In addition, studies have reported that antisaccades are both slower and less accurate when
precued to attract attention[10,11].
In addition to these two approaches, there have been a number of other proposals. For example,
there are models that support the idea of a functional relationship between the two processes [12],
some that dispute a physiological relationship between them [13], and others that argue against any
specific attentional effects on saccades at all, either facilitatory or inhibitory [14]. In this last
framework, saccadic performance is largely a function of low-level perceptual representations and
the reciprocal inhibition between them. Attentional influences on eye movements are reduced to a
minimal level.
These inconsistencies in the literature might be resolved if more consistent, precise definitions of
spatial selective attention and saccadic eye movements were applied. Much work now supports a
dissociation between voluntary and reflexive saccades. For instance, Henik et al.[15] demonstrated
that patients with unilateral prefrontal lesions including the frontal eye fields showed longer latencies
to the contralesional visual field when performing a voluntary saccade task, but shorter latencies to
the contralesional field when performing a reflexive saccade task. Also, Machado and Rafal[16]
demonstrated a dissociation in the modulation of the fixation offset effect for voluntary and reflexive
saccades and suggested that this dissociation was supportive of neural activity changes in two
different parts of the brain. In addition to a dissociation in overt orienting, a similar distinction
between a voluntary (endogenous) and a reflexive (exogenous) process has been demonstrated with
respect to covert orienting (i.e., spatial attention[17]). Drawing from this large amount of evidence
suggesting that both eye movements (overt orienting) and spatial attention (covert orienting) can be
subdivided into two categories, voluntary and reflexive, Sereno[18] has proposed that systematically
distinguishing between voluntary and reflexive processes might clarify these issues.
A reflexive saccade is a seemingly automatic eye movement elicited by a target, such as in the
prosaccade task, where the subject must make a saccade to a sudden onset stimulus occurring in an
unpredictable location. Alternatively, voluntary saccades require an eye movement that is internally
generated. For example, in the antisaccade task, the subject must make an eye movement to a point in
the visual field opposite the stimulus, and thus suppress a reflexive prosaccade towards the stimulus.

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With respect to covert orienting, or shifts of spatial attention in the absence of eye movements, a
similar distinction between voluntary and reflexive processes can be made. The nature of the
attentional shift is determined by the method used to direct spatial attention. In a reflexive task, a
peripheral, exogenous cue (e.g., the brightening of a box) indicates the upcoming target location[12].
This is similar to reflexive prosaccades, because an actual sensory event is used to attract attention to
a position in the visual field. Facilitation effects occur very rapidly, within 50–100 ms after cue
onset[19]. In contrast, a voluntary attentional task involves the presentation of a symbolic cue (e.g.,
an arrow) at the central fixation point indicating where the upcoming target will most likely appear.
Similar to reflexive attention, voluntary cueing also benefits the detection of the upcoming target.
However, the task exhibits a much slower and less effective facilitation beginning only 200–300 ms
after cue onset[20,21].
Sereno[22] proposed a model of attention and eye movements that included separate reflexive
and voluntary components. Sereno's tonic-inhibition model of orienting asserted that separate neural
systems control voluntary and reflexive saccades (involving the frontal eye fields and the prefrontal
cortex, and the superior colliculus, respectively) and that the voluntary system plays a controlling
role with respect to the tonic inhibition of the reflexive system. Different lines of research have
suggested that the frontal eye fields play a controlling and inhibitory role with respect to the superior
colliculus, involving an indirect pathway through the caudate and substantia nigra pars
reticulata[23,24,25]. Voluntary control involves both the activation of voluntary processes as well as
perhaps an increase in inhibition of the reflexive eye movement system. Thus, Sereno's model
predicts that voluntary attention would affect voluntary and reflexive saccades differently. While
voluntary attention should facilitate voluntary saccades, it may also increase inhibition of the
reflexive system and hence slow reflexive saccades.
These predictions were tested in a preliminary investigation by Sereno[26]. The study
investigated the effects of voluntary spatial attention in both the prosaccade and the antisaccade
tasks. The cues were always valid. Subjects performed each condition (Prosaccade, Prosaccade-Cued,
Antisaccade, Antisaccade-Cued) in four separate blocks counterbalanced across subjects. Results
indicated that voluntary attentional cues affected voluntary and reflexive saccades differently. As
expected, spatial attention facilitated voluntary saccades (Table 1). However, there was a
nonsignificant trend suggesting voluntary attention inhibits reflexive saccades. The present study
attempts to expand on this preliminary study in order to clarify exactly how voluntary spatial
attention affects voluntary and reflexive eye movements and perhaps resolve inconsistencies in the
literature[1,6,12].
TABLE 1
Mean Response Times and (% Error) from Sereno[26]
Task Uncued Cued Uncued – Cued
Antisaccade
Prosaccade
361 (3.2%)
299 (0.2%)
329 (0.3)
314 (0.1)
32 msa (2.9%)
–15 msb (0.1%)
ap < 0.01; bp > 0.17
It is important to resolve the issues surrounding effects of voluntary attention on reflexive and
voluntary eye movements in order to better understand how covert and overt orienting mechanisms
interact. The present study investigated whether voluntary attention truly has different effects on
voluntary and reflexive saccades, and what conditions might modulate these effects. The first
experiment attempted to replicate the original experiment by Sereno[26], using the same four blocks

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of trials described previously. The second experiment investigated whether mixing cued and uncued
trials alters the results. The third experiment replaced previously uncued trials with a neutral cue to
control for alerting effects. The fourth experiment further explored the effects of fixation condition,
using neutral and directional cues.
EXPERIMENT 1

Methods
Subjects
Sixteen college students ranging between the ages 18 and 24 were tested as normal control subjects.
All subjects had normal or corrected vision.
Apparatus
Eye movements were recorded using a high-speed infrared sensitive camera interfaced with an
ISCAN RK-426 eye tracking system. Gaze position was converted to screen coordinates and
displayed on a second monitor to inform the experimenter, in real time, where the subject was
looking. Spatial resolution of the eye tracking system was approximately 0.5° of visual angle and
temporal resolution was set at 180 samples/second. Saccades were detected when eye velocity
exceeded 100°/second and ended when eye velocity fell below 12°/second.
Stimuli
Subjects placed their head on a chin rest positioned 72 cm from a computer monitor employed to
display the stimuli (Sony Trinitron Multiscan sf II, 17 in.). From this distance, the monitor screen
covered a visual area of 25° × 18°. The target appeared 7° to the left and right of a gray central
fixation point of 0.15° projected against a black background. The target was a white square 0.2° ×
0.2°.
Procedure
Subjects performed four blocks of trials, which were counterbalanced across subjects. These blocks
consisted of the following conditions: Prosaccade-No Cue, Prosaccade-Cued (100% valid),
Antisaccade-No Cue, Antisaccade-Cued (100% valid). Cues were always 100% predictive of saccade
direction when present. In each of the four conditions, subjects received 12 practice trials and 48
experimental trials (12 for each of the four delay intervals). Practice trials were not included in the
data analysis.
Prosaccade task — Each trial consisted of the following sequence: (1) a blank screen (black
background) with a gray central fixation point presented for 800 ms; (2) a variable delay of 400, 600,
800, or 1000 ms (to match the duration of the cue presentation, see below); (3) presentation of the
target accompanied by a brief audible tone. This target screen was terminated by either an eye
movement to the target (4), or by a failure to respond within 1000 ms of target onset. Following
either of these outcomes, a blank screen was presented for 500 ms and then the sequence was
repeated (see Fig. 1). All trials were presented in the overlap condition, where the cue or fixation
point remained on the screen when the target appeared. For the prosaccade task, correct saccades

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were defined as saccades directed towards the target that terminated within 4.4° of the target’s
position. All other saccades were classified as errors.

FIGURE 1. Prosaccade and Antisaccade Tasks. Schematic representation of a trial in the prosaccade task with no cue (panel A),
prosaccade task with cue (panel B), antisaccade task with no cue (panel C), and antisaccade task with cue (panel D), prosaccade task with
neutral cue (panel E), and antisaccade task with neutral cue (panel F). Each trial began with (1) the presentation of a fixation screen (a
blank screen with a gray central fixation point) presented for 800 ms, followed by (2) a variable delay with either a fixation point (tasks
with no cue, panels A and C), an arrow predictive of the upcoming eye movement (tasks with cue, panels B and D), or a neutral cue
(panels E and F); then (3) presentation of the target accompanied by a brief audible tone, (4) the long arrow illustrates the correct eye
movement response for the trial.
Antisaccade task — The antisaccade task was identical to the prosaccade task, except that the
subject was required to make an eye movement in the direction opposite the target stimulus. Correct
responses had to be within 4.4° of the screen position directly opposite the target location. All other
responses, in particular saccades to the target itself, were counted as errors.
Voluntary attention — Voluntary spatial attention was manipulated in both the prosaccade and
antisaccade tasks by presentation of a gray arrow cue at the central fixation point prior to the target
presentation, which always validly indicated the direction of the upcoming eye movement. Thus for
prosaccades, the arrow pointed towards the position where the target would appear, and for
antisaccades it pointed towards the location opposite the target. There was a delay interval of variable

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