Attention doesn't slide: spatiotopic updating after eye movements instantiates a new, discrete attentional locus.

Abstract

During natural vision, eye movements can drastically alter the retinotopic (eye-centered) coordinates of locations and objects, yet the spatiotopic (world-centered) percept remains stable. Maintaining visuospatial attention in spatiotopic coordinates requires updating of attentional representations following each eye movement. However, this updating is not instantaneous; attentional facilitation temporarily lingers at the previous retinotopic location after a saccade, a phenomenon known as the retinotopic attentional trace. At various times after a saccade, we probed attention at an intermediate location between the retinotopic and spatiotopic locations to determine whether a single locus of attentional facilitation slides progressively from the previous retinotopic location to the appropriate spatiotopic location, or whether retinotopic facilitation decays while a new, independent spatiotopic locus concurrently becomes active. Facilitation at the intermediate location was not significant at any time, suggesting that top-down attention can result in enhancement of discrete retinotopic and spatiotopic locations without passing through intermediate locations.

Full text

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Attention doesn’t slide: spatiotopic updating after eye
movements instantiates a new, discrete attentional locus
Julie D. Golomb & Alexandria C. Marino &
Marvin M. Chun & James A. Mazer
Published online: 2 December 2010
# Psychonomic Society, Inc. 2010
Abstract During natural vision, eye movements can
drastically alter the retinotopic (eye-centered) coordinates
of locations and objects, yet the spatiotopic (world-
centered) percept remains stable. Maintaining visuospatial
attention in spatiotopic coordinates requires updating of
attentional representations following each eye movement.
However, this updating is not instantaneous; attentional
facilitation temporarily lingers at the previous retinotopic
location after a saccade, a phenomenon known as the
retinotopic attentional trace. At various times after a
saccade, we probed attention at an intermediate location
between the retinotopic and spatiotopic locations to
determine whether a single locus of attentional facilitation
slides progressively from the previous retinotopic location
to the appropriate spatiotopic location, or whether retino-
topic facilitation decays while a new, independent spatio-
topic locus concurrently becomes active. Facilitation at the
intermediate location was not significant at any time,
suggesting that top-down attention can result in enhance-
ment of discrete retinotopic and spatiotopic locations
without passing through intermediate locations.
Keywords Retinotopic.Remapping.Eye-centered.
Reference frame.Coordinate systems.Saccades
Introduction
One of the most effective strategies for coping with
complex visual environments is deploying covert visuospatial
attention to salient objects and locations. When attention is
drawn to a location via either bottom-up (Posner, 1980) or
top-down (Awh, Jonides, & Reuter-Lorenz, 1998) signals,
visual processing is facilitated for stimuli appearing at the
attended location. In the everyday world, frequent saccadic
eye movements dramatically change retinal stimulation,
seriously challenging our ability to sustain attention on a
task-relevant location in the world. In fact, some studies have
concluded that it is not possible to maintain attention on one
spatial location while saccading to another (Deubel &
Schneider, 1996; Hoffman & Subramaniam, 1995; Kowler,
Anderson, Dosher, & Blaser, 1995). This deficiency is often
cited as evidence supporting the premotor theory (Rizzolatti,
Riggio, Dascola, & Umiltà, 1987), which hypothesizes that
attention is merely a by-product of oculomotor planning and
the very act of planning an eye movement precludes the
Electronic supplementary material The online version of this article
(doi:10.3758/s13414-010-0016-3) contains supplementary material,
which is available to authorized users.
J. D. Golomb (*):M. M. Chun:J. A. Mazer (*)
Interdepartmental Neuroscience Program, Yale University,
New Haven, CT, USA
e-mail: jgolomb@mit.edu
e-mail: james.mazer@yale.edu
A. C. Marino
Yale University School of Medicine,
New Haven, CT, USA
M. M. Chun:J. A. Mazer
Department of Psychology, Yale University,
New Haven, CT, USA
M. M. Chun:J. A. Mazer
Department of Neurobiology,
Yale University School of Medicine,
New Haven, CT, USA
Present Address:
J. D. Golomb
McGovern Institute for Brain Research,
Massachusetts Institute of Technology,
Cambridge, MA, USA
Atten Percept Psychophys (2011) 73:7–14
DOI 10.3758/s13414-010-0016-3

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ability to attend anywhere except the saccade target.
However, more recent studies have demonstrated that
attention and eye movements are dissociable (Awh,
Armstrong, & Moore, 2006; Hunt & Kingstone, 2003;
Juan, Shorter-Jacobi, & Schall, 2004), including a recent
article by Golomb, Chun, and Mazer (2008) suggesting
that the difficulty in sustaining attention at an external
location across saccades derives from challenges inherent
in updating spatiotopic (world-centered) representations,
not oculomotor planning itself.
The early stages of visual processing are retinotopically
organized; consequently, to maintain a spatiotopic locus of
attention, either retinotopic attentional representations must
be updated with each saccade, or attentional salience maps
must reside in higher, spatiotopically organized maps.
Golomb et al. (2008) demonstrated that visuospatial
attention is natively maintained in retinotopic coordinates
that can be dynamically updated with spatiotopic informa-
tion with each saccade. However, this updating is neither
automatic nor instantaneous. As a result, when attentional
facilitation has been sustained at a particular location before
a saccade, it lingers at that same retinotopic location for
some period of time after the saccade, even though the
saccade has rendered that location behaviorally irrelevant;
this phenomenon is termed the retinotopic attentional trace
(Golomb, Pulido, Albrecht, Chun, & Mazer, 2010).
Several characteristic features of the retinotopic attentional
trace have been described: It is maximal during the first
100 ms following a saccade, after which it decays (Golomb
et al., 2008); it can be revealed using reaction time (RT) and
behavioral accuracy techniques (Golomb et al., 2008), as
well as fMRI and ERP neuroimaging techniques (Golomb,
Nguyen-Phuc, Mazer, McCarthy, & Chun, 2010); it is robust
across several different types of attentional tasks (Golomb,
Nguyen-Phuc, et al., 2010; Golomb, Pulido, et al., 2010);
and it is specific to the retinotopic coordinate system—that
is, there is no analogous spatiotopic attentional trace
(Golomb et al., 2008). Interestingly, the decaying retinotopic
facilitation can temporarily coexist with emerging facilitation
at the task-relevant spatiotopic location (Golomb et al., 2008;
Golomb, Nguyen-Phuc, et al., 2010; Golomb, Pulido, et al.,
2010). However, the spatiotemporal dynamics of this
transition have not been explored: Does this phenomenon
reflect attention directed simultaneously toward two different
loci or a single locus of attention relocating position?
Figure 1 illustrates several models that could account for
the decaying retinotopic attentional trace and concurrent
updating to task-relevant spatiotopic coordinates. These
models are based on the idea that the native coordinate
system for spatial attention is retinotopic, and when
attention is sustained at a particular location in space,
neurons representing the relevant retinotopic location
become facilitated, increasing spontaneous firing rates
(Luck, Chelazzi, Hillyard, & Desimone, 1997), synchroni-
zation with neighboring neurons (Fries, Reynolds, Rorie, &
Desimone, 2001), and recurrent activity (Wang, 2001).
When attention is shifted to a new retinotopic location, the
recurrentarchitecture of the visualcortexprevents activityat the
previously relevant retinotopic location from instantaneously
returning to baseline firing levels, resulting in a temporary
retinotopicattentionaltrace.Therelevantquestionforthisreport
is how that attentional locus then transitions to the correct, task-
relevant spatiotopic location. One possibility is that the locus of
attention “slides” continuously across the map to the new
location (Fig. 1a). Another model involves a transient change
in shape of the locus, such that it temporarily enlarges to
contain both locations and then shrinks back to the new
relevant location (Fig. 1b). Both models involve a single locus
of attention that transitions from one location to another and
results in transient facilitation along the path between the two
locations. In contrast, a third type of model involves two
discrete attentional loci that independently emerge and decay
(Fig. 1c). Such a mechanism would be consistent with
A
B
C
No-Saccade Time after saccade
SR
I
C
Ci
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R
Ci
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Ci
C
S
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Ci
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SR
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Ci
SR
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Ci
Fig. 1 Possible models of attentional updating. Black square indicates
cued location; white dots and arrows indicate fixation and saccade
positions. In the no-saccade case, an attentional locus (white circle) is
deployed to the spatiotopic/retinotopic (SR) location of the cue. After
the eye movement, attention is initially directed at the retinotopic (R)
location and updates over time to occupy the correct spatiotopic (S)
location. The three models depict different possible spatiotemporal
dynamics of this transition. C, control location; I, intermediate
location; Ci, intermediate-control location. a A single locus of
attention slides progressively from retinotopic to spatiotopic locations.
b A single locus of attention transiently expands to include both
locations, then contracts back to the spatiotopic location. c The old
locus of attention decays at the retinotopic location while a new, discrete
locus of attention arises at the spatiotopic location
8Atten Percept Psychophys (2011) 73:7–14

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demonstrations that in the absence of saccades, attention can be
split between two locations without facilitating the area in
between (Awh, Anllo-Vento, & Hillyard, 2000; Irwin &
Gordon, 1998).
Thepresentarticleisprimarilyconcernedwithdifferentiating
the latter mechanism from the two former mechanisms by
probingattentionatanintermediatelocationpositionedbetween
the spatiotopic and retinotopic locations. As in the previous
studies (e.g., Golomb et al., 2008), subjects were instructed to
remember and sustain attention at a task-relevant spatiotopic
location while saccading to a different location; we then
probed attentional facilitation at several delays after the saccade
at the spatiotopic and retinotopic locations, as well as at the
intermediate location. Since previous work has demonstrated
that attention will update to spatiotopic coordinates only when
behaviorally relevant (Golomb et al., 2008), our task was
heavily biased toward the spatiotopic location. Thus the
present question is not whether attention will update in order
to maintain a spatiotopic representation, but how. If behavioral
facilitation emerges at the intermediate location at some point
after the saccade, that would suggest a single locus of attention
transitioning between the retinotopic and spatiotopic locations.
On the other hand, observing facilitation simultaneously at
both the spatiotopic and retinotopic locations, but not at the
intermediate location, would support the idea of two discrete
loci of attention.
A number of studies have explored how covert
attentional transitions from one location to another when
the eyes remain fixated and attention is shifted to a new
spatial location. Although a few studies have shown
evidence that facilitation passes through an intermediate
location (Shulman, Remington, & McLean, 1979) or
takes longer to “slide” across longer distances (Tsal,
1983), most reports have been more consistent with a
“jumping” model where attention arises at a new location
and diminishes at the old location (reviewed in Cave &
Bichot, 1999; Chastain, 1992a, 1992b; Sperling &
Weichselgartner, 1995; Yantis, 1988). In the context of
saccadic updating or “remapping” in the absence of
sustained attention (Duhamel, Colby, & Goldberg, 1992),
a few studies have also investigated visual or neuronal
sensitivity at intermediate locations, with mixed results. A
recent psychophysical study showed evidence for transient
effects at intermediate spatial locations, suggesting a
spreading or shifting of activity (Melcher, 2007). However,
neurophysiological evidence suggests otherwise; in certain
brain areas, visual responses are found in the original
receptive field and the remapped receptive field, but not
along the path in between (Sommer & Wurtz, 2006).
Because sustained and transient attention may engage
different neural mechanisms (Corbetta & Shulman, 2002),
and attentional updating seems to operate on a different
timescale than does traditional remapping (Golomb et al.,
2008; cf. Kusunoki & Goldberg, 2003), it is important to
investigate how these updating dynamics evolve in the case
of sustained visuospatial attention.
Method
Subjects Twenty subjects participated in the main saccade
task, and 18 subjects in the no-saccade control. Additional
details about subjects and participation criteria are reported
in the online Supplement.
Experimental setup Stimuli were generated on a Macintosh
G4 computer using the Psychtoolbox extension (Brainard,
1997) for MATLAB (The Mathworks, Natick, MA) and
were presented on a 22-in. flat-screen CRT monitor.
Subjects were seated at a chinrest 75 cm from the monitor.
Eye position was monitored using an ISCAN eye-tracking
system (ISCAN, Burlington, MA) recording pupil and
corneal reflection position at 60 Hz.
Task and stimuli The task (Fig. 2) was modified from
Golomb et al (2008). Subjects initiated the trial by fixating
on a dot that appeared at one of four possible fixation
locations (arranged as the corners of an 8.3° × 8.3° square).
After 500 ms, a square memory cue appeared. Subjects
were instructed to covertly attend to the location of the
memory cue and to remember its location in spatiotopic
coordinates (absolute location) throughout the trial. After
200 ms, the memory cue was removed, and subjects
continued fixating for 500 ms. The fixation dot then moved
to a different fixation location, and subjects had 350 ms to
execute a single accurate saccade and fixate this new
location (while still attending/remembering the spatiotopic
location of the memory cue).
Once fixation was acquired at the new location, a probe
stimulus appeared after a delay of 50, 250, or 400 ms. The
probe was presented for 200 ms before being extinguished.
The probe was a thin bar angled 45° to the left or right of
vertical; subjects were instructed to report the orientation of
the tilt (left or right) as quickly as possible by pressing one of
two keypad buttons. The probe could appear at the task-
relevant spatiotopic location of the cue, the retinotopic
location of the cue, or a control location matched for visual
eccentricity and spatial uncertainty. Probes could also appear
at a location intermediate to the spatiotopic and retinotopic
locations. Because this intermediate location was necessarily
located at a shorter eccentricity from fixation, an additional
intermediate-controlprobe locationwas includedtomatchthe
eccentricity of the intermediate location.
After subjects reported the probe orientation, a memory
test stimulus appeared, and subjects indicated whether it
occupied exactly the same spatiotopic position as the
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memory cue. The difficulty of the memory task was adjusted
using a staircase procedure to maintain performance around
75% correct (Golomb et al., 2008); this ensured that the
memory task was challenging enough that subjects would
actively maintain the spatiotopic location in working
memory.
Each block of trials included 6 spatiotopic trials and 2
each of retinotopic, control, intermediate, and intermediate-
control trials, for each of the three delays (total of 42 trials
per block). As in previous studies (Golomb et al., 2008),
this greater likelihood of spatiotopic probes served to
further encourage subjects to maintain attention in
spatiotopic coordinates. Probe delays, probe locations,
and saccade directions (horizontal, vertical, and diagonal)
were randomly intermixed and unpredictable. For each
trial, fixation and cue positions were chosen at random
from a list of possible configurations for the specified
condition. If a trial was aborted due to a fixation break
(greater than 2° deviation), subjects received an error
signal, and the trial was repeated later in the same block
with new positions chosen at random for the same delay
and location. Subjects completed at least 18 blocks of the
task, spread across two to three sessions on multiple
days, for a total of at least 36 trials per condition (delay ×
position).
In separate experimental sessions, a no-saccade version
of this task was also run in order to assess the degree of
facilitation at the intermediate location in the absence of
a saccade. This task was identical to the saccade task,
except that the fixation dot never moved from its original
location. Probes were presented at the same delays as in
the saccade task, relative to the average saccade
completion time. Probes could appear at the spatiotopic
location (which was also the retinotopic location, since
the eyes never moved), as well as at locations corresponding
to the control, intermediate, and intermediate-control
locations.
Analysis of attentional facilitation RT for the probe
orientation report was averaged separately for each subject,
location, and delay and was submitted to random effects
analyses. Trials on which the subject responded incorrectly
(4.2% of the trials) or RT was greater than 1.5 s (1.8% of
the trials) were excluded. Spatiotopic facilitation and
retinotopic facilitation were calculated as the difference in
RT when the probe appeared at the spatiotopic or
retinotopic location, respectively, as compared with the
control location; intermediate facilitation was calculated
relative to the intermediate-control location. Bonferroni-
corrected one-sample, two-tailed ttests were conducted at
each delay to test whether spatiotopic, retinotopic, and
intermediate facilitation were significantly greater than
zero, indicating significantly shorter RTs than on control
trials.
500ms
~250ms
500ms
200ms
50-400ms
200ms
750ms
Time
Fixate
Memory
Cue
Fixate
Probe:
L/R tilt?
Wait
Saccade
Memory Test:
Same Location?
Probe
Delay
Control
Retinotopic
Spatiotopic
IntermediateIntermediate-Control
Fig. 2 Task: Example trial. Subjects maintained fixation on the white
fixation dot, while a memory cue appeared briefly at another location.
Subjects were instructed toholdthis cuedlocation inmemory throughout
the trial. The fixation dot then moved, and after completion of a saccade
to the new fixation location, a probe stimulus (oriented bar) appeared
after a variable delay (shown here in the control location; a schematic of
all five locations is shown in the inset at bottom). Subjects made a
buttonpress response to indicate probe orientation. A memory test
stimulus then appeared, and subjects indicated whether it occupied the
same spatiotopic location as the memory cue. Gray arrow indicating a
saccade did not actually appear on screen. The stimulus configuration
illustrated here represents one example cue–saccade configuration;
configurations were randomly intermixed from the four possible fixation
locations and nine possible stimulus locations
10Atten Percept Psychophys (2011) 73:7–14

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Results
Attentional facilitation at the spatiotopic, retinotopic, and
intermediate locations is plotted across delays in Fig. 3a.
Facilitationat the previouslyrelevant, but currently irrelevant,
retinotopic location of the cue was significant at the early
delay, t(19) = 4.14, p = .001, but not at the middle, t(19) =
1.93, p = .069, or later, t(19) = 1.45, p = .163, delays.
(Significance of multiple comparison tests was Bonferroni
corrected, α = .05/9 = .006.) The decay of the task-irrelevant
retinotopic attentional trace was accompanied by an increase
in task-relevant spatiotopic facilitation. Spatiotopic facilita-
tion was significant at the middle, t(19) = 3.08, p = .006, and
later, t(19) = 4.15, p = .001, delays, but not at the early delay,
t(19) = 1.32, p = .204. This pattern of task-irrelevant
retinotopic facilitation dominating immediately after a
saccade and task-relevant spatiotopic facilitation dominating
later closely replicates the original Golomb et al (2008; e.g.,
Fig. 4b) findings.
The critical question for the present study was whether
facilitationwaspresentattheintermediatelocationduringthis
transition. Facilitation was not significant at the intermediate
location at any of the timepoints tested (early, t(19) = 1.89,
p = .075; middle, t(19) = 0.75, p = .465; late, t(19) = 1.97,
p = .064). Although none of these timepoints were
significant, particularly after Bonferroni correction, it is
possible that some low level of facilitation existed at this
location, perhaps due to residual spatial spread from the
focus of attention (Downing & Pinker, 1985). The results
from the no-saccade control task were consistent with this
idea: The intermediate location exhibited a small benefit, as
compared with the intermediate-control location (Fig. 3b),
although this did not reach significance, t(17) = 1.95, p =
.07. Importantly, whatever small numerical benefit existed
for the intermediate location after a saccade was steady over
time and never exceeded that for the intermediate location in
the absence of any eye movements.
Discussion
The present results replicate earlier descriptions of the
retinotopic attentional trace: Even when the retinotopic
location is not task relevant, attentional facilitation is
strongest at the retinotopic location of the cue immediately
after the saccade and then decays, leaving only task-relevant
spatiotopic facilitation at later delays (Golomb et al., 2008;
Golomb, Nguyen-Phuc, et al., 2010). The present study
probed an intermediate location between the spatiotopic and
retinotopic locations to determine whether a single locus of
RT Difference (ms)
Probe Delays (ms after saccade completion)
50250 400
0
5
10
15
20
25
30
Spatiotopic
Intermediate
Retinotopic
Spatiotopic/Retinotopic
Intermediate
0
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No Saccade
35
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A
B
∗
∗
∗
∗
Fig. 3 Attentional facilitation results. Attentional facilitation is plotted
as the difference in reaction time (RT) for probes appearing in the
spatiotopic, retinotopic, and intermediate locations, as compared with the
controlandintermediate-controllocationbaselines(zero).Positivevalues
indicate attentional facilitation (RTs shorter than those at the control
locations). a Attentional facilitation after saccade (n = 20); data are
plotted as a function of probe delay. b Attentional facilitation in no-
saccade task (n = 18). Insets illustrate sample probe locations colored
according to the plot legends, with white indicating the control location.
Intermediate and intermediate-control locations are shown as hashed
lines. White and gray dots indicate final and previous fixation locations,
respectively; a square indicates the cued location, and an arrow
indicates the saccade. Error bars are standard errors of the means
(SEMs); asterisks indicate facilitation significantly greater than zero
(Bonferroni-corrected). The dashed gray line indicates baseline facili-
tation at the intermediate location in the no-saccade task; intermediate
facilitation after the saccade never exceeded this baseline
Atten Percept Psychophys (2011) 73:7–1411