Running head: INHIBITION OF RETURN IN SACCADIC SEQUENCES
Just Passing Through? Inhibition of Return in Saccadic Sequences
W. Joseph MacInnes12, Hannah M. Krüger13 and Amelia R. Hunt1
1. University of Aberdeen
School of Psychology
William Guild Building
Kings College
Old Aberdeen
AB24 3FX
2. Higher School of Economics (HSE)
Faculty of Psychology
Moscow, Russian Federation
3. Centre Attention and Vision
Laboratoire Psychologie de la Perception
Université Paris Descartes, Paris, France
Corresponding Author:
Dr. W. Joseph MacInnes
Assistant Professor, HSE
j.macInnes@abdn.ac.uk
+7 (495) 709-65-70
Dr. Amelia R. Hunt
Senior Lecturer
a.hunt@abdn.ac.uk
+44 (0)1224 273139
Dr. Hannah M. Krüger
Post Doctoral Researcher
Hannah.kruger@parisdescartes.fr
+33(0)1.42.86.21.99
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Abstract
Responses tend to be slower to previously fixated spatial locations, an effect known as
Inhibition of Return (IOR). Saccades cannot be assumed to be independent, however, and
saccade sequences programmed in parallel differ from independent eye movements. We
measured the speed of both saccadic and manual responses to probes appearing in previouslyfixated locations when those locations were fixated as part of either parallel or independent
saccade sequences. Saccadic IOR was observed in independent but not parallel saccade
sequences, while manual IOR was present in both parallel and independent sequence types.
Saccadic IOR was also short-lived, and dissipated with delays of more than ~1500ms
between the intermediate fixation and the probe onset. The results confirm that the
characteristics of IOR depend critically on the response modality used for measuring it, with
saccadic and manual responses giving rise to motor and attentional forms of IOR,
respectively. Saccadic IOR is relatively short lived and is not observed at intermediate
locations of parallel saccade sequences, while attentional IOR is long-lasting and consistent
for all sequence types.
Keywords: Visual attention, visual search, inhibition of return, saccadic sequences
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When a location in space is cued, responses to targets appearing in the cued location
are speeded relative to control locations. This is thought to occur because attention has been
drawn to the location of the cue, facilitating processing of subsequent information appearing
in the same location. When the time delay between the onset of the cue and the onset of the
target exceeds 200-300ms, however, the effect of the cue reverses, with slower responses to
the cued location relative to un-cued locations, and this effect has been termed Inhibition of
Return (IOR, Posner & Cohen, 1984). It has been argued that IOR reflects a mechanism that
inhibits attention from returning to locations in order to facilitate shifts of attention to novel
locations (see Klein, 2000 for a review).
IOR is typically tested with simple cues to the left and right, and a return back to
fixation prior to probe onset. However, it is rarely the case that in free visual search a single
saccade is enough to detect a target and sequences of two or more saccades are common.
These sequences of saccades can be broadly categorised into two different types: those that
are planned independently and serially, and those that are planned in parallel. In an
independent sequence, each saccade is programmed and executed to a discrete, single target.
In a parallel sequence, multiple fixations are steps on a path to a single target. Intuitively it
may seem that the best strategy in visual search would be to operate entirely with
independent saccade sequences, so that each saccade goal is individually fixated and
inspected. However, parallel programming of saccades (e.g. Becker & Juergens, 1979) is
common in reading (Morrison, 1984) and also comprise a substantial subset of visual search
saccade sequences (Findlay, Brown & Gilchrist, 2001; McPeek, Skavenski & Nakayama,
2000). Parallel sequences differ from independent sequences in a number of respects.
Parallel saccade sequences have longer primary saccadic latency than saccadic latencies in an
independent sequence and this latency is positively correlated with the number of future
targets (Inhoff, 1986; Zingale & Kowler, 1987, but see Crawford, 1991). Furthermore,
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subjects have difficulty changing saccadic vectors to targets in the middle of parallel
sequences (De Vries, Hooge &Verstraten, 2014) and longer intermediate saccadic latencies
result when they do (McPeek & Keller, 2001). Parallel sequences of saccades have also been
shown to interact with saccadic compression. Compression is the mislocalisation of a spatial
probe towards the saccade target when the probe is flashed in the brief time interval around
the saccade onset (Ross, Morrone & Burr, 1997). Lavergne, Dore- Mazars, Lappe, Lemoine
& Vergilino-Perez (2012) demonstrate that localization prior to the initial saccade in parallel
sequences is influenced by both saccade targets.
Attention has been shown to be automatically and obligatorily allocated to the goal of
an impending single saccade (e.g. Hoffman & Subramanian, 1995; Deubel, Bridgeman &
Schneider, 1996). This finding has been taken as evidence in favour of a coupling of attention
and goal selection, and/or a coupling of attention and saccade planning. Consistent with
attention being linked to saccade planning, perceptual benefits associated with attention have
been observed at all saccade targets in a sequence of saccades, not just at the final location in
the sequence (e.g. Baldauf & Deubel, 2008; Gersch, Schnitzer, Sanghvi, Doscher& Kowler,
2006; Godijn & Theeuwes, 2003) but only when sequence targets are marked by features
such as colour (Gersch, Kowler, Schnitzer & Dosher, 2009). For example, Godijn and
Theeuwes (2003) used a letter identification task prior to a parallel sequence of saccades.
Letter discrimination was better at the first fixation location than the second, but both showed
better discrimination than control locations. Other findings show improved contrast detection
thresholds at the current fixation and at an intermediate saccade target (Gersch, Kowler, &
Dosher, 2004; Gersch et al., 2006) but not the final target location. A difference in the timing
of attention probes could explain the discrepancy here; attention may be allocated to all target
locations prior to execution, but during the sequence, only the current fixation and the next
location in the sequence are attended.
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If indeed all locations in a saccade sequence are attended equivalently, one might
expect IOR to be observed at intermediate locations even for pre-planned sequences of eye
movements. On the other hand, an interesting inference that can be drawn from the above is
that, even though intermediate locations along a planned path are attended, it would be
difficult to change the planned vectors once the parallel sequence of saccades has begun.
Presumably, even if a target were detected at an intermediate location in a sequence of
saccades, the eyes would normally complete the parallel sequence before returning to the
previously-visited location. For inhibitory tags to be functional, intermediate fixations along a
planned path should not be inhibited, so that they can be revisited if a target is detected there
en route. An important factor in determining whether a previously-fixated location is
revisited may be whether or not that location was an intermediate location in a parallel
sequence.
In order to test our hypothesis, we contrasted two tasks. Participants were instructed
with a verbal cue to move their eyes to two locations on the display and respond to a target
that could appear in one of two locations: either the intermediate saccade sequence location
or a control location that was equidistant but not previously fixated. In the parallel condition
the locations of both targets in the sequence were visible before the first eye movement,
allowing for pre-planning of both saccades in the sequence. In the independent condition the
final saccade target was only revealed after the participant initiated a saccade to the
intermediate location, forcing participants to plan and execute the two saccades serially. If
IOR is sensitive to the context in which a location is fixated, we expect IOR to be observed at
the intermediate location when saccades in a sequence were independent. When sequences
are parallel, however, we expect the magnitude of IOR to be reduced or eliminated.
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Experiment 1: Saccadic Responses
Method
Participants
Ten participants with normal or corrected to normal vision (6 female, average age 25)
were recruited from students and staff at Aberdeen University and were paid £5 per hour for
their time. All three experiments of the study were approved by University of Aberdeen
ethics committee and all participants provided informed consent.
Apparatus
Experiments were run on a Macintosh PC with 3Ghz quad core processor and 6GB
ram running OS 10.6.4 and a 20” CRT monitor at 1024 x 768 resolution and 120 Hz. Eye
position was monitored with an Eyelink 1000 (SR research, Mississauga, Canada). The
experiment was controlled through Matlab R2009b using Psych toolbox version 3.0.8
(Brainard, 1997).
Stimuli and Procedure
Each participant contributed 264 trials over two blocks during the 50 minute
experiment. The first 15 trials per block were excluded as practice and a further 10% were
catch trials where no probe was presented leaving 210 trials available for analysis. The
participant’s task was to make two saccades and then make a third, speeded saccade to a
visual probe. Trials were initiated by the participant with a space bar press which triggered
an Eyelink drift correction. Participants were then presented with a central fixation dot
surrounded by six marked locations (disks with a 1˚ diameter) equally spaced as if on a circle
of 4˚ radius from the fixation (see Figure 1 for layout and timing). In each trial, three of six
locations were randomly chosen with the caveat that no two would be adjacent. These three
locations were randomly assigned as final saccade location, intermediate saccade location and
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Figure 1. Spatial and temporal properties of the experiment design. The timeline at
the top shows the sequence and timing for all experiment conditions. The layout for (A)
parallel and (B) independent sequences were different prior to the onset of the first saccade
but identical from that point on. Both had equivalent onsets (50% black mask) in mid
saccade. Manual and saccadic experiments were identical except for the modality of the
response.
control location. Each of these locations was further randomly assigned one of the colours
red, green or blue. In parallel sequence trials, all three of the assigned colours were visible at
the start of the trial. In independent sequence trials only the colour for the intermediate
location was visible. Background was uniform grey and all non-coloured locations remained
black throughout the experiment. Randomization meant all six locations and three colours
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were equally likely as the intermediate saccade location, with the final saccade location being
clockwise or counter-clockwise by two locations. The control location was always equidistant
in the opposite direction. Each participant did one block of parallel saccade sequences and
one block of independent saccade sequence, with order alternating between subjects.
All trials began with a 500 ms delay followed by verbal cues announcing the colours
of the first and second saccade location, for example “blue”, “red”. Participants were
instructed not to begin their first saccade until the central fixation was removed. The central
fixation was removed 1500 ms into the trial and participants were given an error tone for
moving early.
During independent sequences, each trial started with the colour of the initial saccade
target visible, but the colour of all other potential saccade targets was hidden. Our methods
required that these locations reveal their colour after the onset of the first saccade so that
planning and execution of the saccade to the second location could begin only after the first
saccade had finished. We timed this colour change to coincide with the eye movement to
minimize the possibility that it would attract attention, but to further equate the conditions we
also used partial masks in both parallel and independent conditions, as follows. In
independent trials, upon detection of a saccade toward the first cued location, colours for both
hidden potential locations were revealed to show their target colour, but with 50% of the
surface covered by a black mask. In both parallel and independent trials, any location whose
colour was initially visible also received a black mask covering 50% of the surface. The end
result was all three locations in both parallel and independent conditions receiving a 50%
surface change in luminance in mid saccade, and the final locations being a 50% mask/colour
blend. The use of these masks meant that any local transients due to colour onsets were
matched across parallel and independent conditions.
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A random time (500 to 1300 ms) after landing at the second cued location, a probe (a
white cross of .66˚ in the centre of the location) was presented at either the intermediate
location or the alternate control location with equal probability. Ten percent of trials were
catch trials and had no probe. Participants were instructed to respond as quickly and
accurately as possible to the probe location by moving their eyes to that location.
Responses before the probe or on a catch trial received an error tone as feedback. All
potential locations were circles extending 1.0˚ diameter and any saccade within 1.5˚ radius of
its centre was considered a ‘hit’ of that location. Saccadic onset events were defined by the
Eyelink default threshold settings of 40˚/s velocity and 8000˚/s2 acceleration.
Results and Discussion
Trials were excluded from analysis if the participant blinked (2.1% of trials), or was
not able to maintain fixation (that is, remain within 1.5˚ of screen centre) prior to removal of
fixation (12.5%). One participant was removed from the analysis for having over 50%
exclusions on these bases. Participants did not respond to any catch trials. Other exclusions
were trials with saccadic reaction times (SRT) of less than 100ms (0.2%), or greater than
three standard deviations from the mean (1.8%), and trials during which any fixation landed
within 1.5˚ of the alternate location (1.6%) or failed to reach a target in a single saccade
(1.8%).
Data were collapsed across the six locations, three location colours and two saccade
directions from the intermediate location (clockwise and counter clockwise). Because we
were interested in the time course of IOR, we included the fixation-probe onset asynchrony
(FPOA) as a factor in the analysis. We measured probe onset time from the fixation onset of
the intermediate location because this best represents the interval from the time the inhibition
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would have been applied to that location to the time when the probe appeared, analogous to
the cue-target interval in more conventional cue-target paradigms.
Saccadic reaction time (SRT) was defined as the saccade onset latency timed from the
onset of the probe and was analyzed with a linear mixed effects (lmer) model in the R
statistical package. Linear mixed effects modelling allows for any combination of random
and fixed effects in a single model. In addition, they provide an intuitive approach to
continuous variables in the analysis and figures which provides a richer representation of the
data as compared to median splits (Bayaan, Davidson & Bates, 2008). IOR (intermediate,
control) and Sequence (parallel, independent) were included as fixed effects and Participant
and FPOA (a continuous factor) as random effects. The significance of each effect was
determined by comparing the model with and without main effects or interactions to see if its
inclusion improved the model as measured by a Chi squared (2) test.
We observed a main effect of IOR (2 (1) = 26.2, p < .001) with slower SRT to
intermediate locations than to control locations. This classic IOR effect interacted separately
with Sequence (2 (1) = 4.0, p < .05) and FPOA (2 (1) = 10.5, p < .01). Planned comparison
confirmed what is evident in Figure 2a, that the interaction of Sequence and IOR was caused
by a significant IOR effect (32ms) for probes appearing in the intermediate location in
independent sequences (t (9) = 3.5, p < .01). IOR in the intermediate location in parallel
sequences was not significant in a paired t-test (t (9) = 1.4). IOR was also observed at
intermediate locations for early probes (less than 1500 ms after landing at the intermediate
saccade location; 32 ms IOR (t (9) = 3.9, p < .01) but not for late probes (those presented
more than 1500 ms after landing; 10 ms IOR t (9) = 1.7, p < .13)) and this difference
disappeared at the latest times as seen in Figure 2. No three way interaction was observed (F
< 1), suggesting the data are better explained by the separate two-way interactions when the
model includes the variances from all factors.
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Figure 2. Saccadic Reaction times for E1 showing separate interactions of a) IOR
and sequence type and b) IOR and fixation-probe onset asynchrony. Error bars represent
Fischer’s Least Significant Difference.
Fixation durations at the intermediate location were measured to see if longer dwell
times in independent sequences could explain why we only observed IOR in the independent
condition. If independent sequences had longer dwell times, then perhaps they were better
attended, leading to the inhibition. However, there was no difference in total dwell time at the
intermediate location between parallel and independent sequences (t (9) < 1.0). Participants
would occasionally make a number of small fixational saccades at this intermediate location
(mean of 1.3) before progressing to the second location, so we compared the length of the
first fixation duration, the number of fixational saccades (< 1˚), and the total dwell time at the
intermediate location. There were no differences in any of these measures between parallel
and independent sequences (all t (9) < 1.0). The inhibitory cost at intermediate locations for
short probe onsets also remained significant when only trials where the intermediate location
had a single fixation were included in the analysis (i.e. even when no additional fixational
saccades were made) (t (9) = 3.45, p < .01).
The failure to find differences between serial and parallel conditions in terms of
fixation behaviour at the intermediate location may initially seem to contradict previous
reports described in the introduction, in which the shorter-duration fixations at intermediate
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locations are taken as a hallmark of saccade planning (e.g. McPeek et al., 2000; Findlay et al.,
2001). However, it is important to note that in our experiment the participant had to wait for
1500ms after the first target was revealed before beginning the sequence of saccades in both
conditions, which could have minimized later differences in the temporal dynamics of the
fixation behaviour. Another relevant difference in our experiment relative to previous ones is
that here the intermediate location was explicitly pre-defined as a saccade target, and was not
an erroneous saccade to a distractor as it was in the previous studies mentioned above, which
could have caused participants to fixate it for longer. The fact that we found clear differences
in IOR between the serial and parallel conditions is in itself reasonable evidence that
participants did, in fact, plan their saccade path differently under the two conditions.
These results demonstrate that saccadic IOR is absent or masked at intermediate
fixations along a parallel sequence of saccades. We observed robust IOR when the conditions
were the same except the second saccade in the sequence could not be planned in advance,
providing clear evidence that parallel-planning was the key factor in reducing IOR. The IOR
we observed was short-lived and was no longer significant at late onsets.
Experiment 2: Manual Responses
IOR can be measured using saccadic responses, as it was in Experiment 1, but it is
also frequently measured using manual responses (i.e., pressing a button to indicate that the
target has appeared). IOR has different characteristics depending on which response modality
is used (Hunt & Kingstone, 2003; Taylor & Klein, 2000). IOR for saccadic responses has
been modelled in terms of short-term cue-related changes in the responses of sensory and
motor neurons in the superficial and intermediate layers of the superior colliculus (SC), a
subcortical structure associated with the generation of eye movements (e.g. Satel, Wang,
Trappenberg & Klein, 2011). Consistent with this, saccadic IOR (but not manual IOR)
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interacts with the effects of fixation offset (Hunt & Kingstone, 2003), which is also thought
to arise from activity in the SC. In contrast, IOR as measured by manual responses has been
associated with an “attentional” form of IOR, that is, an impediment in shifts of attention to
previously-visited locations, with a locus in cortical areas linked with attention and
perception (Klein, 2000 review). Consistent with this, manual IOR (but not saccadic IOR)
interacts with target luminance (Hunt and Kingstone, 2003; Reuter-Lorenz, Jha and
Rosenquist, 1996). Thus multiple sources of IOR may exist in parallel, and response modality
is one way of dissociating them.
Given the dissociation between saccadic and manual IOR, it is reasonable to ask
whether the results from Experiment 1 would extend to manual responses. Since attention is
allocated in parallel to all saccade targets prior to execution (Baldauf & Deubel, 2008),
attentional inhibition, as measured by manual responses to probes, may exist for both
sequence types. Attentional IOR has also been shown to be long lasting (3200ms for manual
responses; Samual & Kat, 2003 and at least 1500ms for saccadic responses; Klein, 2000) and
have late onset depending on the complexity of the task (Lupianez, Milliken, Solano, Weaver
& Tipper, 2001). We therefore examined the effect of parallel planning on IOR for manual
responses in this experiment, using a variety of saccade target intervals (STI) ranging from
500 to 1700 ms.
Method
Participants
Twenty-two participants (15 female, average age 23) participated in this experiment
and were reimbursed £5 for their time.
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Apparatus, Stimuli and Procedures
Experiment 2 was identical to Experiment 1 except that participants were instructed to
make a button press upon target detection. In addition, the first group (N = 12) of our
participants were run with probe onset times that matched Experiment 1 (500-1300ms).
There were no significant effects of FPOA on manual IOR, but we were concerned that the
later onset of manual responses relative to saccadic responses could be responsible for the
difference between the two experiments. We therefore decided to change the range of probe
onsets to 900-1700ms for the remaining participants (N=10). This also had the benefit of
providing a better match for manual IOR in similar designs (e.g., Taylor and Klein (2000)
measured IOR at 1000 ms probe onset). FPOA had no effect in this group of participants
either, so in the subsequent analyses, data from both groups of participants were combined to
maximize power, with FPOA as a continuous variable as measured from the onset of the
fixation at the intermediate location.
Results & Discussion
Trials were excluded if the participant blinked (2.1% of trials) or was not able to
maintain fixation (that is, remain within 1.5˚ of screen centre) prior to its removal (16%).
Catch trials were also excluded from analysis and responses were made to 0.1% of these.
Other exclusions were manual reaction times (MRT) of less than 100ms (0.1%), or more than
three standard deviations from the mean (1.0%), trials during which any fixation landed
within 1.5˚ of the alternate location (3.0%) or failed to reach a target (1.5%).)
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Figure 3. Manual reaction times for E2. Only the main effect of IOR was significant
and it did not interact with any other factors. The graph is split by planning condition for
comparison to SRT data only. Error bars represent Fischer’s Least Significant Difference.
A mixed-effects model was conducted with subject and FPOA as random effects and
IOR (intermediate, control) and Sequence (parallel, independent) as fixed effects. The model
was optimized as described above and showed a main effect of IOR (2 (1) = 10.1, p < .001)
with a 13 ms cost to probes at the intermediate location. We observed a main effect of FPOA
((2 (1) = 4.1, p < .05) with late onsets having slower response times, and a significant effect
of Sequence (2 (1) = 4.3, p < .05) with responses following independent sequences 7 ms
faster than parallel. IOR did not interact with any factors (all F < 1.0). These results suggest
that IOR, as measured by manual responses to probes, is observed at intermediate locations
along the saccade path irrespective of whether or not the sequence of saccades was preplanned in parallel or had to be planned and executed serially.
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Experiment 3: Mixed Responses
The above experiments taken together suggest a different effect of saccade planning
for IOR measured by saccadic and manual responses. A different time course for IOR effects
as measured by the two response modalities was also evident. In a final experiment, we
sought to replicate these two effects within the same study, and within the same group of
participants, to allow for a more direct and powerful comparison of IOR across modality.
Method
Participants
Eleven participants (6 female, average age 21) participated in this experiment and
were reimbursed £5 for their time.
Apparatus, Stimuli and Procedures
Experiment 3 was identical to earlier experiments except each participant contributed
four blocks, two each of manual and saccadic responses, to allow for a within-subject
comparison of response modality. Probe onset time was either 750 or 1150 ms after the end
of the second saccade.
Results & Discussion
Trials were excluded if the participant blinked (3.9%) or was not able to maintain
fixation (1.5˚) prior to its removal (7.6%). Catch trials were also excluded from analysis and
responses were made to 0.1% of these. Other exclusions were manual reaction times (MRT)
of less than 100ms (0.2%) or more than three standard deviations from the mean (0.9%), and
trials during which any fixation landed within 1.5˚ of the alternate location (2.0%) or failed to
reach a target or probe location in a single saccade (9.1%).
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First, to replicate the analyses of previous experiments, a mixed-effects model was
conducted separately for manual and saccadic responses with subject and probe onset time
(as measured from the intermediate location) as random effects and IOR (intermediate,
control) and Sequence (parallel, independent) as fixed effects. Probe onset time was triggered
at either 750ms and 1150ms after completion the saccade to the second location, but as in the
previous two experiments, our fixation-probe onset asynchrony (FPOA) variable for the
analysis was the duration between the start of the fixation on the intermediate location and
the onset of the probe. FPOA was therefore treated as a continuous variable in the linear
effects model.
For saccadic responses, there were main effects of IOR (2 (1) = 4.4, p < .05) with
responses to intermediate locations 13 ms slower than control, and FPOA (2 (1) = 10.7, p <
.01) with reaction times slowed for late probe onsets (note that this is opposite to the results
from Experiment 1, but consistent with the results from Experiment 2). FPOA interacted
with Sequence (2 (1) = 11.5, p < .001) and there was a three-way interaction between FPOA,
IOR and Sequence (2 (1) = 6.2, p < .05). To analyse this further, we examined the FPOA by
saccadic IOR interaction for independent and parallel sequences separately: For independent
sequences, IOR was significant for early target onsets t (10) = 3.2, p < .01), but not later
target onsets (t (10) = 0.5) reflecting the presence of IOR for early but not late probe onsets.
No IOR was observed for parallel sequences (early target onsets t (10) = 0.4), late target
onsets (t (10) = 2.0) with the latter being a non significant trend toward cuing, not inhibition.
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Figure 4. Graphs depicting IOR for increasing fixation-probe onset asynchrony
(FPOA) following the intermediate saccade (X axis) for manual/saccadic responses and
parallel/ independent sequences. IOR was observed across all conditions for manual
responses (A); there was no interaction with sequence type or FPOA and the manual data is
split by sequence type for comparison only. For saccadic responses, IOR was not observed
for parallel sequences (B) and observed only for early onsets in independent sequences (C).
Error bar shading represents 95% confidence interval for the linear approximation.
For manual responses, we observed slower responses to late onsets (2 (1) = 12.4, p <
.001) and slower responses in independent sequences (2 (1) = 22.7, p < .001). Consistent
with Experiment 2, IOR was significant (2 (1) = 7.2, p < .01), and did not interact with either
FPOA (F=1.9), Sequence type (F < 1.0) or the two together (F < 1.0).
A mixed model of the full data set (E3 manual and saccadic responses) was run as a
direct test for an IOR interaction with response modality. The main effect of IOR remained
significant (2 (1) = 9.5, p < .01) and the expected four way interaction (IOR, Sequence,
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FPOA and Modality) was also significant (2 (1) = 6.6, p < .01), confirming the pattern
described above for the two response modalities: saccadic IOR is only observed for
independent sequences and early probes, but manual IOR is observed across sequence types
and probe onset times.
General Discussion
The results demonstrate that saccades to a previously-fixated location are inhibited
only when that location was part of a series of independently planned and executed saccades,
and only when that location is probed soon after the saccade sequence has finished. Locations
fixated as part of a parallel sequence of saccades, or locations probed more than 1500ms after
the intermediate saccade, were not significantly inhibited. For manual responses to probes,
we observed robust IOR for intermediate fixations following both parallel and independent
sequences of saccades, and at all time intervals following the sequence. Below we discuss the
implications for each response modality separately and then in combination.
Saccadic IOR
In Experiment 1, when sequences of two saccades were programmed and executed
serially (the “independent” condition), saccadic responses to intermediate locations along the
saccade path were slowed relative to novel locations, confirming the presence of IOR.
However, IOR was not observed for intermediate locations along the saccade path when the
two saccades in the sequence could be planned in advance. Furthermore, saccadic IOR was
only present when probes appeared relatively soon after the end of the saccade sequence (less
than 900ms), but not if the probe appeared late. It is important to note that the conditions
under which we observed saccadic IOR generally match the basic parameters of a typical
cueing experiment, in which a peripheral cue is followed by a delay (typically 500-1000ms)
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or a central reorienting event, and then a probe appears in either the cued location or the
opposite location. Therefore our results are consistent with the literature on the whole, but
demonstrate some important boundary conditions on saccadic IOR effects.
Although we did not test earlier than 500ms after the end of the second saccade in the
sequence, the relatively early detection of saccadic inhibition is consistent with previous
research (Hooge & Frens, 2000). The fact that saccadic IOR diminished over time, and was
no longer significant by around 1500ms after the initial fixation on the intermediate location,
matches other reports in the literature (e.g. Fecteau and Munoz, 2005; Pertzov, Zohary &
Avidan, 2010), and is also consistent with a recent model of saccadic IOR as reflecting shortterm depression of sensory sensitivity within the intermediate layers of the SC (Satel, Wang,
Trappenberg & Klein, 2011). The transient nature of saccadic IOR that we observe suggests
that inhibition may only persist to two or three subsequent eye movements, although other
forms of IOR could affect responses over a longer timeframe.
One possible interpretation of the slower responses to intermediate locations in the
independent sequence of saccades is that it may not reflect IOR at all, but rather saccadic
momentum (Smith & Henderson, 2009), that is, a tendency to continue forward rather than a
delay in shifting backward. This seems unlikely, given that the intermediate location was a
reversal of the current trajectory, and the control location against which it was compared was
closer to a return vector than a forward vector. But a momentum account could predict a
faster response to the control location, if there exists a gradient of facilitation that is strongest
for a forward vector and weakest for a reversed vector. However, any momentum that would
be reflected in this measure would be expected to be quite weak. Probes at the forward
location or at two back saccadic locations could differentiate between an IOR and momentum
account of these data, but our current design does not support these conditions. In any case,
our independent condition, in which we also observed slower responses to the previously-
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21
visited location, matches the “one-back” location measured in previous experiments
examining IOR in natural search. Saccadic momentum has been convincingly ruled out as an
explanation for the inhibitory effects in these conditions (Bays & Husain, 2012).
It is important to note that a lack of measured IOR does not mean the underlying
mechanism is absent. Some authors have suggested that inhibitory and facilitative effects
could coexist (Tipper et al., 1999; Wascher, & Tipper, 2004). In other words, the fact that
IOR was not observed could be due to the expression of a facilitative effect that counteracts
the inhibition.
Saccadic IOR seems to be generated by the selection of a final motor goal. Several
recent models of IOR suggest it is generated at multiple, independent sites, including both
within the Superior Colliculus (Satel et al., 2011) and upstream from the SC (e.g. Dorris,
Klein, Everling & Munoz., 2002). The Posterior Parietal Cortex (PPC) plays a role in
attention (Kastner & Ungerleider, 2000, Buschman & Miller, 2007) and preparation of goaldirected movements (Snyder, Batista & Anderson, 1997). The PPC has also been found to
transform object representations from retinotopic to motor coordinates (Colby & Goldberg,
1999; Buneo, Jarvis, Batista & Anderson, 2002) and it has been suggested to incorporate
spatiotopic information through gain fields (Anderson & Mountcastle, 1985). Therefore, its
involvement would explain findings of IOR in a spatiotopic reference frame (Krüger & Hunt,
2012; Mathot & Theeuwes, 2010; Pertzov, et al., 2010). Coordinate transformations and IOR
in PPC would be based on locations and vectors involved at the time of saccadic
programming, and for parallel sequences, these saccades are programmed simultaneously at
the initial fixation location. PPC’s involvement in IOR is consistent with recent EEG studies
that see a delayed N2PC (an event related potential (ERP) likely to originate from the PPC)
for probes at valid locations (Yang, Yao, Ding, Qi & Lei,2012; but see McDonald, Hickey,
Green & Whitman, 2009).
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IOR IN SACCADIC SEQUENCES
22
One can speculate about the implications of these results for eye movements during
free search. Parallel sequences of saccades are frequent (Findlay, et al., 2001; McPeek, et al.,
2000), do more work from the primary fixation (Inhoff, 1986; Zingale & Kowler, 1987) and
are difficult to cancel from the intermediate location(De Vries, et al., 2014). This suggests
that planning for both saccades is done primarily at the initial fixation and no further saccadic
planning occurs at the intermediate fixation locations. If this is the case, information that is
gained while an oculomotor program is being carried out will not be able to influence
subsequent saccadic selection processes until after the current sequence is completed. The
lack of inhibition at these “drive-by” locations could help make search more efficient:
fixation locations can be selected in parallel, executed in sequence, and still revisited
efficiently if necessary.
Manual IOR
In Experiment 2, manual responses to probes appearing at the previously fixated
location were delayed compared to novel locations, confirming the presence of IOR at
intermediate locations along a sequence of saccades. Unlike for saccadic responses, IOR was
observed equally in both parallel and independent sequences, and was long lasting.
Manual responses have been suggested to elicit an attentional or cortical component
of IOR based on their interaction with other attention effects, while saccadic responses have
been associated with the superior colliculus component, based on their interaction with
oculomotor effects (Hunt & Kingstone, 2003). This framework suggests that the manual
responses in our experiment were more influenced by where attention has previously been
focused, while the saccadic responses were influenced by saccade planning and motor
factors. Our results are therefore in line with the literature that suggests attention is allocated
to all saccade locations before execution of the first saccade of a sequence (Godijn &
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23
Theeuwes, 2003) and during execution at the current fixation location and the next-in-line
saccade target (Gersch et al., 2004). Since all locations are attended, regardless of planning,
our manual response result likely reflects an inhibition of attention to return to the previously
fixated location. Additionally, unlike with saccadic IOR, we observed manual IOR at late
probe onsets, which is consistent with the proposal that IOR is a long-lasting attentional
inhibitory tag which facilitates visual search (Klein & MacInnes, 1999; Klein, 2000, Samuel
& Kat, 2003).
Coming together: Two types of IOR
Consistent with other results (Taylor & Klein, 2000; Hunt & Kingstone, 2003), we
observed different patterns of IOR depending on which response modality was used.
Saccadic IOR was observed only for independent sequences and early probe onsets, whereas
manual IOR was consistent regardless of sequence type and probe onset time. Based on the
premise that attention is allocated to all the targets along the saccade path, we suggest that
IOR, when measured by saccades, is locked to the saccade planning process, while IOR as
measured by manual responses is generated wherever attention resides. IOR can be generated
by oculomotor planning, giving rise to oculomotor IOR, and IOR can also be generated by
shifts of covert attention, giving rise to attentional IOR. In both cases, for IOR to reflect its
origins, a response modality must be used that is sensitive to the type of IOR generated. In
the current experiment, these two components of IOR were presumably both generated at the
intermediate location in the independent condition. In the planned condition, no oculomotor
was applied at the intermediate location, leaving only attentional IOR.
Another promising framework for understanding IOR suggests that the form it takes
depends on whether or not the oculomotor system is, or has recently been, inhibited. Based
on a meticulous review of the literature, Klein and Hilchey (2012) argue that IOR reflects an
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24
inhibition of attention from the previously cued location if, and only if, the oculomotor
system is inhibited. When the oculomotor system has been activated (or there is no need to
inhibit it), IOR reflects a motor bias, that is, an inhibition of response in the direction of the
cue. In the context of the current results, it could be argued that the oculomotor system is
activated for both manual and saccadic responses, since it has just been engaged in the
process of executing the sequence of saccades, which would suggest both experiments should
elicit a motor form of IOR according to Klein and Hilchey’s taxonomy. However, the
oculomotor system would need to be inhibited in the final stages of the manual IOR task,
since the instruction is to maintain fixation and not saccade to the final probe, which could
provide the necessary conditions for generating an attentional form of IOR. Alternatively,
response modality per se could be a key factor (Taylor & Klein, 2000; Hunt & Kingstone,
2003) or perhaps the two forms of IOR co-exist (Kingstone & Pratt, 1999), and our results
represent a combination of saccadic and attentional IOR.
The finding that saccadic IOR is absent in parallel sequences provides insight into the
function of IOR in visual search. Klein (1988) and Klein and MacInnes (1999) have
postulated that IOR reflects a mechanism that biases saccades away from previously fixated
locations and towards novel locations. While this seems to hold for a majority of saccades
there has been some debate over those saccades that do return to recent locations (Hooge, et
al., 2005; Smith & Henderson 2009, 2011; but see Bays & Husain, 2012). In the current study
we have found that saccadic IOR is reduced at an intermediate location within a parallel
saccadic sequence. Given that dwell times at intermediate saccade locations are reduced in
search (McPeek& Keller., 2001) and the intermediate saccade cannot be easily cancelled
(DeVries, et al., 2014; McPeek & Keller, 2001), it would not be functional for such saccades
to be inhibited. It is possible that the reduction in IOR for return saccades after a parallel
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25
sequence can account for at least some of the return saccades that are observed during visual
search.
The time course of the two forms of IOR in the current results suggest that saccadic
IOR is more likely to inhibit responses to recently fixated locations as it is short lasting, while
attentional IOR could be more dominant over a longer time frame, as it persisted over the late
intervals tested (900+ ms). During a natural search process, saccadic IOR could therefore be
expected to prevent return saccades to locations that were already selected as the final
saccade goal, but this inhibition is short lived and not applied to locations that were fixated
along the way to that goal. Attentional IOR could play a role in inhibiting attention from
returning to all locations of a saccade sequence, and it could prevent returns to locations
fixated two or more previously. The current results therefore suggest that in natural search,
refixations of previous locations would be more likely when that location was part of a
parallel sequence of saccades, and the response to that location is executed soon after the
sequence is completed. Given that visual search encompasses many strategies incorporating
both of these patterns of sequences, it is not surprising that detecting evidence of IOR in free
search garners noisy results.
One final important additional implication of this result is that the intermediate
location can be inhibited for attention, but not for oculomotor planning and execution. As
such, our findings are consistent with other results demonstrating independence of saccade
planning and attention (Klein, 1980; Hunt and Kingstone, 2003), and are inconsistent with the
premotor theory of attention, which proposes that attention and saccade planning are the same
process.
Acknowledgements: This research was supported by BBSRC research grant BB/H01280X/1
and the James S. McDonnell Foundation (ARH).
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26
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