Download Anti-saccades away from faces: evidence for an influence of high

Exp Brain Res (2006)
DOI 10.1007/s00221-006-0455-1
RE SE AR CH AR TI C LE
Iain D. Gilchrist · Henning Proske
Anti-saccades away from faces: evidence for an influence
of high-level visual processes on saccade programming
Received: 10 August 2005 / Accepted: 8 March 2006
 Springer-Verlag 2006
Abstract The anti-saccade task is an important tool for
investigating both the generation of voluntary saccades
and the suppression of involuntary, stimulus driven, saccades. In the anti-saccade task participants have to suppress an involuntary saccade to the stimulus in order to
generate a voluntary saccade away from the stimulus. The
extent to which errors occur in this task indicates the ability of the stimulus to trigger an orienting response that is
beyond the control of the participant. Here we show an
increase in anti-saccade error rates away from an upright
face compared to a non-upright face. This suggests that
complex high-level visual properties of the stimulus can
inXuence whether involuntary orienting occurs.
Introduction
Saccadic eye movements move the high-resolution fovea
to points of interest in the environment (e.g. Walls 1962).
This happens for two, apparently distinct, reasons. First,
saccadic eye movements can be generated in a voluntary
manner—these are the saccades that are generated for
example in exploration, search and reading. Second, saccades can be generated in an involuntary manner. In this
case the eyes are drawn by an event or speciWc feature in
the environment, for example a sudden movement or
particularly salient visual object.
To investigate when involuntary saccades are generated requires a speciWc set of experimental conditions.
One task that can be used to investigate under what circumstances involuntary saccades are generated is the
anti-saccade task (Hallett 1978). In the anti-saccade task,
I. D. Gilchrist (&) · H. Proske
Department of Experimental Psychology, University of Bristol,
12a Priory Road, Bristol, BS8 1TN, UK
E-mail: [email protected]
Tel.: +44-117-9299004
Fax: +44-117-9298450
participants are instructed to generate an eye movement
in the opposite direction away from a visual onset when it
appears. The anti-saccade paradigm pits the two types of
saccades directly against each other. In a single trial, the
involuntary programming of a saccade towards a stimulus is initiated by the onset and at the same time the participant is programming a voluntary movement in the
opposite direction. Each trial represents a competition
between the voluntary and involuntary orienting
response. Typically, participants are able to control their
saccadic responses and to execute a voluntary saccade in
the correct direction on most trials (e.g. Hallett 1978).
However, on a proportion of trials an error occurs and a
saccade is directed towards the stimulus. In this case the
onset has resulted in the generation of an orienting
response that is performed against the participant’s intentions and therefore is best thought of as involuntary (see
Everling and Fischer 1998; Munoz and Everling 2004).
A number of studies have investigated what properties modulate the error rate in the anti-saccade task (see
Munoz and Everling 2004). For example, error rates
increase when the central Wxation point disappears a
short interval before the onset of the target (Fischer and
Weber 1997) and, when the target is more likely to
appear on one side than another, errors are more likely
to occur to that side (Koval et al. 2004).
As far as we know there have been no studies of how
the visual properties of the stimulus aVect the error rate
in the anti-saccade task. Recent work from our group
(Ludwig et al. 2005) using a diVerent saccade paradigm
suggests that visual information within the Wrst 100 ms
of Wxation determines where the eyes are directed and
that the response is related to the contrast of the stimuli
in a manner that closely mirrors the known response
properties of cells in primary visual cortex. In the current
experiment we were interested in investigating whether
we could Wnd any evidence of an eVect of high-level
object processes on saccade programming. The challenge
for such a study is to exactly match the low-level visual
properties of the stimuli in the experiment while at the
same time changing the high-level visual properties.
In pilot work we investigated anti-saccade performance using objects and faces as stimuli and compared
them to scrambled objects and faces (cf., Kourtzi and
Kanwisher 2000). We found a reliable diVerence in error
rate between faces and scrambled faces, but no such
diVerence between objects and scrambled objects. Having
carried out these experiments, we were not convinced that
these scrambling methods were useful in this context. SpeciWcally it is certainly not the case that the low-level characteristics of the stimuli remain unchanged by the
scrambling process. Because of the properties of natural
images, scrambling of this kind reduces the energy in the
low spatial frequencies—the very kind of signal that may
be most eVective at driving saccades (Ludwig et al. 2004).
However, keeping the low-level properties of the stimulus constant while manipulating the higher-level properties can be achieved by using faces and inverted face
stimuli as outlined below.
There is extensive behavioural evidence that upright
faces are processed in a qualitatively diVerent manner to
inverted faces (see Valentine 1988). In addition neurons
in the inferior temporal lobe (IT) not only respond selectively to faces but appear to be tuned to respond preferentially to upright faces (Perrett et al. 1988). This
neurophysiological evidence is supported by fMRI evidence for reduced activation in IT to inverted faces compared to upright faces (Haxby et al. 1999).
These data suggest that faces presented in an upright
orientation are treated diVerently in high-level vision
from non-upright faces. Importantly, because the same
face stimuli can be used at diVerent orientations, lowlevel visual factors, such as brightness, energy at diVerent
spatial frequencies and object size are identical across
conditions. For this reason face stimuli uniquely allow us
to look for an inXuence of high-level vision while matching the stimuli on low-level factors.
In the current experiment we used an anti-saccade
task to look for high-level visual eVects on the programming of involuntary saccades. SpeciWcally, we compared
the rates of anti-saccades away from upright faces with
the rates of anti-saccades away from non-upright faces
(inverted, rotated 90° left, rotated 90° right). If saccade
programming is only inXuenced by low-level factors,
such as luminance and contrast, we would expect to Wnd
no diVerence between these four conditions. However, if
high-level factors can inXuence saccade programming
then the upright face should lead to more errors.
Method
Design and procedure
The trial sequence is illustrated in Fig. 1. Each trial commenced with the presentation of a Wxation point. The
experimenter monitored the participant’s eye movements
and initiated the peripheral presentation of the stimulus
as soon as the eyes stabilised on the Wxation point. The
task for the participant was to generate a saccade in the
opposite direction away from the face and the instruction was to make the correct eye movement as quickly as
possible. Participants completed three blocks of 96 trials.
The stimuli were nine diVerent neutral expression
faces taken from Matsumoto and Ekman (1988). All
faces were presented in one of four orientations (0°
[upright], 90°, 180° [inverted], and 270°). Face stimuli
could appear at one of eight spatial locations equidistant
around the centre of the screen and were presented at a
centre-to-centre eccentricity of 8° of visual angle. Eye
movements were monitored with an EyeLink II eye
tracker (SR Research Ltd. Mississauga, ON, Canada).
This infrared tracking system samples eye position at
250 Hz with a spatial accuracy of »0.3°. Saccades were
detected using velocity and acceleration criteria of 30°/s
and 8,000°/s2. The eye movement data were analysed oVline. Only the Wrst saccade after display onset was analysed.
Trials were discarded if (1) the saccade latency was
lower than 80 ms as these are assumed to reXect anticipatory movements (Wenban-Smith and Findlay 1991); (2)
the starting point of the saccade was further than 2°
away from the centre of the Wxation point and (3) the
Wrst saccade-amplitude was less than 2°. These criteria
lead to an exclusion of an average of 8.2% of trials per
participant.
Time
Fixation display
(1000ms)
Response display,
with example eye
position data
Participants
There were 32 naïve participants (13 females, mean age
25.5 years). All were recruited from the University of
Bristol and were paid for participation. The project was
approved by the Ethical Committee of the Department
of Experimental Psychology, University of Bristol.
Fig. 1 The trial sequence over time in the experiment is shown. The
second display shows the face stimuli overlaid with an example eye
movement. Eye position was sampled at 250 Hz (white circles)
As the instruction to the participants was to saccade
away from the face we deWned an error in the task as a
Wrst saccade towards the face (i.e. within §90° of the centre of the face).
30
800
29
700
28
600
27
500
26
400
25
300
24
200
23
100
Error rates
The results are presented in Fig. 3. It is not clear why
error rates in this experiment were somewhat higher than
those previously reported. However, the displays used
here where diVerent in a number of ways when compared
to the stimuli used in a typical anti-saccade task (e.g. Hallett 1978; Koval et al. 2004). First, the face stimuli were
large. Second, there were eight possible target locations
rather than the more usual two. And third, the target and
the Wxation point disappeared at the onset of the target.
A one-way analysis of variance (ANOVA), revealed a
reliable eVect of the orientation of the face on the percentage of errors—F(3, 93)=4.12, p<0.01. Participants
made reliably more errors to upright faces (29.0%) than
22
0
90
180
270
Saccade Latency (ms)
Figure 2 illustrates the spatial distribution of saccade
landing positions across participants. Saccades successfully generated away from the target (downward movements in this Wgure) tend to have amplitudes consistent
with the position of the target. However, saccades directed
towards the target (upward movements in this Wgure) tend
to be less spread and the majority fall within the area
occupied by the face stimuli. It would appear that the
error saccades in this task are genuinely target directed.
Error rate (%)
Results
0
Face Orientation
Fig. 3 A graph of the results from the experiment. The grey bars
plot the mean error rates (left hand y axis) with within-participant
SEM error bars. The mean of the median saccadic reaction time for
each participant is plotted for correctly directed anti-saccades responses (white circles) and incorrectly directed pro-saccades responses (black circles)
to the faces in the other orientations (25.2%)—F(1,
31)=7.68, p<0.01. There was no reliable diVerence
between error rates for the three non-upright orientations—F(2, 62)<1. We can also apply a stricter criterion
that classiWes an error as a saccade that is directed
directly at the face and a correct saccade as one directed
in the opposite segment. The boundaries of these criteria
are shown by the solid white lines in Fig. 2 and correspond to §38.7° towards and away from the face. With
this deWnition a number of saccades that were previously
classiWed as both errors and correct saccades are now
excluded. However, there is still a reliable diVerence
between upright faces (30.1%) and the faces in the other
orientations (26.8%)—F(1, 31)=4.24, p<0.05.
Fig. 2 A two dimensional frequency distribution plot of saccade
landing positions in the experiment. The units on both axes are degrees of visual angle and each square in the plot represents the number of saccades that landed within that 0.5£0.5° area. The more
saccades that landed in any given sector the brighter the square. The
scale to the right of the plot indicates how the number of saccades
maps onto the brightness of the square. The saccade landing position has been normalised so that upward saccades are towards the
face and downward saccades are away from the face. The circle indicates the spatial extent and position of the face and the lines indicate
one saccade classiWcation criteria discussed in the text
Saccadic reaction times
We also analysed saccadic reaction times for both the
correct and incorrect saccades. The median saccadic
reaction times were analysed using a 2£4 (correct or
incorrect £ orientation: 0, 90, 180, 270) repeated
measures ANOVA. There was a signiWcant main eVect of
error—F(1, 29)=165.5, p<0.001. Error saccades were
on average 82 ms faster than correct saccades. There
was no main eVect of orientation (F(3, 87)<1) but there
was an interaction between error and orientation—F(3,
87)=2.95, p<0.05. The diVerences between correct and
incorrect saccades for each orientation condition were as
follows 0°: 75 ms, 90°: 81 ms, 180°: 90 ms and 270°:
75 ms. The interaction in the ANOVA represents a reliable increase in the magnitude of these diVerences
between the 180° and the 270° condition (t(29)=2.19;
p<0.05). However, in a comparison between upright and
non-upright faces this interaction was not signiWcant:
F(1, 29)=2.07, ns (p=0.16). This provides strong evidence that the error rate diVerence between upright and
non-upright faces was not a result of a speed-accuracy
trade oV.
Discussion
Participants made more errors in the anti-saccade task
when the stimulus was a face than when it was an
inverted face. Upright faces generated a stronger involuntary saccadic orienting response. Controlling for other
factors this in turn suggests that high-level visual information (in this case a face) is available to inXuence these
involuntary saccadic responses.
We chose to use face stimuli here for the methodological reasons detailed above. Because face processing is
uniquely disrupted by changes in orientation (Valentine
1988), this allowed inverted faces to be used as a comparison stimulus. This comparison is useful because the overall
low-level visual properties of the two stimuli are identical,
but the high-level processing of these stimuli change. As a
result we can conclude that the eVects reported are a result
of these high-level visual properties. The current results do
not rule out the possibility that other high-level meaningful object stimuli can also inXuence saccade programming
in this way. However, it is not possible to test this using the
current method as object processing, unlike face processing is not orientation sensitive in the same way (see Valentine 1988). In fact no other method except stimulus
inversion will leave both the energy over spatial frequencies and the spatial structure intact.
Saccade generation involves parietal and frontal cortices (see Schall and Hanes 1998) as well as sub-cortical
structures. Frontal structures appear to be particularly
important for successful performance in the anti-saccade
task (see Munoz and Everling 2004). For example, in
humans, error rates increase dramatically following damage to the frontal lobes (Guitton et al. 1985). In contrast,
converging evidence suggests that neurons in the temporal
lobe appear to be important for complex high-level visual
processing, including the processing of faces (e.g. Perrett
et al. 1988; Haxby et al. 1999). At a neural level, the current behavioural result suggests an interaction between the
parietal–frontal system involved in spatial orienting and
the temporal lobe, which is involved in complex high-level
visual processes. This is a surprising result for theories in
which these two systems are assumed to act in an independent manner (e.g. Milner and Goodale 1995).
The current result suggests that the high-level visual
properties of the target can inXuence the error rate in the
anti-saccade task. One explanation for errors in the antisaccade task is the motor preparation hypothesis (Koval
et al. 2004). Within this framework, errors are a result of an
increased level of neural activity before the target appears,
which results in the stimulus-related activity being more
likely to reach threshold. The current result suggests that
errors may not be solely motoric in origin but could also be
visual. One possibility is that errors can result from an
increase in the stimulus-related activity induced by the recognition of an upright face, which can also results in it
being more likely that the threshold is reached.
The increase in error rate found in the current study is
relatively small. However, the size of the interference
may not reXect, in a simple way, the strength of the interaction between high-level visual processes and saccadic
orienting. To observe any interference in this task the signal that indicates the presence of an upright face has to
arrive at ocular motor structures concurrently with the
generation of the voluntary saccade. The latencies of
visual responses in frontal areas are on average 40 ms
faster than the visual responses in the inferior temporal
lobe (Bullier 2001); as a result the correct saccade will
often be generated before the inferior temporal area can
signal the presence of a face. However, there is substantial variation in the speed of both of these signals from
trial-to-trial. On some trials these two signals will therefore overlap in time and so interference can occur. Saccade latencies also vary considerably across diVerent
tasks and so we might expect to observe more, or even
less, interference under diVerent conditions.
Whatever the exact neural mechanism, the current
result provides evidence for an interaction between highlevel visual processing and involuntary saccadic orienting.
Acknowledgements IDG is supported by the UK EPSRC and the
Wellcome Trust. HP was supported by a Wellcome Trust vacation
scholarship. We thank Casimir Ludwig for comments on a draft of
this manuscript.
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