Cerebral Cortex April 2014;24:898–907
doi:10.1093/cercor/bhs368
Advance Access publication November 25, 2012
Parieto-Occipital Cortex Shows Early Target Selection to Faces in a Reflexive
Orienting Task
Stéphanie M. Morand1, Monika Harvey2 and Marie-Hélène Grosbras1
1
Institute of Neuroscience and Psychology and, 2School of Psychology, University of Glasgow, Glasgow G128QB, UK
Address correspondence to Stephanie M. Morand, PhD, Institute of Neuroscience and Psychology, University of Glasgow, 58, Hillhead street,
G128QB Glasgow, UK. Email: stephanie.morand@glasgow.ac.uk
It is well established that human faces induce stronger involuntary
orienting responses than other visual objects. Yet, the timing of this
preferential orienting response at the neural level is still unknown.
Here, we used an antisaccade paradigm to investigate the neural dy-
namics preceding the onset of reflexive and voluntary saccades eli-
cited by human faces and nonface visual objects, normalized for their
global low-level visual properties. High-density event-related potentials
(ERPs) were recorded in observers as they performed interleaved pro-
and antisaccades toward a lateralized target. For reflexive saccades,
we report an ERP modulation specific to faces as early as 40–60 ms
following stimulus onset over parieto-occipital sites, further predicting
the speed of saccade execution. This was not linked to differences in
the programming of the saccadic eye movements, as it occurred early
in time. For the first time, we present electrophysiological evidence of
early target selection to faces in reflexive orienting responses over
parieto-occipital cortex that facilitates the triggering of saccades
toward faces. We argue for a 2-stage process in the representation of
a face in involuntary spatial orienting with an initial, rapid implicit pro-
cessing of the visual properties of a face, followed by subsequent
stimulus categorization depicted by the N170 component.
Keywords: event-related potential, human faces, saccadic programming,
timing
Introduction
Our ability to respond automatically to external events and to
voluntary suppress responses to irrelevant cues requires flex-
ible behavior. This flexibility can be assessed easily within the
visual saccadic system using pro- and antisaccade paradigms
as they elicit different behavior patterns in response to the
same stimulus. The prosaccade task requires participants to
look toward a suddenly appearing stimulus in the periphery,
whereas the antisaccade task requires participants to look
away from the stimulus by generating an eye movement in the
opposite direction to its mirror location. To correctly perform
an antisaccade, the neural process that triggers the reflexive,
stimulus-driven response to the target must be inhibited, so
that a voluntary, task-driven saccade can be generated in the
opposite direction (Hallet 1978; Connolly et al. 2000; Munoz
and Everling 2004). Antisaccade tasks thus represent very sen-
sitive means of dissociating voluntary from reflexive (auto-
matic) orienting responses. Regarding the neural correlates of
antisaccades performance, event-related functional magnetic
resonance imaging (fMRI) and human lesion studies have re-
vealed that the dorso-lateral prefrontal cortex (DLPFC) and su-
pramarginal gyrus (SMG) are likely to be involved in the
reflexive saccadic inhibition, whereas the frontal eye fields
(FEFs) and intraparietal sulcus (IPS) are more selectively in-
volved in the preparation and generation of voluntary antisac-
cades (Pierrot-Deseilligny et al. 2002; Connolly et al. 2002;
© The Author 2012. Published by Oxford University Press. All rights reserved.
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Cornelissen et al. 2002; DeSouza et al. 2003; Ploner et al.
2005; Brown et al. 2006; Ettinger et al. 2008).
While the antisaccade task has been studied intensively
with abstract stimuli (mainly dots) that can be viewed as
Downloaded from http://cercor.oxfordjournals.org/ at California Institute of Technology on July 11, 2015
being somewhat remote from real word object recognition, to
date, very few studies have employed this paradigm with
more realistic high-level stimuli (Gilchrist and Proske 2006;
Morand et al. 2010). Human faces, among other visual
objects, are arguably the most salient visual stimuli we
process every day, conveying crucial information for social
interactions, and are thus likely to have a special impact on
saccadic orienting responses. Indeed, we recently reported a
significant increase in antisaccade error rates for faces as well
as faster prosaccades to faces compared with other visual cat-
egories, indicating that human faces induced stronger invo-
luntary orienting responses than other visual objects (Morand
et al. 2010). Importantly, this perceptual bias could not be ac-
counted for by global low-level visual properties as these
were normalized across stimuli. It is therefore very likely that
the reflexive response to faces, which is beyond the control of
the observer, is influenced by high-level visual properties.
Here, we quantify this preferential orienting response toward
faces and, for the first time, link it to the timing of activity in the
human brain. We used stimulus-locked event-related potentials
(ERPs) to investigate, with high-temporal resolution, the neural
dynamics preceding the occurrence of voluntary and reflexive
saccades to faces and nonface visual objects. We employed a
task-cued paradigm for which the stimulus type was task irre-
levant as participants were not asked to perform a categoriz-
ation. We aimed to determine at what stage in the saccadic
programming, a voluntary saccade dissociates from a reflexive
saccade, and more importantly, to unravel just “when” face
sensory information impacts on the saccadic programming.
We show electrophysiological evidence of an implicit categor-
ization of faces in reflexive orienting responses with an early
face-specific target selection at 40–60 ms over posterior parie-
tal and parieto-occipital scalp regions. Most importantly, this
early activity predicted the speed of the upcoming saccades
toward the faces. This supports 1) controversial claims that
the stimulus-response integration for a face starts at a very
early stage of saccadic programming and 2) a 2-stage process
in the representation of a face in involuntary spatial orienting
with an initial, rapid implicit processing of the visual proper-
ties of a face, followed by subsequent stimulus categorization
depicted by the N170 component.
Materials and Methods
Participants
Twelve healthy individuals (aged 20–37; mean = 24 years; 8 women)
received financial compensation for participating in this study. Eleven
of the 12 participants were right handed (Oldfield 1971). All reported
normal or corrected-to-normal vision. All participants provided
written informed consent to participate in this experiment, which was
approved by the local Ethics Committee of the University of Glasgow.
Stimuli
Full details about the antisaccade paradigm and stimuli used in this
experiment can be found in Morand et al. (2010). Briefly, neutral
Western Caucasian faces (6 male and 6 female faces), cars (n = 12
from the database of Schweinberger et al. 2007), and noise phase
scrambled patterns (n = 12) were used as stimuli. Faces and cars
(image size: 128 × 128 pixels, 8 bits/pixel) were front view gray
scaled photographs pasted onto a uniform gray background and sub-
tended a visual angle of approximately 4.20° × 3.8° (Fig. 1A). Stimuli
were presented on a gamma corrected 21-in. A Sony GDMF520 CRT
monitor with a resolution of 1280 × 1024 and refreshed at 85 Hz. The
monitor was placed at 68 cm from the chinrest.
To control for low-level visual properties between stimuli, faces,
and car, images were equated for spatial frequency, luminance, and
contrast. To this end, the average amplitude spectrum of all images in
the dataset was calculated first and the phase of each image was then
combined to this average amplitude spectrum. As a result, faces and
cars were normalized for their amplitude spectra. Noise patterns were
generated by randomizing the phase of the normalized face and car
images. Finally, the root-mean-square contrast was also normalized
for all images resulting in stimuli normalized for their “global” low-
level visual properties.
Task and Procedure
Participants were instructed to generate a saccade either in the direc-
tion of the stimulus appearing on the screen ( prosaccade) or in the
opposite direction away from the stimulus (antisaccade; Fig. 1B).
Each trial consisted of 4 stages. (1) The initial display consisted of a
central fixation cross (0.8°) on a white background and lasted at least
Figure 1. Schematic representation of the antisaccade task. (A) Examples of the
images used. See methods for image processing details. (B) Within a block, subjects
were asked to generate either a prosaccade (PS) or an antisaccade (AS) depending
of the color of the cue: A green dot indicated that the participant had to perform a
saccade toward the stimulus (PS), while a red dot instructed the participant to
generate a saccade in the opposite direction (AS). Stimuli were faces, cars, and
noise phase scrambled patterns as shown in (A) and were presented in random
order.
1000 ms, while the experimenter initiated the stimulus presentation
as soon as the participant’s eyes were stabilized on the fixation cross.
(2) This was followed by the display for 200 ms of a central cue (0.8°
in size), whose color instructed the participant to generate either a
prosaccade (green dot) or an antisaccade (red dot). (3) The cue
display was followed by a 100-ms blank screen that was inserted
before the presentation of the stimulus to reduce reactions times for
both pro- and antisaccades and to further increase the difficulty in
antisaccades (Munoz and Everling 2004). (4) The blank screen was
followed by the stimulus display, which remained in view for 1000
ms. Stimuli (faces, cars, and noise patterns) appeared in each trial at
1 of the 2 possible peripheral locations on the horizontal meridian, at
10° either to the left or right of the center of the screen. Cue type
( pro- or antisaccade), stimulus type (face, car, and noise pattern) and
stimulus location (Left [LVF] or Right [RVF] visual fields) were ran-
domly interleaved. Participants completed 12 blocks of 60 trials (720
trials in total) and were asked to perform the correct eye movement
as rapidly and as accurately as possible. In this task-cued paradigm,
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the stimulus type was task irrelevant as participants were not asked to
perform any categorization. Moreover, participants could not predict
what type of stimulus nor what location would be presented on the
next trial.
Saccadic Eye Movement Acquisition and Analysis
The horizontal and vertical positions of the eyes (left or right) were
recorded with a video-infrared eye tracker (EyeLink 2K SR Research
Ltd., Mississauga, Canada), which has a sampling rate of 1000 Hz and
a spatial resolution of 0.01°. The system uses the center of the pupil
and corneal reflection technique to define the pupil position. Partici-
pants were seated at the table with their head resting on a chin rest.
Each of the 12 blocks started with a 9-point grid calibration and vali-
dation procedure to ensure accurate eye tracking. Participants were
asked to saccade to a gray, circular disk that appeared sequentially
(but unpredictably) in a 3 × 3 grid. Prior to testing, participants re-
ceived 30 practice trials.
Data were analyzed off line with the Data Viewer Software (SR Re-
search Ltd., Mississauga, ON, Canada). Saccades were detected using
velocity and acceleration criteria of 30°/s and 8000°/s2. Only the first
saccade after stimulus display, onset was analyzed. Trials were dis-
carded if (1) the saccade latency was shorter than 80 ms (antici-
pations) or (2) the amplitude of the first saccade was less than 2° or
(3) initial fixation was larger than 0.5° away from the fixation cross.
Furthermore, blinks were excluded. These criteria led to an exclusion
of an average of 5.9% of trials per subject. Discarded trials were
equally distributed across conditions and stimuli. The resulting sac-
cades belonged to 1 of the 12 conditions defined by saccade type
( pro- and antisaccades), saccade direction (left and right visual
fields), and stimulus type (face, car, and noise pattern).
EEG Acquisition and Analyses
Continuous electroencephalogram (EEG) was acquired at 1024 Hz
through a 128-channel Biosemi EEG system (Biosemi V.O.F., Amster-
dam, The Netherlands) covering the entire scalp. Analyses were per-
formed using Cartool (http://brainmapping.unige.ch). As our main
purpose was to reveal electrophysiologically when the stimulus cat-
egory impacted upon the saccade programming (specifically when
saccades toward faces and saccades toward other visual objects dif-
fered), we performed stimulus-locked averaging and focused our
analysis on presaccadic activity (Ptak et al. 2011). Peristimulus epochs
of EEG starting 100 ms prior to and ending 250 ms after the onset of
the stimulus, which satisfied the inclusion criteria defined by the eye
movement analysis (see above), were averaged for each experimental
condition and participant, with a ±100 µV artifact rejection criterion.
Before group averaging, data from artifact electrodes of each partici-
pant were interpolated using a spherical spline interpolation (Perrin
et al. 1987). Data were baseline corrected using the prestimulus
period (−100 ms to 0), bandpass filtered (0.18–60 Hz and using a
notch at 50 Hz), and recalculated against the average reference. Only
correct pro- and antisaccades generated in response to faces, cars,
and noise patterns are described in the Electrophysiological Results.
Cerebral Cortex April 2014, V 24 N 4 899
EEG Analysis
To disentangle the effects specific to the stimulus identity (face, car,
and noise) from the effects related to the programming of the differ-
ent eye movements ( pro- and antisaccade), 2 distinct analyses were
conducted: First, we searched for “task-related” effects and compared
ERPs with pro-and antisaccades directed to the same visual field, re-
gardless of stimulus type. Then, we searched for “stimulus-specific”
effects and compared ERPs with face, car, and noise stimuli presented
in the same visual field for each task condition (pro- and antisaccade
analyzed separately).
For both analyses (hereafter referred to as “task-effect” and
“stimulus-effect” analyses), we used a multistep analysis procedure
that examines local and global measures of the electric field at the
scalp (Murray et al. 2008). Briefly, it entails analyses of the response
strength and response topography to differentiate effects due to the
modulation in the strength of the responses of statistically undistin-
guishable brain sources from alterations in the configuration of these
sources (resulting in a change of scalp topography), as well as latency
shifts in brain processes between experimental conditions. These
methods have been successfully used for analyzing EEG data from
larger electrode sensor arrays and have been detailed extensively else-
where (Morand et al. 2000; Michel et al. 2004; Murray et al. 2008;
Cappe et al. 2010; Cocchi et al. 2011).
ERP Waveform Analysis
We identified periods of amplitude modulations by contrasting the
ERPs involved respectively in the task-effect and stimulus-effect ana-
lyses from each electrode, as a function of time after the stimulus
onset in a series of pairwise comparisons (t-tests) and 1-way analysis
of variances (ANOVAs). The results of the analyses are presented as
an intensity plot representing time, electrode location, and P-values at
each data point. Only differences with P-values ≤0.05 (Bonferroni
corrected by the number of electrodes −1) and extending over at least
15 ms were considered reliable (Guthrie and Buchwald 1991) and
will be illustrated in the Results section.
Response Strength and Topographical Analyses
Amplitude modulations of ERP waveforms do not allow a distinction
between activation of different networks (with different topographies
of the electric field at the scalp) and modulation of similar networks.
To determine whether amplitude modulations of ERPs result from a
change in response strength (which would be consistent with a
modulation in response gain) or result from a change in response to-
pography (which would be consistent with a change in underlying
brain sources), we applied 2 types of analyses focusing on 2 features
of the electric field. The first type of analysis identified the periods of
time when the strength of the ERP differed across experimental con-
ditions, irrespective of the topography of the ERP. The second type of
analysis identified the periods of time when the topography of the
ERP differed within and across experimental conditions, irrespective
of the strength of the ERP.
Changes in electric field strength were determined by analyzing
the global field power (GFP; Lehmann and Skrandies 1980). A GFP is
calculated as the root-mean-square across all electrodes and rep-
resents the spatial standard deviation of the electric field at the scalp.
Large values of GFP yield stronger electric fields. GFP was analyzed
in a similar manner to what we described above for the analysis of
ERP waveforms, using millisecond-wise paired t-tests on GFP wave-
forms (P-values ≤0.05 over at least 15 ms were considered). Obser-
vation of a GFP modulation without accompanying topographical
changes across experimental conditions is best explained by a
strength or power modulation of statistically undistinguishable neural
generators across experimental conditions.
To identify statistically significant periods of topographical
changes, we applied a spatio-temporal analysis approach that
searches for topographical differences of the global electric field
(potential map) between conditions across time (i.e., Morand et al.
2000; Schnider et al. 2002; Nahum et al. 2009). We emphasize that
changes in the electric field topography derive from changes in the
configuration of the brain’s underlying active generators (Lehmann
900 Face Selection in Reflexive Orienting Responses • Morand et al.
1987). This method is based on a modified spatial k-means clustering
analysis (Pascual Marqui et al. 1995) that determines the most domi-
nant map topographies and the periods during which they are
present in the whole group-averaged data. This approach is based on
the observation that scalp topographies do not change randomly, but
rather remain stable for a period of time in a certain configuration
and then rapidly switch to a new configuration. The periods of stab-
ility have been called “functional microstates” (Lehmann 1987; Murray
et al. 2008) and are thought to reflect the different information pro-
cessing steps. Note that the topographical analysis method is indepen-
dent of the reference electrode and is insensitive to amplitude
modulation of the same scalp configuration across conditions, as to-
pographies of normalized maps are compared. The optimal number
of maps explaining the averaged data sets was determined with the
cross validation (Pascual Marqui et al. 1995) and the Krzanowski–Lai
criterion (Krzanowski and Lai 1985).
The cluster analysis was applied to the group-averaged ERPs in-
volved in the task-effect analysis ( pro- and antisaccades directed to
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the same visual field, all stimulus types pooled together) and in the
stimulus-effect analysis (face, car, and noise presented in the same
visual field separately for pro- and antisaccades). The distribution of
the topographical maps across time was examined within and com-
pared between conditions.
The significance of the pattern of maps observed in the group-
averaged data was then tested statistically by comparing each of these
maps with the moment-by-moment scalp topography of individual
subject’s ERPs. That is, each time point of the individual subject’s
ERPs was labeled according to the map with which it best correlated
spatially, yielding a measure of map presence (global explained var-
iance, GEV) that was in turn submitted to repeated-measures ANOVA
using conditions (task or stimulus type) and map as within-subject
factors. P-values of post hoc single comparisons were Bonferroni-
corrected. This fitting procedure shows whether a given experimental
condition is more often described by one map versus another and,
therefore, whether different generator configurations better account
for particular experimental conditions.
Results
Behavioural Results
Error Rates
We assessed error rates for both the pro- and antisaccade per-
formance for the 3 stimulus types (faces, cars, and noise) and
the 2 stimulus locations (left and right). A 3-way ANOVA re-
vealed main effects of task (F1,11 = 50.725, P = 0.00002),
showing greater errors for anti- compared with prosaccades
and of stimulus type (F2,22 = 14.237, P = 0.0001), showing
greater errors for faces compared with other stimuli, yet there
was no stimulus location effect. As the stimulus location did
not have any effect on the independent variables, stimuli pre-
sented to the left and right visual field of the same task and
stimulus type were pooled together. The resulting 2-way ANOVA
revealed a main effect of task (F1,11 = 50.725, P = 0.00002), a
main effect of stimulus type (F2,22 = 14.237, P = 0.00011) and a
significant interaction between task and stimulus type
(F2,22 = 12.007, P = 0.0003). Pairwise comparisons showed
that antisaccades generated higher error rates (20.65%) than
prosaccades (1.76%, Fig. 2A,B). More importantly, face stimuli
induced greater errors (24.12%) compared with cars (19.15%,
F1,11 = 48.9, P < 0.001) and noise patterns (18.67%, F1,11 = 14.92,
P = 0.0026; Fig. 2B). There was no difference in error rates for
prosaccades for the 3 stimulus types (Fig. 2A).
Saccadic Reaction Times
Saccadic reaction times for correct pro- and antisaccades were
analyzed in a 2-way repeated-measures ANOVA as described
above. This analysis revealed a main effect of task (F1,11 = 17.2,
P = 0.0016), a main effect of stimulus type (F2,22 = 5.3,
P = 0.013) and a significant interaction between task and stimu-
lus type (F2,22 = 7.2, P = 0.004). As expected, post hoc com-
parisons revealed that antisaccades (197 ms) were on average
26 ms slower than prosaccades (Fig. 2C,D). More interestingly,
face stimuli induced faster prosaccades (166 ms) compared
with cars (173 ms, F1,11 = 22.74, P < 0.001) and noise patterns
(175 ms, F1,11 = 17.44, P < 0.001, Fig. 2C). No differences in
latency were found for antisaccades (Fig. 2D).
The saccadic eye movement analysis thus revealed that faces
induced both, a higher error rate in antisaccades and faster pro-
saccades in comparison with cars and noise patterns, replicat-
ing our previous study.
Electrophysiological Results
Task Effect (Pro- vs. Antisaccades)
Saccades directed to the left (LVF) and to the right (RVF) were
analyzed separately. Figure 3 summarizes the results of the
multistep analysis applied to pro- and antisaccades directed to
the same visual field. As similar electrophysiological patterns
of difference were found between eye movements directed to
the left and right visual fields, except that the electrical field
was flipped between left and right, we chose to present the
differences found between pro- and antisaccades directed to
the LVF only. We first identified electrode amplitude differ-
ences in the whole electrode set between ERP waveforms
Figure 2. Saccadic eye movement results. Error rates and saccadic reaction time
obtained for pro- and antisaccades as a function of stimulus type (faces, cars, and
noise patterns). Bars indicate within-participants standard error of the mean error
bars. Asterisks represent the least significant P-values of the tests performed
(**P < 0.01).
preceding prosaccades and antisaccades, by computing point-
wise t-tests over the epoch covering −100 ms to +250 ms fol-
lowing the stimulus onset. These tests identified significant
and temporally sustained differences (i.e., P < 0.05 for at least
15 ms) at 70–90 ms over central electrodes and from 110 ms
to around 160 ms at central and right posterior electrode sites
before extending over time to the left and right frontal electro-
des up to 200 ms (Fig. 3A). It is worth noticing that differ-
ences in neural responses found after 171 ms (average latency
for prosaccades, ±17 ms) most probably reflect differences in
saccade latencies between pro- and antisaccades and are thus
likely to be contaminated by eye movement execution. With
this in mind, we think that it is very unlikely though that any
differences found before 150 ms are linked to such eye move-
ment artifacts and would argue that they are better explained
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by differences in the programming of saccadic eye movements.
The analysis of the GFP revealed statistically reliable differ-
ences in response strength of the saccade programming
Figure 3. Task-effect analysis contrasting pro- and antisaccades directed to the
same visual field (here LVF). (A) Results of time point-wise t-tests applied on
amplitude across the whole 128 electrodes set. The x, y, z axes display time (time 0
representing the stimulus onset), electrode position, and P-values. Only P-values
< 0.05 Bonferroni-corrected extending for at least 15 ms are displayed. (B) Results
of the GFP analysis (response strength) as a function of time (only effects P-values
< 0.05 for a minimum of 15 ms are represented). (C) Results of the topographical
pattern analysis: 4 stable topographies were identified over the poststimulus period
(0–250 ms). Their temporal succession and spatial distribution are shown. Changes
in topographies started at around 110 ms after stimulus onset, indicating a change of
the configuration of underlying brain sources involved in pro- and antisaccades.
Cerebral Cortex April 2014, V 24 N 4 901
between 70–87 and 109–126 ms after the stimulus onset
(Fig. 3B). The late time period of difference in response
strength between pro- and antisaccades was concomitant with
a topographical change at 110 ms, as identified by the topo-
graphic pattern analysis. Four stable electrical brain configur-
ations that explained 94.3% of the variance (GEV) were
identified over the poststimulus period. The temporal succes-
sion of these maps and their spatial distribution are shown in
Figure 3C. While topographies were identical over the first
110 ms (map A) and after 200 ms (map C), 3 maps (maps B,
D, and E) were identified during the 110–200-ms period that
differentially accounted for pro- and antisaccades. The fitting
procedure in individual’s ERPs and within-subjects ANOVA
over the 110–200-ms poststimulus period revealed a signifi-
cant task × map presence interaction (F2,22 = 22.47, P < 0.0001)
with maps D and E better characterizing the programming of
antisaccades (map D: F1,11 = 25.28, P = 0.0003; map E:
F1,11 = 7.6, P = 0.018) and with map B significantly better ex-
plained in the programming of prosaccades (F1,11 = 12.44,
P = 0.0004). In contrast, the early difference in response
strength found at 70–87 ms (Fig. 3B) was not temporally coinci-
dent with a change in topographical patterns. Map A was
equally represented in pro- and antisaccades (GEV,
F1,11 = 1.3495 , non significant [ns]), but prosaccades generated
stronger global electrical response in this time window,
suggesting a higher response magnitude of identical underlying
brain sources for prosaccades compared with antisaccades.
To summarize, these results show that the neural response
differences in the programming of pro- and antisaccades
involve first a change in response strength of identical brain
generators indicating a modulation of response gain between
70 and 90 ms for prosaccades, followed by a change in
response topography at 110 ms consistent with different con-
figurations of underlying brain sources for pro and anti
saccades.
Stimulus Effect (Face vs. Other Visual Categories)
To investigate when the stimulus type interferes with the
saccade programming, ERPs to face, car, and noise pattern
stimuli presented in the same visual field were compared for
pro- and antisaccades separately. Among all tasks ( pro, anti
directed to the LVF and RVF), only prosaccades directed to
the LVF showed significant neuronal response differences
across stimulus categories (Fig. 4). A time point-wise 1-way
ANOVA applied to the ERPs waveforms from each electrode
revealed a main effect of stimulus type in 2 time windows, at
40–60 ms and 125–140 ms after the stimulus onset (Fig. 4C).
Further amplitude modulations were found from 165 ms on,
which correspond to the time period of the average latencies
of prosaccades to face, car, and noise patterns and conse-
quently, and might reflect the neuronal activity related to
motor execution. Post hoc tests ( paired-wise t-tests with
P-values <0.05 after Bonferroni correction) indicated that, at
40–60 ms, faces evoked stronger amplitude responses over
right posterior parietal and parieto-occipital electrodes, com-
pared with noise patterns (CP2, P2, P4, PO4,PO6, and PO8)
and cars (P4 and PO4) as illustrated in Figure 4D (left panel).
In the late time period of significant amplitude differences
(125–140 ms), faces and cars generated stronger activity over
parieto-occipital electrodes (PO6 and PO8) when compared
with noise, respectively, while no significant differences were
found between face and car stimuli (Fig. 4D, right panel).
902 Face Selection in Reflexive Orienting Responses • Morand et al.
This suggests that the early stimulus effect at 40–60 ms over
right parietal and parieto-occipital sites is “face specific”,
whereas, at 125–140 ms, the stimulus effect seems to be
object specific. To strengthen this finding, we performed a
conservative correlation analysis between the mean amplitude
response of each above-mentioned electrodes depicting the
stimulus effect and the saccadic reaction time in the 2 time
periods of interests. The early face-specific effect was con-
firmed by a direct relationship between the amplitude
response for faces over PO6 and PO8 electrodes at 40–60 ms
and the speed of saccadic execution. Indeed, early face-
specific modulation over right parieto-occipital sites corre-
lated negatively with the saccadic reaction time (nonpara-
metric Spearman, R = − 0.64, P < 0.05), indicating that
between 40 and 60 ms after the stimulus onset, the stronger
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(the more positive) the neuronal response to face stimuli, the
faster the prosaccade execution (Fig. 5). No significant corre-
lation could be established for faces during the late time
period, nor for the car or noise patterns in any of the 2 time
periods of interest. Finally, to exclude the possibility that the
face-specific effect reported here at 40–60 ms could be due to
a difference in reaction times to faces compared with cars or
noise, we searched for latency differences in ERPs over the
right parietal and parieto-occipital electrodes depicting the
stimulus effect (CP2, P4, and PO8 as illustrated in Fig. 4D).
No significant differences in latency were found across faces,
cars, and noise patterns on electrodes CP2 (F2,22 = 1.32,
P = 0.28, ns), P4 (F2,22 = 0.88, P = 0.42, ns), and PO8
(F2,22 = 1.38, P = 0.27, ns). The latency of the maximal ampli-
tude was on average 49 ms ±8.6 for faces, 48.11 ms ±8.8 for
cars, and 49.6 ms ±9.4 for noise patterns over the CP2, P4,
and PO8 electrodes. This demonstrates that the stimulus effect
(e.g., face specific) in the parieto/parieto-occipital electrodes
is not confounded by differences in reaction times between
the different stimulus categories.
It is important to note that the GFP analysis failed to reveal
statistically reliable differences in response strength (Fig. 4A).
The topographic pattern analysis identified 3 stable electrical
brain configurations over the poststimulus period that ex-
plained 96.2% of the variance of the group-averaged ERP
dataset (Fig. 4B). The fitting procedure in individual’s ERPs
and within-subjects ANOVAs over the 0–170-ms poststimulus
period revealed no significant stimulus type × map presence
interaction or significant main effects, indicating that the 3
maps were equally explained in the prosaccades directed to
face, car, and noise pattern stimuli. The early neuronal
response modulation elicited by the face stimuli was not tem-
porally synchronous with a change in topographical patterns
across stimulus categories, suggesting a strength or power
modulation of identical underlying brain sources across the
contrasted categories.
Discussion
We pinpoint the neural correlates associated with the fast in-
voluntary orienting responses to faces described previously
(Gilchrist and Proske 2006; Morand et al. 2010). We first
report effects of task in the 70–90 and 110–200-ms time
windows following target presentation. In addition, in the
context of prosaccades, we observed an effect of stimulus as
early as 40 ms following the target onset, with faces eliciting
higher activity over parieto-occipital sensors. To disentangle
 Downloaded from http://cercor.oxfordjournals.org/ at California Institute of Technology on July 11, 2015
Figure 4. Stimulus-effect analysis contrasting prosaccades directed to the left visual field across visual categories (faces, cars, and noise pattern stimuli). (A) GFP as a function
of time. The analysis of GFP did not reveal any difference in response strength between stimuli. (B) Results of the topographical pattern analysis: 3 stable topographies equally
represented across stimulus categories were identified over the poststimulus period (0–250 ms). Their temporal succession and spatial distribution are shown. (C) The main
effect of stimulus type as revealed by a time point-wise 1-way ANOVA applied on amplitude across the whole 128 electrodes set with stimulus type as the within-subjects
factor. Only P-values <0.05 for at least 15 ms continuously are displayed. Two time periods of significant differences across stimulus types were identified at 40–60 and 125–
140 ms after stimulus onset. (D) Results of post hoc tests ( paired-wise t-tests with P-values <0.05 after Bonferroni correction). P-values are mapped on the 3D electrode
configuration (back view) for the early 40–60 ms (left panel) and late 125–140 ms (right panel) time windows and the 3 paired contrasts: Face/noise (upper row), face/car
(middle row), and car/noise patterns (lower row). Exemplar waveforms from parietal and parieto-occipital electrode sites (CP2, P4, and PO8) are also displayed. Faces evoked
stronger amplitude responses over posterior parietal and parieto-occipital electrodes compared with noise patterns (CP2, P2, P4, PO4,PO6, and PO8) and cars (P4, PO4) at 40–
60 ms after stimulus onset, suggesting a early face-specific effect on saccadic programming.

face-specific effects that can occur at the level of stimulus pro-
cessing from those at the level of motor programming during
saccadic implementation, we first isolated the motor
programming-level neural activity by comparing pro- with
antisaccades.
Modulation in Amplitude and Topography During
Pro- and Antisaccades
The results showed that the programming of pro- and antisac-
cades generated a first change in electrophysiological
response strength for prosaccades at 70–90 ms after the stimu-
lus onset over central electrodes. There were no accompany-
ing topographical changes, indicating a modulation of
response gain for prosaccades. This was followed by a change
in response topography at 110 ms for antisaccades, with 2
successive electric field configurations, consistent with a
modification of the underlying brain sources. These results
are in line with a recent ERP study showing an increase in P1
component amplitude (onset at 70–90 ms) prior to reflexive
saccades in a visual search task (errors in this case), which
the authors interpreted as the neural correlate of a sensory
gain control mechanism that enhanced target saliency or de-
creased distracter saliency through a modulation of sensory
information during saccade planning (Ptak et al. 2011). Our
data are in agreement with this interpretation as in antisac-
cades, the observer has to look away from the target and
target selection and relevance might thus be reduced. The
gain response observed at 70–90 ms in the reflexive orienting
response ( prosaccades) could possibly reflect stronger
sensory signals for an enhancement of target selection. The
fact that this was depicted over central electrodes supposes a

Cerebral Cortex April 2014, V 24 N 4 903


Figure 5. Early modulation of parieto-occipital activity by faces and the speed of saccadic execution. This graph illustrates a negative correlation (nonparametric Spearman,
R = − 0.64, P < 0.05) between amplitude responses to faces at PO6–PO8 electrodes with the saccadic reaction time in the early time period (40–60 ms after stimulus onset).
The strongest the neuronal response to face stimuli was, the fastest was the prosaccade execution.
possible role of the FEFs in this modulation activity. Several
studies have shown that the FEF contributes to saccade target
detection through top-down signals that modulate activity of
visual neurons and, thus, target saliency (Moore and Arm-
strong 2003; Treue 2003). Moreover, in humans, the FEF exhi-
bits very early visual activation in response to visual stimuli
(Kirchner et al. 2009; Liu et al. 2009).
Our results further revealed distinct patterns of electro-
physiological activity associated with voluntary and reflexive
saccades at 110 ms after the stimulus onset, on average about
80 ms prior to the onset of the saccade. Antisaccades were
characterized by 2 successive topographical maps (110–170
and 170–200 ms) that were concomitant with a modulation of
the amplitude response over the central and parietal electro-
des. These additional processes in antisaccades could possibly
reflect the top-down inhibition of the reflexive, automatic pro-
saccade and the reprogramming of a voluntary saccade. In
fact, previous EEG studies have reported differences in a
similar time range between the programming of reflexive and
voluntary saccades and have identified the FEF, IPS, and the
DLPFC as good candidates for the source of the top-down
inhibitory control and saccade re-programming (i.e., Everling
et al. 1998; Mc Dowell et al. 2005; Clementz et al. 2007; Ptak
et al. 2011). Interestingly, a transient presaccadic increase in
alpha range brain oscillation (7–8H z) has been observed over
central–parietal electrodes in voluntary saccades starting 100
ms prior to the onset of the saccade and was interpreted by
the authors as a marker of suppression of bottom-up oculo-
motor capture (Mazaheri et al. 2011).
Early Target Selection to Faces in Prosaccades
Most interestingly, our study revealed a very early gain response
over right posterior parietal and parieto-occipital sites for pro-
saccades. This response modulation was specific to faces and
occurred at 40–60 ms following the onset of the stimulus. Cru-
cially, it was also predictive of the speed of the saccade
execution: The greater the amplitude over parieto-occipital sites
the faster the prosaccade toward faces. This is evidence for an
904 Face Selection in Reflexive Orienting Responses • Morand et al.
Downloaded from http://cercor.oxfordjournals.org/ at California Institute of Technology on July 11, 2015
early target selection to faces in reflexive orienting responses
over parieto-occipital cortex that facilitates the triggering of sac-
cades toward faces. Moreover, numerous studies have shown
hemispheric asymmetries for faces with preferential right over
left hemisphere processing (De Renzi et al. 1994; Wojciulik
et al. 1997) and, more specifically, an LVF advantage for face
processing (Burt and Perrett 1997; Luh et al. 1991; Dutta and
Mandal 2002; Schyns et al. 2002; Butler et al. 2005; Butler and
Harvey 2006, 2008; Yovel et al. 2008). These studies fit perfectly
with our finding of the early gain response occurring over the
right hemisphere (for targets in the LVF).
It is important to clarify that this finding does not contra-
dict the numerous studies demonstrating the link between the
N170 and face categorization (e.g., Schyns et al. 2007; Van
Rijsbergen and Schyns 2009; Vizioli et al. 2010) as our para-
digm did not require categorization. Participants were simply
asked to move toward or away from an upcoming target, and
the target contents were irrelevant to the task. The early face
effect described here for the prosaccades might instead indi-
cate a multiphase process in the representation of a face in
automatic spatial orienting, implying a rapid preselection for
faces in comparison with other nonface categories, followed
by subsequent stimulus categorization depicted by the N170.
Our data support that this hypothesis as a significant response
amplitude was found at 120–140 ms differentiating between
stimulus categories and noise patterns, a latency compatible
with the onset of the N170 component.
The rapid selection of faces in the reflexive saccades is
most probably due to the processing of the visual properties
of the stimulus, rather than to an effect of the faces on the
motor programming of the saccadic eye movements. We
argue that this as there was no overlap in time between the
face-specific modulation identified at 40–60 ms over
parieto-occipital sites in prosaccades and the effects due to
the programming of pro- and antisaccades (identified at 70–
90 ms over central sites for all stimuli categories). Further-
more, the early selection of faces cannot be accounted for by
the global low-level visual properties of the faces as these
were normalized across all stimulus categories. This ruled out
the possibility that the faces could be discriminated solely on
the basis of a bias in the global contrast, luminance or spatial
frequency content or, indeed, a difference in the spectral pro-
files of the contrasted categories (VanRullen and Thorpe
2001; VanRullen 2006; Honey et al. 2008; Schyns et al. 2003).
Thus, we think that the early selection for faces could either
be driven by high-level “social” properties (e.g., the global
appearance of a face, familiarity, expertise) or/and local low-
level physical properties intrinsic to faces (e.g., the high con-
trast present in the eye region, spatial frequencies carried by
face features). In any case, high-level or local low-level visual
properties, or their combination, render face stimuli more
salient than other visual objects and this could trigger their
early selection.
Our results bring a possible electrophysiological expla-
nation to recent studies showing fast saccadic detection/categ-
orization for faces in complex scenes in just 100 ms, both in
humans and monkeys (Crouzet et al. 2010; Girard and
Koenig-Robert 2011). The fast target selection to faces in invo-
luntary orienting responses in the parieto-occipital scalp
region reported here, together with the extreme rapidity of
saccades toward faces in saccadic detection/categorization
tasks (Crouzet et al. 2010; Girard and Koenig-Robert 2011)
places constraints on the brain mechanisms underlying the
processing of complex stimuli. It implies a fast integration
between the structures involved in the control of eye move-
ments and spatial attention, among those the FEF and the pos-
terior parietal cortex of the dorsal stream, the superior
colliculus, and the face fusiform area (FFA), part of the ventral
stream and responsible for face processing. The distribution
of neuronal latencies in different cortical areas (Nowak and
Bullier 1997; Schmoleski et al. 1998) precludes the possibility
that the saccadic categorization process uses multiple iter-
ations between brain regions before the motor response.
Visual information has been shown to rapidly reach the
human FEFs in very short latencies (Blanke et al. 1999), with
only 45 ms in response time to natural scene containing
faces (Kirchner et al. 2009). These latency data fit our
results over the posterior parietal and parieto-occipital scalp
regions. A rapid stimulus-driven enhancement in response
discriminability has been described in ventral area V4
quasi-instantaneously after microstimulation of FEF (Am-
strong and Moore 2007). A growing body of TMS studies has
demonstrated a role for FEF in modulating extrastriate cortex
activity with respect to the target (Grosbras and Paus 2003;
Silvanto et al. 2006; Taylor et al. 2007), in as early as 40 ms
(O’Shea et al. 2004; Morishima et al. 2009). Moreover, reduced
category selectivity to faces and scenes over the extrastriate
cortex has been described recently following a disruption of
the PFC by repetitive transcranial magnetic stimulation (Miller
et al. 2011). It is thus conceivable that the FEF, with its sensi-
tivity to faces, enhances the representation and selection of
faces through top-down modulating responses over extrastriate
cortex during spatial attention.
Given the absence of electrical source localization analysis
in this study and the low spatial resolution of the EEG tech-
nique, we can only speculate about the exact cortical areas
activated during the early face-specific ERP modulation at 40–
60 ms over the right posterior parietal and parieto-occipital
scalp sensors in reflexive saccades. Nevertheless, this early
modulation fits perfectly with crucial results reported by
Sadeh et al. (2011). For the first time, they demonstrated a
causal relationship between the activation of category selec-
tive (face and body) areas and ERP to these preferred cat-
egories, showing that early TMS stimulation (60–100 ms after
stimulus onset) to subjects’ individually defined right occipital
face area (OFA) significantly increased the subsequent N170
amplitude to faces. Complementary to this, we now report an
early face-specific modulation over similar ( parieto-occipital)
sites.
Moreover, Sadeh et al. (2010), in a combined EEG-fMRI
study found a high correlation between face selectivity in the
OFA and ERP selectivity around 100 ms, whereas the N170
face selectivity was not correlated with OFA face selectivity
but instead correlated with the FFA and pSTS ( posterior
superior temporal sulcus) activity. Thus, they argue that, in
Downloaded from http://cercor.oxfordjournals.org/ at California Institute of Technology on July 11, 2015
their experiment, the magnetic stimulation modulated neural
output from the OFA to face-selective areas in the temporal
cortex, which in turn directly contributed to the N170 com-
ponent (Sadeh et al. 2011). Apart from our early face-selective
modulation, we also found an N170 modulation on similar
scalp sites as described in Sadeh et al. (2010, 2011), yet in our
study, this modulation was object- but not face-specific. It is
possible that our analyses lacked the power to pick up these
sites and/or that, due to the normalization procedure, applied
to exclude low-level visual confounds across stimulus cat-
egories, our car stimuli might have been too similar to the
face stimuli to allow a distinction at this later component.
Nevertheless our data agree with Haxby et al.’s (2000) model,
which proposes feed-forward connections within the core
face processing system from the OFA to both the FFA and
pSTS. More specifically, we suggest a 2-stage process in the
representation of a face in involuntary spatial orienting with
an initial, rapid implicit processing of the visual properties of
a face (either social, high-level properties and/or physical
local low-level visual properties), not driven by global low-
level visual properties, followed by subsequent stimulus cat-
egorization depicted by the N170 component.
To conclude, we bring here electrophysiological evidence
of an early target selection in reflexive orienting to faces, oc-
curring over parieto-occipital sites at a very early stage of
saccade programming. We suggest that this fast selection for
faces is related to the implicit processing (or preprocessing)
of the visual properties of a face not driven by global low-
level visual properties.
Notes
We thank Gregor Thut for helpful discussion and Roberto Caldara
and Luca Vizioli for previous analyses. This work was supported by a
grant from the Economic and Social Research Council and the Medical
Research Council (RES-060-25-0010) awarded to all authors. Conflict
of Interest: None declared.
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