Isolating endogenous visuo-spatial attentional effects using the novel visual-evoked spread spectrum analysis (VESPA) technique.

Abstract

In natural visual environments, we use attention to select between relevant and irrelevant stimuli that are presented simultaneously. Our attention to objects in our visual field is largely controlled endogenously, but is also affected exogenously through the influence of novel stimuli and events. The study of endogenous and exogenous attention as separate mechanisms has been possible in behavioral and functional imaging studies, where multiple stimuli can be presented continuously and simultaneously. It has also been possible in electroencephalogram studies using the steady-state visual-evoked potential (SSVEP); however, it has not been possible in conventional event-related potential (ERP) studies, which are hampered by the need to present suddenly onsetting stimuli in isolation. This is unfortunate as the ERP technique allows for the analysis of human physiology with much greater temporal resolution than functional magnetic resonance imaging or the SSVEP. While ERP studies of endogenous attention have been widely reported, these experiments have a serious limitation in that the suddenly onsetting stimuli, used to elicit the ERP, inevitably have an exogenous, attention-grabbing effect. Recently we have shown that it is possible to derive separate event-related responses to concurrent, continuously presented stimuli using the VESPA (visual-evoked spread spectrum analysis) technique. In this study we employed an experimental paradigm based on this method, in which two pairs of diagonally opposite, non-contiguous disc-segment stimuli were presented, one pair to be ignored and the other to be attended. VESPA responses derived for each pair showed a strong modulation at 90-100 ms (during the visual P1 component), demonstrating the utility of the method for isolating endogenous visuo-spatial attention effects.

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Isolating endogenous visuo-spatial attentional effects using
the novel visual-evoked spread spectrum analysis
(VESPA) technique
Edmund C. Lalor,1,2,3Simon P. Kelly,1,2,4Barak A. Pearlmutter,5Richard B. Reilly2,3and John J. Foxe1,2,4
1The Cognitive Neurophysiology Laboratory, Nathan S. Kline Institute for Psychiatric Research, Program in Cognitive Neuroscience
and Schizophrenia, Orangeburg, NY 10962, USA
2The Cognitive Neurophysiology Laboratory, St Vincent’s Hospital Fairview, Dublin, Ireland
3School of Mechanical, Electrical and Electronic Engineering, University College Dublin, Dublin, Ireland
4Program in Cognitive Neuroscience, Department of Psychology, City College of the City University of New York, 138th Street &
Convent Avenue, New York, NY 10031, USA
5The Hamilton Institute, National University of Ireland Maynooth, Co. Kildare, Ireland
Keywords: EEG, P1, split spotlight, visual evoked potential
OnlineOpen:This article is available free online at www.blackwell-synergy.com

Abstract
In natural visual environments, we use attention to select between relevant and irrelevant stimuli that are presented simultaneously.
Our attention to objects in our visual field is largely controlled endogenously, but is also affected exogenously through the influence of
novel stimuli and events. The study of endogenous and exogenous attention as separate mechanisms has been possible in
behavioral and functional imaging studies, where multiple stimuli can be presented continuously and simultaneously. It has also been
possible in electroencephalogram studies using the steady-state visual-evoked potential (SSVEP); however, it has not been possible
in conventional event-related potential (ERP) studies, which are hampered by the need to present suddenly onsetting stimuli in
isolation. This is unfortunate as the ERP technique allows for the analysis of human physiology with much greater temporal resolution
than functional magnetic resonance imaging or the SSVEP. While ERP studies of endogenous attention have been widely reported,
these experiments have a serious limitation in that the suddenly onsetting stimuli, used to elicit the ERP, inevitably have an
exogenous, attention-grabbing effect. Recently we have shown that it is possible to derive separate event-related responses to
concurrent, continuously presented stimuli using the VESPA (visual-evoked spread spectrum analysis) technique. In this study we
employed an experimental paradigm based on this method, in which two pairs of diagonally opposite, non-contiguous disc-segment
stimuli were presented, one pair to be ignored and the other to be attended. VESPA responses derived for each pair showed a strong
modulation at 90–100 ms (during the visual P1 component), demonstrating the utility of the method for isolating endogenous visuo-
spatial attention effects.
Introduction
Much of what is currently known about the mechanisms and effects of
visual spatial attention in the brain is owed to advances in modern
electrophysiological and hemodynamic imaging techniques (e.g.
Kanwisher & Wojciulik, 2000; Luck et al., 2000). Of these techniques,
the event-related potential (ERP) method has been most informative in
uncovering the temporal dynamics of attentional processes in humans.
For example, the longstanding issue of whether spatial selection can
occur at the early sensory level, and not only at later levels of decision-
making and response programming, has seen major steps toward
resolution using ERPs (e.g. Luck et al., 1994; Hillyard & Anllo-Vento,
1998). Typically in such studies a comparison is made between the
responses to a stimulus when attended vs when unattended. Because
the responses to each of multiple stimuli presented together cannot be
separated in standard ERP data, stimuli must be presented in isolation
to the attended or unattended space at different times. This represents a
serious limitation of the technique, in that it is not possible to emulate
the more common real-life situation where both relevant and irrelevant
information are present in the visual field at the same time.
Aside from having lower ecological validity, there is a fundamental
limitation that stems from the stimulus presentation constraints in ERP
attention paradigms. This issue arises in designs attempting to assess
the physiological effects of endogenous attention using paradigms in
which suddenly onsetting stimuli appear in either a cued (and hence
attended) or uncued (unattended) location in space. Specifically, the
sudden onset of the stimuli may actually ‘grab’ attention exogenously,
either assisting the subject in attending to the cued location or causing
involuntary, transient reorienting from cued to uncued or ‘distracter’
locations, a phenomenon for which there exists a long line of evidence
(e.g. Jonides, 1981). Thus, it is not certain that the observed
modulations of electrophysiological responses to ‘endogenously’ cued
stimuli solely reflect endogenous attentional influences.
Correspondence: Dr J.J. Foxe,1The Cognitive Neurophysiology Laboratory, as above.
E-mail: foxe@nki.rfmh.org
Re-use of this article is permitted in accordance with the Creative Commons Deed,
Attribution 2.5, which does not permit commercial exploitation.
Received 31 July 2007, revised 29 September 2007, accepted 29 October 2007
European Journal of Neuroscience, Vol. 26, pp. 3536–3542, 2007
doi:10.1111/j.1460-9568.2007.05968.x
ª The Authors (2007). Journal Compilation ª Federation of European Neuroscience Societies and Blackwell Publishing Ltd

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Several ERP studies have attempted to disentangle the interactions
between endogenous and exogenous attention on visual processing
through manipulation of various aspects of the experiment design. For
example, the use of centrally and peripherally located cues to
emphasize endogenous and exogenous attention, respectively, has
been reported (Fu et al., 2005; Hopfinger & West, 2006). Manipu-
lation of the likelihood of stimuli appearing at particular locations has
also been used to emphasize endogenous vs exogenous attention
(Natale et al., 2006). However, all of these experiments utilize
suddenly onsetting stimuli to measure endogenous and exogenous
attention alike and, thus, are still somewhat confounded.
The VESPA (visual-evoked spread spectrum analysis) technique
recently developed by our group (Lalor et al., 2006) allows for the
measurement of electrophysiological activity in response to each of
several simultaneously presented stimuli with high temporal resolu-
tion, thus overcoming the abovementioned limitations. In this paper
we aim to utilize this VESPA method to establish the time range over
which electrophysiological effects of sustained endogenous attention
to a visual stimulus are seen while ignoring another concurrent visual
stimulus.
Materials and methods
Subjects
Fifteen healthy subjects (three female) aged between 20 and 41 years
participated in the study. All had normal or corrected-to-normal vision.
The experiment was undertaken in accordance with the Declaration of
Helsinki, and the Ethics Committee of St Vincent’s Hospital in Dublin,
Ireland approved the experimental procedures and each subject
provided written informed consent.
Experimental paradigm
The stimulus configuration is shown in Fig. 1 (left panel). It consisted
of four checkerboard-patterned segments of an annulus, the inner
diameter of which subtended 1? of visual angle and the outer diameter
7?. The refresh rate of the monitor was set to 60 Hz and, during trials,
the contrast of the checkerboard pattern in each segment was
modulated on every refresh by a stochastic waveform to facilitate
the estimation of the VESPA (Lalor et al., 2006; see also VESPA
analysis section below). For all of the trials the upper-left and lower-
right segments (‘UL–LR’) were modulated together using one signal,
and the lower-left and upper-right segments (‘LL–UR’) using another.
Thus, the four segments can be considered as two pairs.
A sequence of black symbols from a set of five, one of which was
defined as the target (Fig. 1 right panel), was superimposed on the
center of each checkerboard segment. This target could be identified by
the presence of a diagonal bar running through its center. Subjects were
required to respond with a button press on detection of target symbols
appearing in both attended segments simultaneously (‘valid’), while
ignoring the opposite pair of segments (‘invalid’). A different stream of
symbols was displayed in each of the four segments at all times, with a
change in the symbols occurring every 11 frames, i.e. every 183 ms,
with no interval between symbols. It has been reported that the
minimum time needed to identify a target at one location and then
switch attention to identify a target at a second location is in the range
of 200–500 ms (Mu ¨ller et al., 1998). The brief durations used in the
present study suggest therefore that it would be impossible to achieve a
high rate of target-pair detections using a switching strategy and that
accurate performance could only be achieved by dividing attention
between the two locations. Target symbols occurred equally often in all
segments. If a target symbol appeared in only one segment of a pair, it
was guaranteed that a target symbol would not appear in the other
segment of that pair on the next change. Target-pairs appeared equally
often at random intervals in both attended and unattended segment-
pairs and were separated in each pair by a minimum of 733 ms, with a
mean (± SD) rate of 8.5 (± 2.5) target-pairs per segment-pair per trial
(i.e. one every 4.7 s on average). A video illustrating the experiment
can be seen in the Supplementary material (Video S1).
Each subject underwent a total of 20 runs, each consisting of five
trials. Each trial lasted 40 s after which there was a 20 s break before
the next trial. During the break periods the setup shown in Fig. 1 left
panel was displayed on the screen with the corresponding targets
displayed in each segment and no modulation of the contrast of the
checkerboard segments. Prior to the start of every trial (1200 ms) a
warning stimulus was presented, wherein the targets in one pair of
segments flickered off for 200 ms, on for 800 ms and back off for the
remaining 200 ms indicating the segment-pair to be attended during
the upcoming trial. The pair of segments to be attended to alternated
with every trial with the initial pair counterbalanced across subjects.
Behavioral performance
Because the paradigm did not involve a simple ‘go⁄no-go’ task, the
sequence of stimuli had to be examined carefully in order to determine
whether or not a button press was actually made in response to the
presentation of a double-target in the to-be-attended segments. For
example, while a button press may have occurred after the presentation
of a double-target in the to-be-attended segments, it is possible that it
was actually in response to a double-target in the to-be-ignored
segmentsandthatthesubjectwasinfactnotcomplyingwiththetask.To
fully account for this possibility, the data were examined in two ways.
In the first analysis all responses occurring in the interval 200–
1000 ms following target symbols appearing in any segment were
accounted for in the following order:
(1) valid double-target;
(2) valid single-target;
(3) invalid double-target;
(4) invalid single-target.
Fig. 1. (left panel) Stimulus setup showing UL–LR stimulus at one contrast
level and LL–UR stimulus at another contrast level. Target symbols are shown
in the UL–LR stimulus. (right panel) The symbols displayed in the upper right
segment, with the target symbol for all runs shown at the bottom.
Isolating endogenous attention using the VESPA 3537
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Responses counted towards each successive category were
excluded from the remaining categories. In the second analysis, the
order was rearranged so that the invalid targets were considered first.
Eye movement control
Subjects were required to maintain central fixation during all trials.
While we reasoned that the nature of the divided attention task would
be such as to discourage eye movement given the rapid rate of change
of the symbols (183 ms), electrooculographic (EOG) data were
recorded and examined to explicitly monitor this. Horizontal EOG
(HEOG) was recorded from the outer canthi of the eyes and each was
referenced to the nasion. During a trial, if the HEOG for one eye was
above 16 lV concurrent with the HEOG for the other eye being below
)16 lV a deviation from fixation was deemed to have occurred and
the trial was rejected. This limit, which may be considered conser-
vative in light of the experimental design, resulted in a mean rejection
rate of 15% of trials.
Electroencephalographic (EEG) acquisition
EEG data were recorded from 72 electrode positions referenced to
location Fz, filtered over the range 0–134 Hz and digitized at a rate of
512 Hz using the BioSemi Active Two system. Offline, the EEG was
digitally filtered with a passband of 1–35 Hz.
VESPA analysis
The VESPA is an estimate of the first order impulse response of the
visual system (Lalor et al., 2006). It is based on the assumption that
the EEG response to a stimulus whose luminance or contrast is rapidly
modulated by a stochastic signal consists of a convolution of that
signal with an unknown impulse response. That is, we assume that the
known rapid stimulus modulation signal causes correlated activity in
the EEG. Thus, a reverse correlation procedure facilitates estimation of
the impulse response, which, when convolved with the input stimulus
signal, approximates the output EEG. This impulse response function
is known as the VESPA. As mentioned above, in the present study the
contrast of the checkerboard patterns in each segment was modulated
on every refresh of a monitor set to 60 Hz. The signals that controlled
these contrast modulations had their power spread uniformly over the
range 0–30 Hz. It is important to realize that the VESPA is not a
response to the onset of any particular discrete event. It is derived over
a period of time from the continuous stimulus and the concurrently
recorded EEG. The VESPA itself is plotted on a time axis that
indicates the relationship between the incoming stimulus signal at any
particular time and the output EEG a certain fixed time later. It should
also be noted therefore that the estimation of the VESPA in this study
is unrelated to the symbols superimposed on the modulating
checkerboard segments.
The profiles of these VESPAs are highly correlated with those of
transient visual evoked potentials (VEPs). However, unlike the
transient VEP, multiple stimuli driven by orthogonal modulating
signals can be simultaneously presented within a visual display and a
separate VESPA can be derived for each. It is not necessary for these
signals to have differing frequency distributions, they can simply be
different instantiations of the same random process, i.e. they can have
exactly the same statistics. In the present study, using the data from
every 40-s trial and the corresponding contrast modulation signals, we
simultaneously derived a VESPA for each of two pairs of non-
contiguous disc segments, while subjects attended to one pair and
ignored the other. We then averaged VESPA responses for each pair
and condition across trials. The same two stochastic signals were used
for all trials. The assignment of signals to segment-pairs was switched
after 10 runs, with the starting assignment counterbalanced across
subjects.
VESPAs were measured using a sliding window of 500 ms of data
starting 100 ms prestimulus. This results in a VESPA plotted on a time
axis from )100 ms to 400 ms. Therefore, the VESPA at )100 ms, for
example, indexes the relationship between the input noise signal and
the EEG 100 ms earlier; obviously this should be zero. As another
example, the VESPA at 100 ms indexes how the input noise signal
affects the EEG 100 ms later.
In an effort to improve the signal-to-noise ratio (SNR) of the
VESPAs we carried out blind source separation of the data as a pre-
processing step. This resulted in an improvement in SNR for the
average VESPA, from 12.9 dB to 17.7 dB, where the SNR was
calculated by defining the noise as the mean of the squared values in
the 100-ms interval immediately preceding the stimulus, and the signal
as the mean of the squared values in the interval 35–175 ms post-
stimulus. The details of the blind source separation method are
provided in the supplementary Appendix S1.
Results
Behavioral performance
The behavioral performance on the task, averaged across all trials and
subjects is shown in Table 1 and confirms that subjects were
deploying their attention correctly. The first two columns list the
percentage of 200–1000-ms intervals following the presentation of
targets that contained a response, when the to-be-attended segments
were considered first, i.e. the first analysis outlined above. In this case,
when the interval following the presentation of a target-pair in the to-
be-attended segments was checked for a response, one was present in
68% of cases. In contrast, when the to-be-ignored segments were
considered first (third and fourth columns), just 10% of intervals
following a target-pair in the to-be-ignored segments contained a
response. There was no significant difference in behavioral perfor-
mance between attending to the UL–LR segments and the LL–UR
segments F1,14¼ 0.38, P > 0.5.
Attentional modulation of the VESPA
Figure 2 shows the group average VESPAs for the UL–LR and
LL–UR stimuli, in the cases where they were attended and unattended,
for six representative parieto-occipital electrode locations. Because
of the prevalence of attentional modulations of the P1 component in
the VEP literature, we first wished to test the hypothesis that a
Table 1. Behavioral results averaged across subjects
To-be-attended first To-be-ignored first
UL–LRLL–UR UL–LRLL–UR
To-be-attended double
To-be-attended single
To-be-ignored double
To-be-ignored single
68%
3%
?0%
?0%
67%
3%
?0%
?0%
15%
10%
10%
?0%
15%
9%
10%
?0%
The first two columns list the performance determined by accounting for
responses to valid segments first, and the second two columns list that deter-
mined by accounting for responses to invalid segments first.
3538E. C. Lalor et al.
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Fig. 2. Plots of the VESPAs to the attended
and unattended stimuli for six occipito-parietal
electrodes for both the UL–LR (upper panel) and
LL–UR (lower panel) trials. Significant P1
attention effects are highlighted in gray.
Fig. 3. Scalp topographies of the attention effects averaged across the
90–100 ms range (P1), and across all subjects for both the UL–LR (upper
panel) and LL–UR (lower panel) stimuli for the attended and unattended
cases, and the difference between the attended and unattended cases.
Isolating endogenous attention using the VESPA3539
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similar effect would be seen with the VESPA. We defined the
P1-dependent measure as the average amplitude in the interval
90–100 ms, selected on the basis of peak latencies in group-average
waveforms. Attentional modulations of the P1 component were
statistically tested first via an omnibus 2 · 2 · 3 · 3 anova with
factors of stimulus (UL–LR vs LL–UR), attention (UL–LR vs
LL–UR), region(threelevels;
Oz⁄POz⁄Pz; and right: O2⁄PO4⁄PO8 scalp) and electrode (three
levels;O1⁄Oz⁄O2;PO3⁄POz⁄PO4;
restricted our analysis to these electrode locations based on the
scalp distribution of VESPA amplitude being confined to posterior
regions (Fig. 3).
Confirming the principal hypothesis of the study, a strong
interaction was found between stimulus and attention (F1,14¼ 9.32,
P < 0.01). As can be seen in Fig. 2, this was driven by greater VESPA
P1 amplitude when each stimulus was attended compared with when
unattended. A main effect of electrode (F2,28¼ 8.96, P < 0.005) and
a marginal effect of region (F2,28¼ 3.89, P ¼ 0.055) alluded to the
topographic specificity of the P1.
Also, a four-way interaction between all factors (F4,56¼ 3.94,
P < 0.01)indicatedadegreeoftopographicspecificityintheattentional
modulation of the P1. Post hoc comparisons revealed that the effect of
attentiononLL–URstimulireachedsignificance atallelectrodes across
the three regions (P < 0.05), and on UL–LR stimuli at electrodes O1,
PO7, Oz, O2 and PO8 (all P < 0.05; highlighted in gray in Fig. 2). To
test for a possible hemispheric bias of the P1 attentional modulation, a
follow-up anova was carried out using the attended-minus-unattended
difference as the dependent measure, with the two factors of stimulus
(UL–LR vs LL–UR) and hemisphere (left: PO3; right: PO4). However,
no interaction was found (F1,14¼ 0.06, P > 0.5).
The ‘N1’ and ‘P2’ components, measured as the average amplitude
in the interval 105–120 ms and 130–145 ms, respectively (see Fig. 2),
were subjected to the same omnibus anova as the P1. In both cases,
no interaction was found between stimulus and attention (‘N1’:
F1,14¼ 0.19, P > 0.5; ‘P2’: F1,14¼ 0.18, P > 0.5).
left: O1⁄PO3⁄PO7;midline:
andPO7⁄Pz⁄PO8). We
Discussion
In this study we have quantified, with detailed temporal precision, the
electrophysiological effects of endogenous attention to a subset of
non-contiguous, simultaneous, continuously presented stimuli. Our
paradigm avoids using suddenly onsetting stimuli and, in so doing,
avoids bringing confounding exogenous attentional effects into play.
We found a strong attentional enhancement of the amplitude of the
VESPA in the range of the P1 component (90–100 ms), indicating that
endogenous attention occurs during the early stages of sensory
processing.
Modulation of the P1 component of the transient VEP in visual
spatial attention studies has been reported widely (e.g. Hillyard et al.,
1995; Mu ¨ller & Hillyard, 2000). Unlike other studies in which the
amplitude of multiple N1 (140–200 ms) and⁄or later components (N2,
P300) of the transient VEP have been enhanced with attention
(Mangun & Hillyard, 1987; Rugg et al., 1987; Heinze et al., 1990), no
enhancement of VESPA components other than the P1 was observed
here. While the waveforms for the LL–UR stimulus in Fig. 2 suggest
that there may be attentional enhancements of the negative peak at
175 ms, this did not appear to be the case for the UL–LR segments,
and no significant effects were found.
The notion that only endogenous, and not exogenous, attentional
orienting mechanisms are called upon in this paradigm may be the
reason for the restricted timeframe of the modulations found in the
present study. Our finding is consistent with Natale et al. (2006), who
reported that attentional modulation of the P1 component of the VEP
reflected endogenous mechanisms, while modulation of the N1
component represented exogenous attention. They suggest that the
P1 effect might index an attentional facilitation of early sensory
processing while the N1 effect may index exogenous orienting of
attention, possibly representing activity of frontal and parietal
components involved in eliciting attention changes. This finding
contrasts with the study of Hopfinger & West (2006) who reported that
exogenous attention dominated the late phase of the P1 component,
regardless of where endogenous attention had been orientated and that
endogenous attention dominated a later, higher-order stage of
processing indexed by an enhancement of the P300 that was
unaffected by exogenous attention. These conflicting findings further
highlight the difficulty in disentangling endogenous and exogenous
attention effects using suddenly onsetting stimuli. It is worth noting
that a direct comparison of VESPA and standard transient VEP
componentry may not be straightforward; one apparent difference is
that the succession of components of alternating polarity appears to
proceed in a shorter timeframe in the VESPA. However, as we have
not measured transient VEPs from corresponding stimuli here, this
cannot be judged definitively. In fact, differing behavior between the
‘P1’ components in the VEP and VESPA has already been seen in a
recent study on schizophrenia, suggesting that in each case the P1
reflects activity of a distinct subpopulation of cells (Lalor et al., 2007).
Future work will aim to elucidate the relationship between VESPA
components and those of the transient VEP. For example, examining
the retinotopic sensitivity of components of the VESPA (e.g. polarity
inversion of the earliest C1-like component for upper- vs lower-field
stimuli) will help to establish their cortical origins, as has been done
with the standard VEP (Di Russo et al., 2002).
Another possible explanation for the narrow timeframe of the
attention effect in the present study is that the task demands inherent in
the paradigm may be such that selection is required only at this level.
The timeframe of the P1 (90–100 ms) may be the critical point at
which targets can be fully classified on the basis of the presence of
centrally located diagonal bars within the symbols in both non-
contiguous locations. That selection could be so finely titrated in the
system may also be particular to the situation where stimuli are
continuously and⁄or simultaneously presented.
The scalp distributions of Fig. 3 provide further illustration of the
attentional modulations during the P1 timeframe. These modulations
were restricted to a relatively small number of posterior electrode
sites. Somewhat surprisingly, the VESPA P1, which has previously
been shown to be restricted to a unimodal midline occipital focus,
displays a similar unimodal focus in this study, despite the paired
stimuli. It is also interesting to note that the distribution of the
difference between the attended and unattended cases, i.e. the
attentional effect, is quite different from that of the response to the
stimulus itself. Though this appears at odds with the common finding
of matched topographies in the difference (attended minus unat-
tended) and unattended conditions (Hillyard & Anllo-Vento, 1998), it
must be considered that the modulations here are measured from
continuous stimuli and thus may receive contributions from control
processes as well as the expression of sensory biasing. This idea will
be investigated in further work.
The ability to assess the timing of electrophysiological effects of
attention using displays containing multiple, continuously presented
elements has other advantages. It allows for the design of more
ecologically valid experimental paradigms and the investigation of
questions that were hitherto very difficult to answer conclusively, and
it also addresses the practical issue that certain attention experiments
carried out using functional magnetic resonance imaging (fMRI) have
3540E. C. Lalor et al.
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not been replicable in ERP designs. In fMRI experiments responses to
each of multiple stimuli can be isolated in retinotopic visual areas with
high spatial resolution (e.g. McMains & Somers, 2004). However, the
low temporal resolution of fMRI precludes examination of the precise
temporal dynamics of the attentional effects. The activation of the
lower-tier visual areas suggests that attention may be expressed in a
modulation of activity at the earliest hierarchical stages; however, it is
possible that the modulation of activity in those areas reflects feedback
of later processing (e.g. Martı ´nez et al., 1999). One example is the
study of McMains & Somers (2004) on the splitting of the attentional
spotlight. This study employed multiple simultaneously presented
stimuli to show that attention divided over non-contiguous regions of
space is expressed in low-level visual areas. Similar split-spotlight
effects were seen using the steady-state visual-evoked potential
(SSVEP) technique (Mu ¨ller et al., 2003), which, like fMRI, lacks
the ability to resolve the temporal profile of modulation.
The results of the present study address this issue of the timing of
the division of visual spatial attention. The experimental paradigm
based on the VESPA has allowed us to analyse, in detail, the timing
of attentional effects on responses to stimuli in non-contiguous
regions of space. It should be noted that in our stimulus configuration
there was no intervening distracter between the regions to be
attended. As a result, there is the possibility that subjects, rather than
splitting their attention, may have performed the task by elongating a
unitary spotlight into such a formation as to encapsulate the regions
where the targets were expected to appear, while remaining spatially
contiguous through the fixation point. However, in a follow-up to
their earlier study, McMains & Somers (2005) investigated the
processing efficiency of split-spotlight attention mechanisms com-
pared with that of a ‘zoom lens’ unitary beam. Using behavioral
measures and retinotopic BOLD signal activation amplitude, the
authors concluded that, when attention is spread over the same
spatial extent, there is significant benefit for dividing attention. Given
the difficulty of the task described in the current study and the
successful performance of that task by the subjects, it is likely that
the subjects sought to harness this benefit by splitting their
attentional spotlight. Mu ¨ller et al. (2003) also demonstrated improved
behavioral performance for the split-spotlight case compared with
attention to adjacent stimuli, which again points to spotlight division
as an optimal strategy.
Another unresolved issue in ERP attention research is whether
spatial attention can operate in foveal vision. A number of fMRI
studies have demonstrated the ability of attention to modulate activity
corresponding to visual field areas both inside and outside foveal
vision (e.g. Tootell et al., 1998; Brefczynski & DeYoe, 1999). These
studies used multi-element displays with subjects required to attend to
some stimuli while ignoring others. In a recent EEG study (Handy &
Khoe, 2005), however, attention-related increases in the P1 ERP
component were found only to target locations in parafoveal vision
(2.2? from fixation), with no similar effect observed to targets located
within foveal vision. This study used a cuing paradigm with single
stimulus presentations, which may explain the incongruity between
the fMRI and EEG findings. While the paradigm described in the
current study was not designed to address this question, it is clear that
the P1 modulations observed herein and the flexibility of the VESPA
method would facilitate the design of a paradigm that would be
suitable to investigate this further.
In summary, we have utilized the novel VESPA method to examine
the electrophysiological effects of visual spatial attention to multiple,
continuously presented stimuli. This has allowed us to resolve the
timing of the deployment of endogenous attention in isolation. The
strong modulations found in the 90–100-ms range demonstrate that, in
the current paradigm, endogenous attention is expressed in modulation
of activity during early stages of sensory processing.
Supplementary material
The following supplementary material may be found on http://
www.blackwell-synergy.com
Appendix S1. The blind source separation method.
Video S1. A video illustrating the experiment.
Acknowledgements
The authors thank Dr Sherlyn Yeap for excellent assistance in the lab. This
work was supported by a US National Science Foundation grant BCS0642584
to J.J.F., and by a Fund for Digital Research Programme grant from the Higher
Educational Authority of Ireland to R.B.R. The authors would like to express
their sincere gratitude to the Chief Executive Officer at St Vincent’s Hospital,
Mr Edward Byrne and to the Director of Nursing, Mrs Phil Bourke, for their
ongoing and essential support of the Cognitive Neurophysiology Laboratory.
Abbreviations
EEG, electroencephalogram; EOG, electrooculogram; ERP, event-related
potential; fMRI, functional magnetic resonance imaging; HEOG, horizontal
electrooculogram; SNR, signal-to-noise ratio; SSVEP, steady-state visual-
evoked potential; VEP, visual-evoked potential; VESPA, visual-evoked spread
spectrum analysis.
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