NeuroImage 55 (2011) 669–680

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Neural representation of feature synergy

Tetsuo Kida a,b,c,⁎, Emi Tanaka a, Yasuyuki Takeshima a, Ryusuke Kakigi a

a Department of Integrative Physiology, National Institute for Physiological Sciences, Okazaki, Japanb Japan Society for the Promotion of Science, Tokyo, Japanc Department of Neurobiology and Behavior, Graduate School of Biomedical Sciences Nagasaki University, Nagasaki, Japan

⁎ Corresponding author. National Institute for PhysiolIntegrative Physiology, 38 Nishigonaka, Myodaiji, Okaz564 53 7913.

E-mail address: nikita@nips.ac.jp (T. Kida).

1053-8119/$ – see front matter © 2010 Elsevier Inc. Aldoi:10.1016/j.neuroimage.2010.11.054

a b s t r a c t

a r t i c l e i n f o

Article history:Received 9 February 2010Revised 11 November 2010Accepted 16 November 2010Available online 25 November 2010

Keywords:Feature synergySignal detection theoryProbability summationVisual evoked potentials (VEPs)

Interactive non-linear cooperation of different feature dimensions, feature synergy, has been studied inpsychophysics, but the neural mechanism is unknown. The present study investigated the neuralrepresentation of feature synergy of two second-order visual features by combining electroencephalography(EEG) with the signal detection theory (SDT). Two kinds of a 27-by-27 array of Gabor patches were presentedin a random order; a reference stimulus which has no segregated region, and a target stimulus whose innerregion differed in spatial frequency, orientation, or both from the surround. Subjects performed a Yes–Nodiscrimination of whether the inner region was different from the surround, while EEG signals were recordedfrom 62 locations. When the SDT measure showed feature synergy, EEG activity showed a long-lastingenhancement starting at 130 ms around the inferior temporal region. In contrast, no EEG modulation wasobserved when feature synergy was not present. Thus, our combined approach demonstrates that non-linearcooperation between different features is represented by neural activity starting at 130 ms post-stimulus inthe ventral visual stream.

ogical Sciences, Department ofaki 444-8585, Japan. Fax: +81

l rights reserved.

© 2010 Elsevier Inc. All rights reserved.

Introduction

The visual system is believed to have separate modules orprocesses specialized for different features, such as luminance,contrast, orientation, spatial frequency and color. A number of studieswith patients (Damasio et al., 1980; Meadows, 1974; Zeki et al., 1991;Zihl et al., 1983) and neuroimaging (Corbetta et al., 1991; Gulyas andRoland, 1991; Sereno et al., 1995) have reported cortical specializa-tion corresponding to these processes. However, it remains a matterof debate whether the different features are processed in anindependent manner or interact with each other.

Psychophysical experiments have demonstrated that differentvisual features are processed in independent pathways but alsointeract with each other in a variety of tasks (Kubovy et al., 1999;Meinhardt and Persike, 2003; Meinhardt et al., 2006, 2004; PersikeandMeinhardt, 2006, 2008; Treisman and Sato, 1990;Wilkinson et al.,1997; Wilson and Wilkinson, 1997; Wilson et al., 1997). Theinteraction between feature dimensions (e.g., orientation and spatialfrequency) is examined by measuring the alteration of performancewhen the observer discriminates targets that differ in more than onefeature dimension from the surround. If performance with more thanone feature is better than expected from the assumption of

independent processing of each individual feature, then this indicatesthat there is an interactive non-linear cooperation between feature-specific modules, termed “feature synergy” (Kubovy and Cohen, 2001;Kubovy et al., 1999; Meinhardt and Persike, 2003; Meinhardt et al.,2006, 2004; Persike and Meinhardt, 2006, 2008). However, the neuralsystem underlying this non-linear cooperation between differentfeature dimensions is still unknown.

In the present study, we used electroencephalography (EEG) toreveal the neural representation of feature synergy between spatialfrequency and orientation. Two types of a 27-by-27 array of Gaborpatches (Gabor random field, GRF) were presented in a random order,a reference GRF stimulus which consists of a homogenous pattern ofGabor patches and thus has no segregated region, and a target GRFstimulus that has an inner region (a 9-by-9 array) statisticallydifferent in spatial frequency, orientation or both from the surround,which consists of the same pattern as the reference stimulus (Figs. 1and 2). Observers can discriminate better the inner region of thetarget GRF stimulus from the surround as feature contrast betweenthe inner and outer regions increases. The focus of this study is to seethe non-linear improvement of discrimination performance (featuresynergy) and corresponding EEG modulations when the inner regionof the target GRF stimulus is defined by two features in comparisonwith a single feature. We hypothesized that, in conjunction withpsychophysical evidence for feature synergy, there will be EEGactivity that is modulated for the double-feature target stimuluscompared with that for the reference stimulus, but not for the singlefeature target stimulus. The signal detection theory-based approachemployed in the present study enables us to demonstrate the neural

Fig. 1. Stimuli used in the present study. (A) Gabor random field (GRF) stimuli consisting of a 27-by-27 array of Gabor patches. The upper left image shows a reference GRF stimulus,and the lower left shows a target GRF stimulus. Spatial frequency and orientation parameters of each Gabor patch were randomly sampled from the Gaussian distribution which isdrawn at side each. The inner region of the target GRF stimulus displayed here differs in both spatial frequency and orientation parameters from the surround. The dotted black linewas not present in actual experiments. (B) Stimulus sequence. In experiment 1, only the reference GRF stimulus was presented as frame 2 without the target. In experiments 2 and 3,either of the target or reference stimulus was presented as frame 2.

670 T. Kida et al. / NeuroImage 55 (2011) 669–680

representation of non-linear cooperation between different featuresas explained in more detail in the Materials and methods.

Materials and methods

Two psychophysical and three EEG experiments were carried outto examine the neural representation of feature synergy. First, apreliminary psychophysical experiment was conducted to determineparameters of a reference stimulus to be used in the subsequentpsychophysical and EEG experiments. Second, a psychophysical

experiment was performed to determine parameters (orientationand spatial frequency) of a target stimulus best to cause featuresynergy in individuals for the subsequent EEG experiment. Third, theEEG experiment using appropriate stimulus parameters, which hadbeen determined in the prior psychophysical experiments, wascarried out to observe simultaneously feature synergy and its neuralrepresentation. In this experiment, target discriminability was low,which has been reported to produce a clear synergy. The next EEGexperiment examined whether the synergy is present or not andwhether the corresponding EEG modulation is present or not, when

Fig. 2. Examples of target GRF stimuli. From left to right, orientation-defined (φ), spatialfrequency-defined (f) and double-feature (φ+ f) GRF stimuli are shown.

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target discriminability is high. In the third EEG experiment, weexamined whether the EEG modulation when feature synergy ispresent is independent of the alteration of target discriminability.

Subjects

Twelve healthy subjects (2 women and 10 men) with normal orcorrected-normal vision, aged 24 to 45 years old, participated in twopsychophysical experiments and the first EEG experiment. Tensubjects participated in the remaining two EEG experiments. Allsubjects gave written informed consent prior to the study, which wasfirst approved by the Ethics Committee at the National Institute forPhysiological Sciences.

Stimulus

Stimuli were a 27-by-27 array of Gabor patches on a greybackground. In Gabor patch texture, orientation and spatial frequencycan be separately manipulated with little luminance and aliasingartifacts (Landy and Bergen, 1991). Each of the Gabor patches had adiameter of about 0.41° visual angle with a standard deviation of theGaussian envelope equal to 0.0815°. Orientation and spatial frequencyparameters of each Gabor patch were sampled randomly fromindependent Gaussian distributions (Fig. 1A, right). Therefore, wecall this stimulus as the Gabor random field (GRF) stimulus, accordingto Persike and Meinhardt (2006) (Figs. 1 and 2). The theoreticaldistribution of the two parameters is a two-dimensional normaldistribution N [(μf|σf), (μφ|σφ)] with density

g f ;ϕð Þ = 12πσfσϕ

exp −12

f−μfσf

� �2+

ϕ−μfσϕ

!2 !" #

where μ and σ are, respectively, the mean and standard deviation ofthe Gaussian distribution to be used for sampling orientation andfrequency parameters of Gabor patches, f is spatial frequency (incycles per degree, cpd), and φ is the orientation (in degrees, deg) ofGabor patches.

For reference GRF stimuli (Fig. 1A, upper left), parameters of eachGabor patch were sampled from the Gaussian distribution with fixedvalues μ0 and σ0 for each of the two feature dimensions. The fixedvalues μ0 and σ0 were determined in the first psychophysicalexperiment (Experiment 1).

For target GRF stimuli (Fig. 1A, lower left), parameters of eachGabor patch in a 9-by-9 stimulus array in the center of a 27-by-27array was sampled from the Gaussian distribution different in one ortwo feature parameter(s) from the surround. Parameters of Gaborpatches in the surround were sampled from the same Gaussiandistribution as the reference GRF stimulus. That is, a target GRFstimulus consisted of both an outer part with the same parameters asthe reference stimulus and an inner part with different parameter(s)from the reference stimulus.

The visual stimuli were generated using a VSG Visage stimulusgenerator (Cambridge Research System) and displayed on a Sony

Trinitron Color Monitor (Sony, GDM-F520). The refresh rate of themonitor was 60 Hz at a horizontal frequency of 81.4 MHz, and thepixel resolution was set to 800 by 600 pixels. A GRF stimulus waspresented in the center of the monitor with a range of 600 by 600pixels (10.86 by 10.86 degrees). The mean luminance of the screenwas 50 cd/m2. All Gabor patches were displayed with a fixedMichelson contrast of 100%. Color values were taken from a lineargrey staircase consisting of 256 steps (0–255), the medium step (128)always referring to a grey value. To ensure accurate reproduction ofstimulus contrast or absolute luminance, gamma correction wascarried out using a measuring device, OptiCAL. The VSG systemoutputs a sequence of 256 voltage levels for each active color-gun in atarget area on the display, and the light output was measured usingOptiCAL. Then, inverse curves were calculated to correct for themonitor's non-linearity.

Experiment 1 (determination of parameters for the reference stimulus)

To establish parameters for the reference GRF stimuli to be used insubsequent psychophysical and EEG experiments, reference stimuliwith several parameters were presented as follows. The centroid (i.e.,mean) of the joint spatial frequency and orientation distributionof reference GRF stimuli was determined arbitrarily (μ0 (f) =7.0 cpd,μ0 (φ)=36°), while the standard deviation was varied in one featuredimension and set to zero in the other. Each trial was performed insequences shown in Fig. 1B, and the subjects had to rate the variabilityof the texture patterns on a nine-category rating scale, ranging from“absolute homogeneous” (1) to “absolute heterogeneous” (9). Valuescorresponding to a rating of 3 were used as the standard deviationparameters σ0(f) and σ0(φ) for defining reference GRF stimuli and theouter region of target GRF stimuli. In actuality, these were σ0 (f)=0.8(cpd) and σ0(φ)=9.7 (deg), which were used in all the subsequentexperiments (see Tables 1, 2 and 3).

Experiment 2 (determination of parameters for the target GRF stimulus)

Determination of feature dimension parametersThe discriminability of the inner target region is calibrated to

present the double-feature target stimulus consisting of two differentfeature parameters which produces the same discriminability inindividual feature dimensions, because feature contrast is different inquality between different features (orientation and spatial frequency)and cannot be equalized between them. In particular, this is essentialfor examination of feature synergy, because the degree of featuresynergy depends on discriminability. Therefore, the purpose of thisexperiment was to calibrate discriminability across different featuredimensions. This was done using the following procedure.

Each trial consisted of the GRF stimulus of 500 ms duration,immediately followed by a mask of 250 ms duration, and then a2250 ms interval frame with a grey image (Fig. 1B). Reference andtarget GRF stimuli were presented in a random order at an equalprobability under several different conditions where the mean of eachfeature parameter distribution was varied, and subjects performed aYes–No discrimination task. In this task, subjects judged whether theinner region of the GRF stimulus looked different from the outerregion (target) or the whole GRF stimulus contained only onehomogenous region (reference). The mask stimuli were squares filledwith spatial pixel white noise having a resolution of 3 pixels. About 5 safter an experimenter told the subject to start, the trial started and afixation point was presented in red on the grey background. The firstGRF stimulus was presented 3 s after the fixation point had beenpresented. The fixation point was presented throughout a block. Theparameters of Gabor patches were randomly sampled from theGaussian distribution in each trial, i.e., every GRF stimulus displayedon the monitor was the result of a new sampling process in each trial.The Yes–No judgment by subjects was made using a button-pressing

Table 1Across-subject mean (and S.E.) of mean (μ) and standard deviation (σ) parametervalues of Gaussian distributions for sampling spatial frequency and orientationparameters of Gabor patches in target and reference GRF stimuli used in experiment 3.

Gabor path parameters Spatialfrequency

Orientation

Gaussian mean and SD parameters μ σ μ σ

Inner region of target GRF stimulusSpatial frequency-defined 7.8(0.1) 0.8 36 9.7Orientation-defined 7 0.8 42.7(1.7) 9.7Double-feature 7.8(0.1) 0.8 42.7(1.7) 9.7

Reference GRF stimulus 7 0.8 36 9.7

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device with two buttons. After practicing for a few minutes, eachsubject performed the task with 8–12 feature parameter levels of 2feature dimensions (spatial frequency and orientation). Each condi-tion consisted of 64 trials (reference 32, target 32), thereby resultingin at least 512 target and 512 reference trials. Based on the hit andfalse alarm rates obtained in the experiment, the sensitivity measured' was calculated as an index of discriminability on the basis of thesignal detection theory (Macmillan and Creelman, 1991). If hit rates of1 and false alarm rates of zero are observed, it is necessary to correctthe d' value. A Loglinear approachwas used for the correction (Hautus,1995). This approach adds 0.5 to the numbers of both hits and falsealarms, and adds 1 to the numbers of both signal trials and noise trials.Then, the hit rate and false alarm rate, and d' are calculated. Thiscorrection method seems to act better than the other correctiontechnique (Hautus, 1995; Stanislaw and Todorov, 1999). d' wasplotted as a function of parameter difference between target andreference stimuli (Δμ (f)=μt (f)−μ0 (f)) (Fig. 3), and was fitted by theSigmoid function. The fitting with this function converged iterationsin all the subjects. In most cases, the determination coefficientwas larger than 0.9. The maximal d’ value obtained in this experimentwas 4.33, i.e., if the subject performed perfectly the discrimination,the numbers of correct rejections, misses, hits and false alarmswere 32, 0, 32, and 0, respectively, resulting in a d' value of 4.33 byloglinear correction. Low discriminability produces strong featuresynergy whereas high discriminability produces little or no synergy(Meinhardt et al., 2004; Persike and Meinhardt, 2006). To examineEEG modulation when feature synergy is present or not, we selectedd' values of 0.5 and 2.0 for experiments 3 and 4 (Tables 1 and 2),respectively, and extrapolated the corresponding feature parametervalues via the Sigmoid function. We also selected d' values of 0.5, 2.0and 3.5 for experiment 5.

Experiment 3 (EEG experiment at low feature contrast)

This EEG experiment was performed using the GRF stimuli withlow target discriminability to demonstrate psychophysical evidencefor feature synergy and the neural representation simultaneously(Table 1).

Stimulus and taskSpatial frequency and orientation parameters with a d' value of 0.5,

on the basis of the prior psychophysical experiment, were used in this

Fig. 3. The left figure shows results from the psychophysical experiment (exp. 2) in arepresentative subject. The d' value is plotted against a difference in feature parameterbetween the inner and outer regions of the target GRF stimulus. The data are fitted bythe 4-parameter Sigmoid function. The determination coefficients were extremely high(R=0.98 or 0.99). We selected specific d' values for subsequent EEG experiments (e.g.,d'=0.5 for experiment 3) and extrapolated the values to corresponding featureparameter values via the Sigmoid function. Dotted lines show the extrapolation in thecase of d'=0.5. The feature parameter values were used in the subsequent EEGexperiments. μ0 and μt, mean parameters of the Gaussian distribution for samplingfeature parameters of the reference and target GRF stimuli, respectively; Δμ, differencein Gaussian mean parameter between the inner and outer regions of the target GRFstimulus (i.e., feature contrast); φ, orientation; f, spatial frequency; d’, discriminabilitymeasure.

EEG experiment. The same CRT display, presentation system, andstimulus sequence as in the prior psychophysical experiments wereused (Fig. 1B). Reference and target GRF stimuli were presented in arandom order. The subjects were seated in an electrically-shielded,darkened room, and performed a Yes–No discrimination task using abutton-pressing device with two buttons while EEG activity was beingrecorded from their scalp. They were instructed to judge by pressingeither button with the thumb during a blank interval period whetherthe inner region of the GRF stimulus looked different from the outerregion (target) or the whole GRF stimulus contained only onehomogenous region (reference). There were three conditions, wherea feature parameter of the inner region of the target GRF stimulus wasdifferent from the surround in (1) orientation, (2) spatial frequency or(3) both (Fig. 2). The parameters used are listed in Table 1. Theseconditions were presented in a random order. Each conditionconsisted of 128 reference and 128 target GRF stimuli, divided into4 blocks. In this experiment, a “Rest” displaywas also presented for 5 safter the mask stimulus, three times randomly in each block todecrease fatigue. Thus, an experiment lasted for about 1 hour.

EEG recordings and analysisEEG signals were recorded from 60 locations on the scalp (Fig. 4)

using a cap and from the left and right earlobes (Ag/AgCl electrodes).They were digitized at a sampling rate of 1000 Hz and filtered offlinewith a band-pass filter of 0.03–50 Hz. The EEG signal was referencedto averaged potential across all the electrodes, which is perhaps theleast biased of possible references (Dien, 1998) and particularlyappropriate for topographic comparison (Picton et al., 2000). Theanalysis period was from 100 ms before to 500 ms after the onset ofGRF stimuli. EEG data were averaged across trials to calculate theaveraged waveform in individuals but trials with EEG signalsexceeding 80 μV were rejected automatically from the averaging. Acurrent source density (CSD) map was drawn on the scalp usingspherical spline interpolation. This method eliminates the effect of thereference electrode and illustrates local contributions to the surfacemap, providing estimates of approximate locations of intracranialgenerators, without the constraints and prerequisites generallyrequired by the source estimation algorithm.

Mean amplitudes of C1 and N150 responses were measuredbetween 76–100 ms and 121–170 ms respectively at an occipitalelectrode (Oz). Mean amplitudes of P100 were measured between 91

Table 2Across-subject mean (and S.E.) of Gaussian mean parameter values (μ) used inexperiment 4.

Gabor path parameters Spatial frequency Orientation

Gaussian mean parameter μ μ

Inner region of target GRF stimulusSpatial frequency-defined 8.3(0.2) 36Orientation-defined 7 48.5(1.0)Double-feature 8.3(0.2) 48.5(1.0)

Parameters of the reference GRF stimulus and standard deviation parameter (σ) of thetarget GRF were the same as in experiment 3.

Table 3Across-subject mean (and S.E.) of Gaussian mean parameter values (μ) used inexperiment 5.

Gabor path parameters Spatial frequency Orientation

Gaussian mean parameters μ μ

Inner region of target GRFLow discriminability 7.7(0.2) 42.4(0.7)Middle discriminability 8.3(0.2) 48.5(1.0)High discriminability 8.9(0.2) 51.5(0.6)

Parameters of the reference GRF stimulus and standard deviation parameter (σ) of thetarget GRF were the same as in experiments 3 and 4.

673T. Kida et al. / NeuroImage 55 (2011) 669–680

and 100 ms at bilateral occipital electrodes (PO7 and PO8). Theelectrodes which showed the maximal amplitude were selected formeasurements. EEG activity at an inferior temporal electrode wasdivided into 4 temporal clusters (time of interest, from TOI-1 to TOI-4)because there was a long-lasting difference in amplitude starting ataround 130 ms between the double-feature target and referencestimuli. For each of the mean amplitudes, a two-way analysis ofvariance (ANOVA) with repeated measures was performed withfeature (orientation, spatial frequency and both) and stimulus(reference and target) as factors. If the assumption of sphericity wasviolated in Mauchly's sphericity test, the Greenhouse–Geisser (G–G)correction coefficient epsilon was used to correct the degrees offreedom, and then F- and P-values were recalculated. If the G–Gcorrection was applied, the epsilon and corrected results werereported. A two-tailed paired t-test was used for the comparisonbetween two stimuli, and Turkey's multiple comparison method wasused for the comparison among three feature conditions. Statisticalsignificance was set at Pb0.05 in all the statistical analyses.

Analysis of psychophysical dataThe d' in this experiment was calculated as in the prior

psychophysical experiment. If spatial frequency and orientation areprocessed independently of each other, this d' can be expressed interms of the d' of the individual features d'f and d'φ according to

d0⊥ =

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffid0f� �2 + d0φ

� �2r

where the subscript ⊥ denotes orthogonality (independence) of thed'f - and d'φ-components. d'⊥ represents the distance of the centroids ofthe noise and signal plus noise distribution for the case of twoindependent random variables, each representing the degree ofactivation resulting from stimulation with a single feature. That is,this d' value calculated as a scalar product (vector length) from thetwo d' values in orientation-defined and spatial frequency-definedconditions corresponds to the independence of specific modulesunderlying the two features. If the observed discriminability for thedouble-feature GRF stimulus, d’f+φ, is significantly larger than d’ , thenthe processes underlying the two features have an interactive, non-linear synergistic influence on each other. %correct measures werealso calculated as a percentage of the sum of hits and correctsrejection in relation to the number of trials.

Experiment 4 (EEG experiment at high feature contrast)

To examine whether there is feature synergy or not when featurecontrast is high and also whether there is corresponding EEGmodulation or not, the d' of 2 was used to select feature parametersin this EEG experiment. With this level of d', it is expected that therewill be no feature synergy. Therefore, we assumed that there is no EEGmodulation representing feature synergy. The experimental proce-dure, EEG measurements, and analysis were the same as in exper-iment 3, except for a different d' value (Table 2).

Experiment 5 (discriminability and EEG modulation)

As will be described later, we found EEG modulation to beassociated with feature synergy in experiment 3. However, thereremains a possibility that the observedmodulation reflects changes intarget discriminability because feature synergy is evidenced by anincrease of target discriminability. To test this possibility,we examinedEEG modulation when target discriminability varies by manipulatingfeature contrast in individual feature dimensions. Reference andsingle-feature target GRF stimuli were presented in a random orderunder different conditions where d' varied in orientation or spatialfrequency. Double-feature target GRF stimuli were not used. The d'values used were 0.5, 2.0, and 3.5 for each feature. Thus, thisexperiment had a 3-by-2-by-2 factorial design (3 d’ values, 2 features,2 stimuli). The other experimental conditions and EEG measurementsand analyses were the same as in experiments 3 and 4 (Table 3).

Results

Experiments 1 and 2

These two experiments were performed to determine severalparameters of the GRF stimuli to be used in subsequent experimentswhere psychophysical and EEG experiments were combined. The resultsare explained together with a methodological description in theMaterials and methods. The results in experiment 2 are shown in Fig. 3.

Experiment 3 (EEG experiment at low feature contrast)

EEG response to GRF stimulusAt mid-occipital electrodes, GRF stimuli elicited a negative

response at 75–100 ms, the so-called C1 response (Fig. 4). A CSDmap at this latency showed a high current density (sink, in blue) inthe mid-occipital region. At lateral occipital electrodes, GRF stimulielicited a positive response between 90 and 110 ms, P100, which wasfollowed by a negative response peaking at about 150 ms, N150,which covered a wide range of occipital electrodes. P100 was greatestat the bilateral occipital electrodes, and the CSD map at this latencyshowed a high current density (source, in red) at these electrodes.N150 had a positive counterpart, P150, at frontal electrodes. Atinferior temporal electrodes, there was a negative response peaking atabout 135 ms (N130) without preceding deflections. CSDmaps at 135and 150 ms showed a high current density (sink, in blue) in the mid-occipital and inferior temporal regions, respectively, suggesting theinvolvement of different neural sources in the generation of N130 andN150. A similar pattern of EEG responses was observed in thesubsequent two EEG experiments.

Psychophysical dataFig. 5B shows the performance of discrimination. Both d'φ and d'f

showed the same degree of magnitude, about 0.5, in this experiment,which shows that the calibration of discriminability was successful.The d' for the double-feature target GRF stimulus (d'φ+f) wassignificantly increased in comparison with that for the single-featuretarget GRF stimulus (d'φ or d'f). This indicates that the simultaneouspresentation of two different features improves discriminationperformance compared to individual features. More importantly,d'φ+f was increased in comparison with the prediction of independentprocessing of orientation and spatial frequency (d'⊥), representingnon-linear synergistic cooperation between different feature dimen-sions. Corresponding %correct measures was also plotted here.

EEG response modulationFig. 5A displays responses evoked by reference and target GRF

stimuli in each condition. For C1, P100 and N150, there were nosignificant differences in amplitude between target and reference

Fig. 4. Grand-averaged waveforms of the EEG responses evoked by reference GRF stimuli. (A) Top view. (B) Superimposed waveforms from all electrodes. (C) CSD maps at severallatencies. (D) Waveforms at electrodes where C1, P100, N150 and N130 were prominent. CSD, current source density.

674 T. Kida et al. / NeuroImage 55 (2011) 669–680

stimuli in the three conditions, as confirmed by no significant resultsin the 2-way ANOVA. In contrast, there was a long-lasting differencein amplitude at the right inferior occipito-temporal electrodes (e.g.,

TP10) between reference and target GRF stimuli in the double-featurecondition, with amplitude enhanced for target compared withreference GRF stimuli. The enhancement started at around the peak

Fig. 5. Results from experiment 3. (A) Grand-averaged waveforms of the EEG responses to reference and target GRF stimuli in all 3 conditions where the orientation and/or spatialfrequency of the inner region of the target GRF stimuli are different from the surround. In the double-feature condition (φ+ f), target GRF stimuli evoked an enhanced negativitystarting at around 130 ms, compared to reference stimuli. This enhancement lasted up to 500 ms. The period of enhancement was divided into 4 clusters of time of interest (TOI):130–230, 230–330, 330–430, and 430–500 ms. (B) Discriminability measure (d') in all 3 conditions and predicted by the independent processing of orientation and spatial frequency.The double-feature stimulus produced an increased d’ value compared to the single-feature stimulus, indicating that double-feature stimulus enhances target discriminability. Inaddition, the d’ value obtained with the double-feature stimulus was enhanced compared to the prediction of independent processing of orientation and spatial frequency, indicatinga non-linear cooperation of their feature dimensions, feature synergy. Corresponding % correct measures is also displayed here in red. (C) Mean amplitude at an inferior temporalelectrode (TP10) in different TOIs. For all the TOIs, the double-feature target GRF stimulus produced a long-lasting amplitude enhancement in comparison with reference stimuli, butsingle-feature stimuli did not. (D) CSD maps during a long-lasting EEG modulation observed at the inferior temporal electrode. In any condition, the maps showed a high currentdensity of the sink (blue) in the inferior temporal region. (E) CSD maps for double-feature target GRF stimuli at the right hemisphere. Activated region was similar during the long-lasting modulation.

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of N130 and lasted up to 500 ms (Fig. 5A, shaded areas). For theamplitude, there was interaction between stimulus and feature inTOI-1 (F(2,22)=3.47, Pb0.05), TOI-3 (F(2,22)=3.49, Pb0.05), and

TOI-4, F(2,22)=3.60, Pb0.05), such that there was a larger negativedeflection for target GRF stimuli than reference GRF stimuli in thedouble-feature condition, but not in the other two single-feature

676 T. Kida et al. / NeuroImage 55 (2011) 669–680

conditions (Fig. 5A and C). In TOI-2, no significant interaction wasfound but the pattern of amplitude modulation was similar to that forthe other TOIs.

Moreover, two-way ANOVAs were performed on the data in thedouble-feature condition with electrode (TP9 and TP10) and stimulus(target and reference) as factors, to test the laterality of the long-lasting negative deflection elicited by double-feature target GRFstimuli. The laterality (i.e., interaction between the two factors) wasobserved only for TOI-1 (F(1,11)=17.75, Pb0.005), with right-hemisphere dominance.

Comparison of CSD mapsTo examine the source underlying the observed response

modulation, scalp CSD maps were compared between target andreference GRF stimuli (Fig. 5D and E). For all stimuli in all conditions,CSD maps indicated a similar distribution, with a strong sink (in blue)in the inferior temporal region. It is therefore assumed that the EEGresponse at the inferior temporal electrode was mainly generated inthe visual ventral pathway. The CSD maps for double-feature targetGRF stimuli showed long-lasting activation in the right inferiortemporal region as shown in Fig. 5E. The effect of laterality on the rightand left inferior temporal regions was significant as indicated by theANOVA of the amplitude.

Fig. 6. Results from experiment 4. (A) Grand-averaged waveforms of the EEG responses to rfrequency of the inner region of the target GRF stimuli are different from the surround. (B) Dof orientation and spatial frequency. Corresponding % correct measures is also displayed. Tfeature stimuli, but it was not significant. Unlike in experiment 3 (with low feature contrasdecreased compared to independent processing of orientation and spatial frequency. Thisdimensions is high (C) Mean amplitude at occipital and inferior temporal electrodes (Oz andtarget compared to reference GRF stimulus in the TOI-2 and 3. The enhancement observecontrast to the occipital electrode, there was no significant modulation at the inferior temp

Experiment 4 (EEG experiment at high feature contrast)

Psychophysical dataThe d' values were about 2 in all 3 conditions, which were clearly

higher than when feature synergy was present in experiment 3. Thediscriminability for the double-feature target GRF stimulus (d'φ+f)was slightly increased compared to the single-feature stimuli (d'φ ord'f), but not significantly (Fig. 6B). In addition, d'φ+f was not increasedbut rather lower than the prediction of independent processing oforientation and spatial frequency (d'⊥). This result shows no featuresynergy when target discriminability in individual feature dimensionsis high. In contrast, experiment 3 indicates that feature synergy ispresent when the discriminability is low.

EEG response modulationWe found a significant difference in amplitude between reference

and target GRF stimuli in all three conditions at the mid-occipitalelectrode but only in TOI-2 (Figs. 6A and C), with amplitude enhancedfor target compared to reference stimuli. Considering that there is nodifference in amplitude between reference and single-feature targetstimuli in experiment 3 using low discriminability, the enhancementobserved here might be associated with an increase of targetdiscriminability (this was tested more directly in experiment 5).

eference and target GRF stimuli in all 3 conditions where the orientation and/or spatialiscriminability measure (d') in all 3 conditions and predicted by independent processinghere was a slight increase in d' with the double-feature stimulus compared to single-t), the d' value obtained with the double-feature stimulus was not increased but ratherindicates that there is no feature synergy when feature contrast in individual featureTP10) in different TOIs. The amplitude at the occipital electrode was enhanced for the

d around the peak of N150 was specific to the orientation-defined target stimulus. Inoral electrode (TP10).

677T. Kida et al. / NeuroImage 55 (2011) 669–680

There was no interaction regarding the modulation, representing nosynergistic effect between different feature dimensions indexed bythe electrophysiological measure.

Experiment 5 (effects of discriminability on EEG modulation)

Psychophysical dataThe d' value was increased from low discriminability to high for

each feature dimension (Fig. 7B). A two-way ANOVA showed maineffects of discriminability and no interaction, with increased d' fromlow to high discriminability independently of feature dimension.

EEG response modulationFor the spatial frequency-defined target condition, the amplitude

of the EEG response at the occipital electrode (Oz) was significantlyenhanced for target compared to reference GRF stimuli in high andmiddle discriminability conditions in the TOI covering N150, but notin the low condition (Fig. 7A and C). In contrast, for the orientation-defined target condition, the amplitude of the occipital activity wasnot significantly different between target and reference stimuli in anycondition. This pattern of occipital modulation was evidenced bya three-way interaction among feature, discriminability and stimulus(F(2, 18)=3.9, Pb0.05). In TOI-2, the amplitude of occipital activitywas

Fig. 7. Results from experiment 5. (A) Grand-averaged waveforms of the EEG responses toorientation or spatial frequency at 3 levels of discriminability. (B) Discriminability measure (feature contrast, independent of feature dimension. (C) Mean amplitude at an occipital electthe orientation-defined target compared to reference stimulus in high and middle discriminnot show the same enhancement of amplitude at around this latency. In TOI-2, the amdiscriminability conditions in both orientation and spatial frequency, but not in the low oelectrode (TP10).

significantly enhanced for target GRF stimuli compared to referenceGRF stimuli in high and middle discriminability conditions for bothorientation- and spatial frequency-defined targets, but not in the lowcondition. This was evidenced by a two-way interaction betweendiscriminability and stimulus (F(2, 18)=4.5, Pb0.05). In contrast toexperiment 3, the amplitude at the inferior temporal electrode wasnot significantly different between reference and target GRF stimuli atany TOI in any discriminability condition. For the amplitudes of C1 andP100, there were no significant differences. Thus, the EEG modulationcaused by increasing discriminability in individual feature dimensionsshoweddifferent spatio-temporal dynamics from those in experiment 3where feature synergy was observed.

Discussion

Feature synergy

Psychophysical data in the EEG experiment provided evidence foran interactive non-linear cooperation (feature synergy) betweendifferent feature dimensions, orientation and spatial frequency. Thisnon-linear cooperation was evidenced by an increase in the d' valuewith double-feature GRF stimuli compared to that with the predictionof independence of individual single-feature stimuli. The results of

reference and target GRF stimuli in all 6 conditions where GRF stimuli were defined byd’) and %correct measures in all 6 conditions. The d' value was increased with increasingrode (Oz) in different TOIs. The amplitude at around the peak of N150 was enhanced forability conditions but not in the low one. Spatial frequency-defined target stimulus didplitude was enhanced for target compared to reference stimuli in high and middlene. There was no significant modulation regarding amplitude at an inferior temporal

678 T. Kida et al. / NeuroImage 55 (2011) 669–680

previous psychophysical studies on feature synergy seem to havebeen controversial until recently. Some studies reported performanceimprovements with multiple features (Caelli and Moraglia, 1985;Callaghan, 1984, 1989; Callaghan et al., 1986; Nothdurft, 2000, 1993;Rivest and Cavanagh, 1996), but others did not (Gray and Regan,1997; Pashler, 1988; Phillips and Craven, 2000). Recent studies haverevealed that feature contrast (or target discriminability) in individualdimensions between figure and background is crucial to featuresynergy (Meinhardt and Persike, 2003; Meinhardt et al., 2004; Persikeand Meinhardt, 2006). Taking these findings into consideration, weemployed the SDT to calibrate discriminability in the prior psycho-physical experiment. As a result, we successfully found clear featuresynergy between orientation and spatial frequency only when featurecontrast was low. In contrast, there was no evidence for featuresynergy when feature contrast was high. This is consistent withprevious psychophysical studies (Meinhardt et al., 2004; Persike andMeinhardt, 2006). These results provide a possibility that there issome neural process representing this interactive non-linear cooper-ation between orientation and spatial frequency.

Neurophysiological correlate of feature synergy

To seek the neural representation of feature synergy, wemeasuredEEG responses to reference and target GRF stimuli in single-featureand double-feature conditions in experiments 3 and 4. In experiment3 where feature synergy was present, we found no significantdifference in amplitude between responses to reference and single-feature target GRF stimuli in either case of orientation and spatialfrequency. In contrast, there was a long-lasting enhancement of theEEG activity at an inferior temporal electrode, staring at around130 ms after double-feature target GRF stimuli, compared to referencestimuli. This enhancement lasted for several milliseconds, which wasevidenced by a significant continuous enhancement of amplitudefrom TOI-1 to TOI-4 at this recording site. The CSD analysis showedthat the source was located in the ventral visual stream that is crucialfor object recognition (Baylis and Driver, 2001; Fujita et al., 1992;Logothetis et al., 1995; Nielsen et al., 2006; Tanaka, 1996). Neurons inthe inferior temporal region of the monkey best respond to complex,colorful stimuli, and respond selectively to some shapes over others(Desimone et al., 1984; Gross et al., 1972; Tanaka et al., 1991). fMRIstudies have reported involvement of the lateral occipital cortex(LOC) in object recognition (Grill-Spector et al., 1998). The shapeinvariance despite changes in retinal position and size suggests theseregions to be responsible for object and shape processing, thoughdifferent kinds of invariance were cautiously reviewed recently(Tompa and Sary, 2010). The long-lasting enhancement in the inferiortemporal region in association with feature synergy is consistent withthese possible functions that have been suggested in monkeys andfMRI. In contrast to activity in the inferior temporal region, the otherresponses, C1, P100 and N150, which reflect neural activities in striateand extrastriate cortices, were not significantly modulated regardingfeature synergy. Thus, feature synergy is represented by the long-lasting response enhancement starting at around 130 ms in the visualventral stream. This contention was strengthened by the absence ofcorresponding EEG modulation in the inferior temporal region whenfeature synergy was not present (experiment 4).

In addition, experiment 5 showed that response enhancement inthe inferior temporal region does not reflect simply the increase ofdiscriminability inherent to feature synergy. Response enhancementwas distributed widely over the occipital region for single-featuretarget GRF stimuli compared to reference GRF stimuli when featurecontrast was high and middle (i.e., d' was high and middle) in bothcases of orientation and spatial frequency, whereas there was nomodulation in the inferior temporal region. The CSD analysis indicatedthe main source of the occipital enhancement to be in and around thestriate cortex. These results demonstrate that the EEG modulation in

the inferior temporal region is not directly related to the alteration ofdiscriminability but the occipital enhancement is. There were nosignificant differences in the inferior temporal activity between targetand reference GRF stimuli even at the d' of 2, though it was higher thanthe d' value (about 1) produced by feature synergy. Thus, the resultsprovide the possibility that the EEG modulation in the inferiortemporal region observed in experiment 3 is not due to changes indiscriminability inherent to feature synergy. However, in experiment5, we did not test EEGmodulation at the level of target discriminability(i.e., d'=1) that induced feature synergy and long-lasting negativedeflection in experiment 3. Therefore, we cannot completely excludethe possibility that target discriminability contribute to the generationof long-lasting negative deflection associated with feature synergy.

Target GRF stimuli with a certain degree of discriminabilityproduce frequently and clearly the figure-ground segmentation(e.g., all the conditions in experiment 4 [d' was about 2] or middleand high discriminability conditions in experiment 5 [d' was about 2or 3]). We here found an enhancement of the EEG activity around theoccipital region for target compared to reference GRF stimuli. Anumber of studies using EEG, MEG and fMRI have demonstratedneural correlates of figure-ground segmentation (Appelbaum et al.,2006; Caputo and Casco, 1999; Casco et al., 2005; Doniger et al., 2000;Grill-Spector et al., 1998; Halgren et al., 2003; Kastner et al., 2000;Murray et al., 2004, 2002; Schira et al., 2004; Schubo et al., 2001;Sehatpour et al., 2006), as well as single-neuron recordings in animals(Lamme, 1995; Polat et al., 1998; Polat and Sagi, 1993, 1994; Zhou etal., 2000; Zipser et al., 1996). These studies have suggested theinvolvement of V1, V2, the lateral occipital cortex (LOC) and V4,supporting the present findings. Despite these extensive studies offigure-ground segmentation, there is no evidence for neural correlatesof feature synergy so far. Only one study has investigated an EEGresponse evoked by double-feature stimuli (Bach et al., 2000). Thisprevious study recorded EEG signals from just a mid-occipitalelectrode and did not consider the non-linearity of feature cooper-ation. In previous studies of single-neuron recordingsmost relevant tothe feature synergy phenomenon, there was no further enhancementof the firing rate of V1 (Kastner et al., 1999; Zipser et al., 1996) and V2neurons (Kastner et al., 1999) when texture figures are defined byadditional features which the neurons were responsive for in single-feature patterns. These single-neuron studies also did not consider thenon-linearity of feature cooperation either. In the present study, weperformed an SDT-based calibration of discriminability prior to thesimultaneous evaluation of EEG and SDTmeasures to demonstrate thenon-linearity of cooperation between different feature dimensions.Then, our approach of combining SDT and EEG measures successfullydemonstrated that feature synergy of orientation and spatialfrequency is represented by a sustained modulation of electrophys-iological activity starting at around 130 ms post-stimulus in theventral visual stream. The SDT-based approach employed here couldalso be helpful for understanding the non-linear synergistic phenom-ena between different systems in the brain.

Two single-neuron studies seemingly contradict with the presenthuman study. An early study demonstrated that cooling of MT inmonkey reduces figure-ground segmentation (Hupe et al., 1998).Another study also reported that the removal of dorsal extra-striateareas of the monkey visual cortex reduces figure-ground capability(Super and Lamme, 2007). These two studies have suggested theimportance of the dorsal pathway and the feedback pathway to lower-order visual cortices in figure-ground segregation. In the presentstudy, so-called figure-ground segmentation produced the modula-tion of the occipital component including activities in the striate andextra-striate cortices, which does not contradict the two studiesmentioned above. In contrast, feature synergy was observed concom-itantlywith neuralmodulation in the inferior temporal region. The twosingle-neuron studies examined figure-ground segmentation, but didnot test feature synergy (non-linear cooperation).

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In very recent studies, Straube and Fahle reported no evidence fora special marker of feature synergy (Straube and Fahle, 2010; Straubeet al., 2010). They found a diminished posterior P2 in association withtexture segregation and this effect was modulated by saliency. Anegative enhancement when it encompasses the P2 time windowcould also be described as a diminished P2. However, they observedthe diminished P2 maximally at the occipital electrodes, while wefound the long-lasting negative deflection in the inferior temporalregion. Rather, the diminished P2 by Straube and Fahle might beassociated with the occipital negative deflection induced by increas-ing target discriminability. Another possibility for the discrepancymay be the difference in the recording montage. We used an averagedpotential across more than 60 recording sites as a reference, becausethis is perhaps the least biased of possible references. Straube andFahle analyzed EEG activity at 25 sites referenced to linked earlobes.The linked-earlobe reference can diminish virtually the activitygenerated around the temporal region, which may explain why theyfound no negative enhancement in the inferior temporal region.Furthermore, figures segregated and subject's tasks performed weredifferent between the present and previous studies, which mightcontribute to the discrepancy.

Comparison with similar ERP components

A contour defined by aligned luminance or color elements in asurround of randomly oriented elements produces a negativedeflection starting at 220 ms across occipital electrodes (Mathes andFahle, 2007; Mathes et al., 2006). This contour-specific negativedeflection resembles a negative shift observed at occipital electrodesfor both single- and double-feature target GRF stimuli in experiments2 and 3 of the present study, regarding latency, spatial distribution,and experimental conditions where these were elicited. The contour-specific negative deflection also resembles the texture segregationvisual-evoked potential (tsVEP), which has been observed at occipitalelectrodes (Bach and Meigen, 1997; Bach et al., 2000; Casco et al.,2005; Fahle et al., 2003; Romani et al., 2003). In contrast, the long-lasting negative deflection we observed was found locally at aninferior temporal electrodewhen synergywas observed by presentingtwo features simultaneously. These findings segregate the synergisticeffect from contour integration and texture segregation.

N2pc is a negative ERP deflection at a latency of 170–300 mselicited by an attended target stimulus presented among distractors invisual search tasks (Eimer, 1994; Luck and Hillyard, 1990, 1994a,b).N2pc showed the greatest amplitude at parieto-occipital electrodes(PO7/8) in the hemisphere contralateral to the attended target (Eimeret al., 2010; Kuo et al., 2009; Mazza et al., 2009, 2007). In contrast, thelong-lasting negative deflectionwe observed showed amore localizedpotential distribution at an inferior temporal site rather than parieto-occipital site. Accordingly, these findings could reflect the activation ofneuronal populations in different regions. In addition, in the presentstudy, a contour defined by the orientation and/or spatial frequency ofgabor patches was presented across different visual hemifields. If thesubjects attended to both hemifields and the double-feature conditionin the low feature contrast experiment (exp 3) neededmore attentionto integrate different features into a contour, then the majority ofN2pc might be obscured by the generation of N2pc in bothhemispheres. Nevertheless, the local presence of a long-lastingnegative deflection would reflect the activation of neuronal popula-tions in regions separate from those involved in the generation ofN2pc. In sum, the long-lasting negative deflection observed in theinferior temporal region in association with feature synergy mightbe caused by separate neuronal activations from ERP componentsrelated to target selection, texture segregation and contour integra-tion, whereas the occipital negative deflection resembles thesecomponents.

Role of attention

The contribution of attention to the long-lasting negativedeflection associated with feature synergy is possible, because theobservers attended to the display in all experimental conditions.Many theories actually postulate that feature integration in a serialsearch requires attention (Treisman and Gelade, 1980), but otherssuggest binding or grouping without focused attention (Gray, 1999;Kubovy et al., 1999). ERP studies have reported some componentsrelated to attention; e.g., Nd, N2pc and P3b. However, the long-lastingnegative deflection was observed locally in the inferior temporalregion in the present study, which was different in spatial distributionfrom those attention-related ERP components. Therefore, it isspeculated that the long-lasting negative deflection was elicited in adifferent context from these attentional modulations. It might bedifficult to believe that the role of attention in producing featuresynergy is the same as that of the attention-related ERP components.

Acknowledgments

This study was supported by a Grant-in-Aid for Young Scientists (B)fromtheMinistry of Education, Culture, Sports, Science andTechnologyofJapan (18700327) and by a Grant-in-Aid for JSPS fellows (19349) to T.K.andby "Developmentof biomarker candidates for social behavior" carriedout under Strategic Research Program for Brain Sciences (SRPBS), by theMinistry of Education, Culture, Sports, Science and Technology of Japan.

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