Early involvement of the temporal area in attentional selection of grating orientation: an ERP study

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1 Cognitive Brain Research 13 (2002) locate/ bres Research report Early involvement of the temporal area in attentional selection of grating orientation: an ERP study Alice Mado Proverbio *, Paola Esposito, Alberto Zani a,b,c, c b a Department of Psychology, University of Milano-Bicocca, Piazza dell Ateneo Nuovo, 1, Milan, Italy b Institute of Bioimaging and Molecular Physiology in Humans, Consiglio Nazionale delle Ricerche, Via Fratelli Cervi 93, Segrate, Milan, Italy c Laboratory of Cognitive Electrophysiology, Department of Psychology, University of Trieste, Trieste, Italy Accepted 6 September 2001 Abstract The aim of the present study was to investigate the neural mechanisms of stimulus orientation selection in humans by recording event-related potentials (ERPs) of the brain with a 32-channel montage. Stimuli were isoluminant black-and-white gratings (3 cpd) having an orientation of 508, 708, 908, 1108 and 1308, randomly presented in the foveal portion (28 of visual angle) of the central visual field. The task consisted in selectively attending and responding to one of the five grating orientations, while ignoring the others. ERP results showed that orientation selection affected neural processing starting already at an early post-stimulus latency. The P1 component ( ms) measured at temporal area, which might well be reflecting the activity of the ventral stream (i.e. WHAT system) of the visual pathways, showed an enhanced amplitude for target orientations. These effects increased with progressive neural processing over time as reflected by selection negativity (SN) and P300 components. In addition, both reaction times (RTs) and ERPs showed a strong oblique effect, very probably reflecting the perceptual predominance of orthogonal versus oblique stimulus orientation in the human visual system: RTs were much faster, and SN and P300 components much larger, to gratings presented vertically than in other orientations Elsevier Science B.V. All rights reserved. Theme: Neural basis of behavior Topic: Cognition Keywords: Attention; Electrophysiology; Sensory gating; Vision; VEP; Ventral stream; P1 component 1. Introduction investigate the neurofunctional bases of feature selection, and to determine the stage at which top-down processes Several functional neuroimaging studies have shown such as attention can affect sensory processing. The effect that visual attention selection modulates activity of the of selective attention to spatial frequency and orientation dorsal and ventral streams of the visual system [4,14,35]. on ERPs in humans was first measured in the pioneering This modulation has been also observed by measuring studies of Harter and co-workers [11,12,26]. They found changes in amplitude, latency and scalp topography of that attention enhanced N1 and N2 components of ERPs, event-related potentials (ERPs) to visual stimuli as a giving rise to a broad negative response called selection function of task relevance and attention condition (e.g. negativity which peaked at about 250 ms post-stimulus. Refs. [1,22,38]). Later electrophysiological studies described modulation A large number of ERP studies have attempted to of ERP responses earlier than selection negativity in attention tasks in which targets were alphanumeric stimuli [32], grating spatial frequency or orientation [18,27,38,39] *Corresponding author. Department of Psychology, University of and color [2]. However, relatively few studies provided Milano-Bicocca, Piazza dell Ateneo Nuovo, 1, Milano, Italy. Tel.: evidence of an early modulation of surface sensory evoked addresses: mado.proverbi@unimib.it or zani@inb.mi.cnr.it activity recorded at visual areas during selective attention (A.M. Proverbio). to non-spatial features (e.g. Refs. [8,17,30]). These differ / 02/ $ see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S (01)

2 140 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) ences across findings reported in the electrophysiological sensory gating. This might have slowed down the latency literature might be due to a series of methodological of the earliest sign of attentional modulation for stimulus factors, including differences in stimulus presentation rate: orientation. Having found evidence of early attentional a fast presentation rate along with a very short presentation modulation for spatial frequency [38,39], which is produration is associated with small early effects (see for cessed by visual neurons selectively tuned to both spatial example the study by Annlo-Vento and Hillyard [1] frequency and orientation, we sought to further investigate adopting a SOA of only 150 ms, and a presentation orientation selection mechanisms by adopting a task duration of only 32 ms). Again, differences in ERP requiring difficult levels of orientation discrimination quantification methods may be responsible for different compared to previous ERP studies dealing with this experimental results. For example, measuring at fixed stimulus feature. We therefore endeavoured to improve as latency intervals (as in Ref. [26]) may not be the best way far as possible the quality of the ERP waveforms recorded to detect early amplitude modulations of responses to (especially the earliest VEP responses). gratings of different spatial frequencies, since VEP mor- Briefly, the goal of the present study was to shed some phology is strongly affected by the latter. In addition, it light on the mechanisms subserving attentional selection of should be borne in mind that V1-related activity is much orientation by adopting task conditions aimed at producing smaller than that due to the activity of other associative ERP waveforms (and especially early responses) with as visual areas (i.e. V2, V4, etc.), as shown by neuro- good a signal-to-noise ratio as possible. In this study, we physiological literature [23]. This implies that, in order to adopted large gratings, foveally presented for 80 ms with a appreciate any attention modulation effect at sensory contrast of 60%. To guarantee a good signal-to-noise ratio component level, it is crucial for ERP waveforms to have a each of five differently oriented gratings were presented good signal-to-noise ratio. To this end, it is necessary to 600 times. The inter-stimulus interval was relatively long provide good sensory stimulation (in terms of luminance, ( ms), and instructions were given at the begincontrast and presentation duration of stimuli) in order to ning of each block of trials in a sustained attention obtain sensory-evoked responses of appreciable amplitude. condition. Overall, the investigation was aimed at de- An example of this effect may be appreciated by compar- termining the timing of attentional selection for a noning the amplitude of evoked responses to spatial frequency spatial feature, which is well known to engage mainly the gratings presented for 10 ms at 5% contrast (as in Ref. ventral visual pathway. [16]) with those presented for 100 ms at 50% contrast (as To make orientation discrimination challenging enough in Ref. [38]). It is obvious that an increase of 10% in the for visual selection mechanisms, so as to make the highest amplitude of the evoked response (as for the attentional demands on attentional resources, five gratings differing modulation of the N115 reported in Ref. [38]) would be only by 208 in orientation were adopted as stimuli in the more consistent if the recorded response was sufficiently present study. Four of them were oblique with respect to large (e.g. several microvolts instead of 1 mv). the vertical meridian. The use of oblique vs. orthogonal Another effect which might contribute to reducing the gratings produced a difference in perceptual difficulty of presence of attention effects on early sensory responses is discrimination that is strongly reflected in ERP and the combined use of symbolic cues (alphanumeric charac- behavioral measures, and is described in the literature as ters) with other, selected, non-spatial features. Several the oblique effect [3,5,9,13,28]. studies have combined selective attention to color or size with the search for a given letter, and these complex selection mechanisms involving processing of symbolic 2. Materials and methods material failed to produce any attention effect earlier than 150 ms [15,36,37] Participants As far as the attentional selection of stimulus orientation in particular is concerned, in classical literature this non- Ten young persons (five males and five females; mean spatial feature has been described as one of the latest age, 23 years) participated in this experiment as volunteers. physical features (in terms of ERP latency) to be attention- All were right handed and had a normal or corrected-toally selected by human observers, following location, color normal vision. Two of them were rejected for excessive and spatial frequency. However, in all previous studies, muscular and/ or ocular artifacts before ERP averaging. with the exception of O Donnel et al. [25], who adopted gratings of 458 and 908, only vertical and horizontal 2.2. Stimuli and procedure orientations, which are of course easily distinguishable from each other, were used as stimuli [11,18,20,21,26,29]. Participants were seated in a dimly lit, acoustically and We believe that the use of stimuli so macroscopically electrically shielded cubicle situated 114 cm from a TV different in terms of luminance distribution and local screen. They were instructed to fixate a cross at the center spatial frequency spectrum, compared to stimuli differing of the screen and avoid any kind of eye or body moveonly slightly in spatial frequency, size or shape, might ment. Stimuli were equiprobable, isoluminant black-andhave contributed to reducing the need for an accurate white square-wave gratings (3 cpd of spatial frequency)

3 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) having 508, 708, 908 (vertical), 1108 and 1308 orientation convention and quantified by measuring peak latency and with respect to the horizontal meridian. The gratings baseline-to-peak amplitude values within a specific latency 2 average luminance was about 33 cd/m, and their stimulus range centered approximately on the peak latency of the contrast was 60%. Stimuli were randomly presented for 80 deflection observed in the grand average waveforms. At ms in the foveal portion (28 of visual angle) of the central posterior sites (O1, O2, OL, OR, T5, T6) P1 positive visual field. The interstimulus interval (ISI) was varied deflection was identified in the time window between 90 randomly between 850 and 1000 ms. Each grating was and 140 ms. Additionally, an early P1 positivity was presented 600 times for a total number of 3000 gratings measured at the temporal area at T3 and T4 electrode sites, presented to each of the 10 subjects. For each of the five and quantified by means of mean area computing between attention conditions and five stimulus orientations the ERP 80 and 140 ms of post-stimulus latency. N1 and N2 were averaged across about 120 trial repetitions. negative deflections were identified in the time windows The task consisted in selectively attending and respond- between 100 and 200 ms, and 200 and 300 ms, respectiveing to a given orientation by pressing a button as accu- ly. An anterior positivity was identified in the time window rately and fast as possible with the index finger while between 270 and 430 ms at temporal (T3, T4), central (C3, ignoring the other stimuli. C4), frontal (F3, F4), centro-parietal (CP1, CP2), centro- The two hands were used alternatively during the temporal parietal (TCP1, TCP2) electrode sites. In the recording session, and the hand order was counterbalanced same time window P300 was measured at midline sites Cz, across subjects. Fz, Pz, Oz. A posterior positivity was recorded and measured at O1, O2, OL, OR, T5, T6 occipito-temporal 2.3. Electrophysiological recording sites. In the same time window a frontal positivity was measured at F3, F4, F7, F8, FTC1, FTC2 electrode sites. The electroencephalogram (EEG) was continuously ERP amplitude and latency measures were analyzed recorded from 28 scalp sites using tiny Ag/AgCl elec- using repeated-measure analyses of variance (ANOVAs), trodes mounted on an elastic cap (Electro-cap, Inc.). The separately for each ERP component. ERPs to oblique and electrodes were located at frontal (Fp1, Fp2, FZ, F3, F4, vertical gratings were analyzed separately. For oblique F7, F8), central (CZ, C3, C4), temporal (T3, T4), poste- gratings, factors were orientation (508, 708, 908, 1108 and rior-temporal (T5, T6), parietal (PZ, P3, P4), and occipital 1308), attention (target and non-target), electrode site scalp sites (OZ, O1, O2) of the International (depending on the ERP component of interest) and cere- System. Additional electrodes were placed half way be- bral hemisphere (left and right). For vertical gratings the tween the anterior-temporal and central sites (FTC1, orientation factor was omitted (see Electrophysiological FTC2), the central and parietal sites (CP1, CP2), the data for an explanation of these separate analyses). Greenanterior-temporal and parietal sites (TCP1, TCP2), and the house Geisser corrections were employed to reduce the posterior-temporal and occipital sites (OL, OR). Blinks and positive bias resulting from repeated factors with more vertical eye movements (i.e. EOG) were monitored by than two levels. Post-hoc Tukey testing was carried out for means of two electrodes placed below and above the right multiple mean comparisons. Topographical voltage maps eye, while horizontal movements were recorded by elec- of ERP components were obtained by plotting color-coded trodes placed at the outer canthi of the eyes. Linked ears iso-potential contour lines obtained by interpolation of served as reference lead. The EEG and the EOG were voltage values between scalp electrodes at specific latenamplified with a half-amplitude band pass of Hz cies. and Hz, respectively. Electrode impedance was For each subject, hit and false alarm (FAs) percentages kept below 5 kv. Continuous EEG and EOG were were converted to arcsine values and subjected to a twodigitized at a rate of 512 samples per second. way repeated-measures ANOVA. Reaction times not faster Computerized artifact rejection was performed before than 140 ms, and not exceeding the mean value 62 averaging to discard epochs in which eye movements, standard deviations were subjected to a three-way reblinks, excessive muscle potentials or amplifier blocking peated-measures ANOVA. Factors were orientation (508, occurred. The artifact rejection criterion was: peak to peak 708, 908, 1108 and 1308), attention (target and nonamplitude exceeding 650 mv. The artifact rejection rate target), and response hand (left and right). was about 5%. ERPs were averaged offline from 100 ms before to 1000 ms after stimulus presentation. ERP trials associated with an incorrect behavioral response were 3. Results excluded from further analysis. For each subject, distinct ERP averages were obtained as a function of grating 3.1. Behavioral data orientation and attention condition. The major ERP components were identified and measured automatically by a The mean percentage of correct responses (independent computer program with reference to the baseline voltage of stimulus orientation) was 93%, whereas the mean averages over the interval from 2100 to 0 ms. ERP percentage of false alarms (FAs) was 3.23%. Fig. 1a and b components were labeled according to a polarity-latency show hit and FA percentages as a function of stimulus

4 142 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Fig. 1. (a) Mean percentage of correct responses (hits) emitted by observers as a function of stimulus orientation. (b) Mean percentage of false alarms (FAs) emitted by observers as a function of stimulus orientation. (c) Mean RTs to gratings as a function of their orientation. difference in response time to vertical than oblique orientation (P,0.01), with a strong bias towards the former Electrophysiological data Fig. 2 shows the grand average ERPs obtained at occipital sites in response to vertical gratings independent of task relevance. At these sites spatial frequency gratings produced a series of early positive and negative deflections which varied in morphology as a function of electrode site, and, along with later ERP components, were strongly affected by stimulus orientation per se. Interestingly, the negativity of N115 and N1 components gradually increased as orientation varied from 508 to 1308, whereas P1 positivity progressively increased as stimulus orientation varied from 1308 to 508. Furthermore, the so-called oblique effect (the bias of orthogonal vs. oblique orientations, e.g. Ref. [5]) occurred as evoked responses of much greater amplitude to vertical than to oblique gratings, independent of attention, especially for P1 and P300 deflections (see Fig. 3). The effects of selective attention on ERP components varied considerably as a function of stimulus orientation. In particular, no consistent attention modulation was evident for oblique gratings in the N1 N2 latency range. In more detail, no selection negativity to target was observable when attention was paid to oblique orientations, whereas reduced P1 and P300 attention effects were still observable. These effects were probably due to the fact that orientations adopted in this study were not sufficiently different from each other to produce large attention effects. It is a known fact that visual neurons respond to oriented gratings within a certain sensitivity bandwidth (the channel size is known to be about 208), but, probably, all oblique gratings fell (to a greater or lesser extent) either within or too close to the same bandwidth, as well as sharing the same spatial frequency with the target. The special status of vertical gratings compared to other orientations caused a different results pattern as regards both the morphology of visual evoked potentials and attention effects. Overall, the data reflected a greater sensitivity of the visual system to the orthogonal orientation, along with a finer attention selectivity when the vertical orientation was to be selected. Because of these widely varying differences in ERP morphology and attention effects for vertical and oblique gratings, separate ANOVAs were performed for ERP components recorded for vertical and oblique gratings, respectively. orientation, indicating a strong advantage for vertically oriented gratings. Repeated measure ANOVAs confirmed the significant effect of orientation both on hit and FA percentages (F4,10; P,0.0000), and post-hoc tests among means proved that hit percentages were much lower to oblique than to vertical gratings (P,0.01), while FA percentages were significantly higher to the former than to the latter (P,0.01). Interestingly, hit percentages were significantly higher (P,0.05), and FA percentages lower 3.3. Vertical gratings (P,0.05) for oblique stimuli of 1308 orientation than for 1108 orientation P1 deflection Mean reaction time (RT) to gratings was about 460 ms Table 1 reports all significant factors found in the (see Fig. 1c). The ANOVA performed on RT data showed various ANOVAs performed in the present study on ERP a significant effect of stimulus orientation (F4, ; values recorded for vertical target and non-target gratings. P,0.0000). Post-hoc comparisons indicated a significant ANOVA performed on P1 mean amplitude values

5 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Fig. 2. Grand average (N58) ERP waveforms recorded at midline (Oz), and left and right mesial (O1, O2) and lateral (OL and OR) occipital sites in response to vertical gratings of 3 cpd independent of task relevance. hemisphere. While P1 was larger at posterior occipital sites, the effect of attention, as revealed by the difference- wave obtained by subtracting ERP to non-targets from ERP to targets, was larger at temporal sites in the time window between 80 and 140 ms. This effect was followed showed a significant electrode and hemisphere effect. This early positive response was larger at lateral occipital and posterior temporal areas, and displayed its maximum amplitude at right hemispheric sites (see Fig. 4), as confirmed by the significant interaction of electrode3 Fig. 3. Grand average (N58) ERP waveforms recorded at right lateral occipital sites in response to stimuli of different orientations independent of task relevance.

6 144 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Table 1 Statistical significances of ANOVAs performed on ERPs to vertical gratings with attention condition, electrode site and hemisphere as factors ERP deflection Factors df F P value Occipital P1 Electrode 2,14 5.6,0.02 Hemisphere 1,7 5.26,0.05 Electrode3hemisphere 2,14 6.8,0.01 Temporal P1 Attention 4,28 3.3,0.025 Hemisphere 1, ,0.01 Occipital N1 Hemisphere 1,7 5.69,0.05 Attention 4,28 2.7,0.05 Occipital N2 Hemisphere 4, , Attention3hemisphere 4, , Attention3elec.3hem. 8, ,0.007 Occipital N2 latency Attention 4,28 2.9,0.05 Anterior P300 Electrode 5, , Electrode3hemisphere 5, ,0.02 Attention 4, , Attention3hemisphere 4,28 2.8,0.05 Midline P300 Electrode , Attention 4, , Attention3electrode ,0.03 Posterior P300 Electrode 2,14 7.5,0.007 Attention 4, ,0.001 Attention3hemisphere 4, ,0.02 Temporal P300 Attention 4, , Electrode 2, , Attention3electrode 8, ,0.007 Attention3hemisphere 8, ,0.004 Electrode3hemisphere 2, ,0.01 by an early frontal positivity, which is an attention effect often found in ERP selective attention studies (see difference maps in Fig. 5). ANOVA performed on mean area amplitude recorded at temporal area in the ms latency range showed a significant attention effect. The early temporal P1 response to targets (20.1 mv) was Fig. 4. Vertical gratings. Grand average (N58) ERP waveforms recorded at posterior sites to vertical gratings as a function of stimulus relevance.

7 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Fig. 5. Top, spatio-temporal maps of attention effect in the P1 latency range obtained by plotting the values of the difference wave (target2non-target) computed by subtracting the grand-average waveform for the irrelevant condition (i.e. ERP to vertical gratings while oblique orientations were attended) from the ERP to vertical targets. A centro-temporal generator is visible, having a certain asymmetry toward the left hemisphere. Bottom, spatio-temporal maps of attention effect for oblique gratings showing a significant but smaller effect and a slightly different scalp distribution. significantly larger than when these same stimuli were unattended because other orientations were attended (20.7 mv), as shown by post-hoc comparisons among means (P,0.01). While the temporal positive response was much larger over the right (0.03 mv) than left (21.25 mv) hemisphere, the attention effect tended to be larger at the left site as shown by mean values reported in Table 2. However the interaction of factors attention3hemisphere did not reach statistical significance N1 deflection The large negative deflection measured between 100 and 200 ms was larger at left posterior sites (see Fig. 4), as shown by the factor hemisphere. The ANOVA also yielded a significant attention effect: selectively paying attention to vertical targets produced larger N1 responses (P,0.05) compared to when the same stimuli were unattended. Although no significant interaction with attention arose from statistical comparisons, the isocontour voltage map of attention effects in the N1 latency range showed a tendency for the selective attention effect to be more prominent at left hemispheric sites, as for the temporal P1 (see maps of Fig. 6) N2 deflection The negative deflection measured between 200 and 300 ms was larger at right posterior sites (factor hemisphere) and very sensitive to attention. ANOVA yielded the significant interaction of attention3hemisphere, showing a greater negativity to attended than unattended gratings at Table 2 P1 mean values (N58) to vertical gratings (908) recorded in the time window between 80 and 140 ms post-stimulus at left and right temporal sites Attention to: 908 target Electrode Mean area S.D. T non-target T T non-target T T non-target T T non-target T T T

8 146 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Fig. 6. Spatio-temporal difference maps of attention effect in the N1, N2 and P3 latency ranges for vertical and oblique gratings. right hemispheric sites (P,0.05), and a triple interaction produced a much larger P300 response compared to when of attention3electrode3hemisphere. Post-hoc comparisons the same stimuli were unattended (P,0.01). This anterior indicated that N2 was larger to attended than to unattended P300 was asymmetrically distributed as indicated by the gratings at mesial occipital and lateral occipital sites. At significant interaction of electrode3hemisphere. Post-hoc the latter sites the attention effect was larger on the right tests proved that anterior P300 was larger at left than right hemisphere (P,0.05). This hemispheric asymmetry for the parietal sites (P,0.01). A further interaction of attention3 attention effect is visible in waveforms in Fig. 4 and the hemisphere showed that P300 to targets was of greater maps in Fig. 6. The ANOVA performed on mean latency amplitude over the left than the right hemisphere (P, values of N2 component yielded the significant effect of 0.01), whereas no hemispheric asymmetry was present for attention, indicating faster latencies for N2 to attended P300 to unattended gratings. (241 ms) than to unattended (252 ms) gratings. P300 recorded at midline sites was also subjected to an ANOVA. Consistent with previous analyses, the electrode P300 deflection effect reflected larger P300 at central sites, while the An anterior late positive response, larger at centro- attention effect reflected larger responses to attended than parietal and central sites, was measured in the time interval to unattended gratings. The significant interaction of between 270 and 430 ms. Attention had a very significant attention3electrode showed that attention significantly effect in this latency range. Post-hoc comparisons showed affected P300 responses at more anterior (Fz and Cz) than that selectively paying attention to the vertical gratings posterior (Pz and Oz) sites (P,0.01).

9 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) ERP components recorded to oblique gratings in the different attention conditions are reported in Table 3. Fig. 7. Mean P3 amplitude values recorded for vertical gratings at posterior sites as a function of attention condition and cerebral hemi- sphere P1 deflection The ANOVA performed on mean area recorded at temporal areas in the ms range showed the significant effect of hemisphere indicating larger positivity at right sites (see Fig. 8). Furthermore, early temporal responses were significantly larger to targets than nontargets as shown by the significant attention effect. Maps of difference waves, obtained by subtracting ERPs to unattended from ERPs to attended orientations, show the scalp topography of this early attention modulation (see Fig. 6). An impression of left hemispheric asymmetry for the temporal activation drawn by these maps turned out to be statistically non-significant, probably because of the inter-individual variability across subjects. P300 recorded at posterior sites in the same time N1 and N2 deflections window was maximally distributed at lateral occipital and The ANOVAs performed on later negative peaks (N1 posterior temporal sites (P,0.01). The effect of attention and N2) failed to show any effect of attention on these reflected larger P300 responses to target than non-target components: no selection negativity was observed for stimuli, while the significant interaction of attention3 oblique gratings, which probably activated partially overhemisphere reflected a hemispheric asymmetry in the lapping neural channels tuned to similar orientations and attention effect. Post-hoc comparisons indicated larger the same spatial frequency of targets (see Fig. 8). attention effects and P300 to targets at left than right hemispheric sites (P,0.01), as is shown in Fig P300 deflection P300 measured at anterior sites was larger at centroparietal and central sites (P,0.01). The effect of attention 3.4. Oblique gratings was also significant, although it was smaller than observed in the attend-vertical condition. In fact, post-hoc com- The significant results of the separate ANOVAs carried parisons among means showed greater P300s to target than out on mean area amplitude, peak amplitude and latency of non-target oblique gratings (P,0.05), but the opposite Table 3 Statistical significances of ANOVAs performed on ERPs to oblique gratings with stimulus orientation, attention condition, electrode site and cerebral hemisphere as factors ERP deflection Factors df F P value Temporal P1 Attention 1, ,0.01 Hemisphere 1, ,0.01 Anterior P300 Electrode 1,7 16, Hemisphere3electrode 5, ,0.006 Attention 2, ,0.05 Attention3electrode 10, , Orientation3attent.3elec. 10,70 1.7,0.01 Anterior P300 latency Attention 2,14 3.8, Electrode 5,35 4.8,0.002 Midline P300 Electrode 3, , Attention 2,14 3.8,0.05 Attention3electrode 6, , Attention3orientation 6,42 3.8,0.05 Midline P300 latency Attention 2, , Posterior P300 Electrode 2, ,0.02 Attention 2,14 7.6,0.002 Attention3hemisphere 2,14 4.7,0.03 Attention3orientation 6, ,0.002 Posterior P300 latency Electrode 2, ,0.003 Attention 2, ,0.006

10 148 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Fig. 8. Oblique gratings. Grand average (N58) ERP waveforms recorded at posterior sites for oblique gratings as a function of stimulus relevance. effect when vertical gratings were attended. Very interest- indicating greater attention effects for oblique gratings at ingly, P300s to target oblique gratings were smaller than frontal (P,0.01) but not centroparietal sites (as in the case that elicited by the same stimuli when non-targets because of vertical gratings), as shown in the maps in Fig. 7. The vertical gratings were attended (P,0.05). Moreover, the interaction of attention3orientation indicated greater P300 significant interaction of attention3electrode showed amplitudes to target stimuli having extreme orientations, greater attention effects at centro-parietal and frontal (P, i.e. 508 (P,0.05) and especially 1308 (P,0.01). At 0.01) than other electrode sites. Again, the ANOVA midline sites P300 latency was also affected by attention displayed a significant hemisphere3electrode interaction, being earlier to target than to non-target stimuli (P,0.01). reflecting a hemispheric asymmetry in P300 distribution The posterior P300 was larger at lateral occipital and that was larger at left sites over the parietal area (P,0.01). posterior temporal sites. Again, it was larger to targets than Very interestingly, the ANOVA also yielded the signifi- non-targets, except for the case in which vertical gratings cant effect of orientation3attention3electrode. Post-hoc were attended. Also significant was the interaction of comparisons indicated larger P300s to target than non- orientation3attention, which showed larger attention eftarget stimuli, especially at centroparietal sites, and greater fects (P,0.01) for extreme orientations of 508 and attention effects (larger differences between P300 to target Consistent with data obtained for vertical gratings, P300 than non-target orientations) to stimuli oriented to 508 amplitude was significantly affected by attention in inter- (P,0.05) or 1308 (P,0.01) rather than to 708 or action with the factor hemisphere. Indeed, attention effects This piece of data might reflect a slight advantage in were larger at left recording sites (P,0.05). The analyses discriminating these extreme orientations consistent of latency showed earlier P300 responses to targets than to with behavioral data (namely hit and FA rates) which non-targets and earlier P300 at lateral occipital (than more were less confused with similar orientations than 708 or temporal) sites stimuli. As for P300 latency, it was earlier at anterior than 3.5. Oblique vs. vertical gratings posterior sites, and to target than non-target stimuli. A separate ANOVA was performed on P300 values Notwithstanding the macroscopic differences in VEPs as recorded at midline sites in the same temporal interval. a function of stimulus orientation (especially at P300 level, Consistent with previous data, the P300 was larger at as visible from waveforms of Fig. 3), a separate repeatedcentral electrode sites, and to oblique targets than oblique measures four-way ANOVA was performed on P300 non-targets. Again, post-hoc comparisons proved that P300 values recorded at frontal and centro-temporal sites (F3, to oblique targets was actually smaller than to the same F4, F7, F8, FTC1, FTC2) to vertical and oblique gratings, stimuli when a vertical grating was attended (P,0.05). in order directly to compare the brain processing of these The interaction of attention3electrode was also significant, two kinds of stimuli, which are very different in terms of

11 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) Table 4 reported shorter VEP latencies for horizontal and vertical Statistical significances of ANOVAs performed on P300 mean amplitudes than for oblique gratings (308 and 608 in the former study, recorded to oblique and vertical gratings at anterior sites in the P300 latency range as a function of attention condition, electrode site and 458 and 1358 in the latter study). The fmri study by hemisphere Furmanski and Egel [9] revealed the probable neurofunc- ERP deflection Factors df F P value tional basis of this effect in humans, demonstrating that the activation of neurons in V1 is greater to horizontal and Frontal P300 Attention 1,7 46, vertical than to oblique orientations (458 or 1358). Electrode 1,7 18,0.005 Hemisphere 1,7 9.2,0.02 In our study, P1 and P300 components were larger to Attention3hem.3orient. 1,7 5.2,0.05 vertical than oblique gratings independent of the attention condition. Behavioral data were consistent with electrophysiological data, showing faster RTs and a better perceptual saliency. Table 4 reports all the statistical discrimination to vertical than oblique stimuli. We also significances obtained in this ANOVA. found an interesting correlation between behavioral (hits Overall, the ANOVA revealed a significant electrode and FAs) and electrophysiological data, as indexed by effect, with P300 being larger at frontal sites. Again, P300 amplitude. In more detail, the performance was better attention significantly affected P300 independent of for stimuli having the extreme oblique orientation (i.e. 508 stimulus orientation, as reflected by larger responses to and 1308) compared to other oblique stimuli, and this targets than non-targets (P,0.01). Very interestingly, while effect was related to the arising of larger P300s to these P300 was larger at right frontal sites, as indicated by the than other targets with intermediate oblique orientations significant main factor hemisphere, the attention effect (i.e. 708 and 1108). In our view, this effect was probably tended to be larger at left sites, as shown by the interaction related to the subject s certainty in discriminating target of attention3hemisphere. More importantly, the ANOVA from non-target patterns: the greater the certainty, the showed an effect of orientation in interaction with attention larger and earlier the P3 and relative attention effects. This and hemisphere. Post-hoc comparisons showed larger finding is very similar to other findings reported in the P300s to vertical than oblique orientations (see Fig. 7), and ERP literature. For example, Zani and Proverbio [38] in a greater attention effects at left frontal sites for both types study adopting an attention to check-size paradigm found of stimuli, this asymmetry being larger for vertical (P, higher hit rates, faster RTs and larger P3 responses to the 0.01) than for oblique (P,0.05) stimuli. largest and the smallest relevant check sizes than to the intermediate sizes in the range of check sizes used, notwithstanding that these stimuli were even closer in 4. Discussion spatial frequency than the intermediate ones. This was probably due to the fact that the extreme check sizes were In this experiment macroscopic differences in the mor- easier to recognize at sensory/ perceptual level as they phology of visual evoked potentials and magnitude of were not accompanied by confusing non-target distractors attention effects were found between vertical and oblique at the lower and higher size scale. Interestingly, as in the gratings. Very interestingly, a posterior selection negativity study cited, in our investigation P300 differences in to attended gratings was absent in response to oblique amplitude and topography affected the prefrontal area (see orientations, and attention effects were smaller in the maps of Fig. 6), which is related somehow or other to attend-oblique than attend-vertical condition. Surprisingly, cingulate activity and task difficulty factors. the anterior P300 was even larger to vertical non-target To our knowledge, the present ERP study is the only than oblique target gratings. In other words, the perceptual one in the literature which has adopted spatial frequency oblique effect (i.e. the advantage of orthogonal vs. oblique gratings so close in orientation (208 difference between gratings) was more powerful than top-down attentional one and the next) in a selective discrimination task. processes in determining an enhanced neural processing. Several previous studies adopted only vertical and horizon- Overall, our findings indicate the crucial role of physical tal orientations [11,18,20,21,26,29], which of course are features, such as stimulus orientation, in affecting the readily distinguishable from each other, whereas O Donnel activity of attention selection mechanisms. Indeed, the and co-workers [25] adopted 458 and 908 gratings. With the amplitude modulation of ERP components depended exception of Karayanidis and Michie [18], who found an strongly on stimulus orientation in relation to the oblique attention modulation of a posterior P125 component, all effect. This effect is well known in psychophysical and the other studies reported attention effects indexed by a neurophysiological literature [5,13,24], which extensively posterior selection negativity not earlier than 150 ms. reports a better visual acuity and performance in discrimi- The main findings of the present experiment concern the nation tasks with orthogonal than oblique gratings. This timing of attentional selection and the scalp distribution of effect has also been investigated by means of electro- attention-related ERP activity. All in all, our data showed physiological recordings. For example, the visual evoked an early attention modulation of P1 response at temporal potential (VEP) studies by Rabin [28] and Arawaka [3] area ( ms) for both vertical and oblique gratings.

12 150 A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) The timing of this early attention effect is pretty much in A further bold hypothesis is that the hemispheric line with Karayanidis and Michie s [18] findings. asymmetry found in both performance and amplitude As for the scalp topography of this early attention effect, measures of ERP components for oblique gratings of 508 the present results indicate an activation of temporal areas ( pointing to the left) with respect to those of 1308 during orientation selection. Although ERPs do not pro- ( pointing to the right) is related to the fact that the latter vide a direct knowledge of the intracerebral sources of the were actually preferred by the left hemisphere. For the various foci of activation recorded at scalp surface, these time being, however, this hypothesis is still pure speculafindings are substantially consistent with recent neuro- tion. physiological and neuroimaging findings in the literature indicating that, as part of the ventral stream, the temporal cortex would play a crucial role in object discrimination, as 5. Summary it too is specifically involved in orientation processing. This, in our view, lends support to the robustness of our In conclusion, the present data do not support the view results notwithstanding the ERP limitations in neural that the first effect of attention to non-spatial features (such source localization. For example, Vogels and Orban [34] as grating orientation) is represented by the occipital and Tanaka [33] found that cells of the inferior temporal selection negativity (SN), as reported for example by cortex in monkey were strongly activated during orienta- Hillyard [17] or Schroeder et al. [30]. Instead, they indicate tion discrimination and object discrimination, respectively, an early increase in positivity to target stimuli (both whereas Kawashima [19], when measuring regional cere- verticals an oblique) in the P1 latency range ( ms). bral blood flow with PET, found a specific activation of the Topographic mapping of our ERP data indicates that this left inferior temporal cortex during object discrimination in early attentional increase in positivity is focused at tempohumans. Our ERP findings indicate that temporal area ral scalp sites. Last but not least, our data also show the activity may be modulated by visual attention processes at strong interdependence between stimulus physical features a very early stage of processing. In this regard, Schroeder and attentional processes, which result in a very different et al. [31] described an early modulatory effect in V4 and pattern of results as a function of stimulus orientation in the inferior temporal regions of monkeys (IT), which (both in terms of visual event-related potentials and their bypassed V1 and preceded the excitatory feedforward attentional modulation). signal. The result of the present ERP investigation in humans possibly suggests the hypothesis that these initial visual inputs in V4 and IT (higher order cortical visual Acknowledgements areas) may be modulated by top-down attentional processes. Certainly, further investigations are needed before This work was supported by a 40% MURST grant to any definitive conclusion can be reached, especially as far Alice Mado Proverbio. We are grateful to Ian McGilvray as electrophysiological studies on humans are concerned. for revising the manuscript, and to two anonymous ref- The present ERP findings also support the hypothesis of erees for their comments on and criticism of a previous a special involvement of the left hemisphere in object version of this paper. discrimination, as suggested also by a very recent neuroimaging study [10], as well as some ERP attention studies [7,38]. References For example, Dupont et al. [6] used PET during tasks involving simultaneous orientation discrimination, identifi- [1] L. Anllo-Vento, S.A. Hillyard, Selective attention to the color and cation and detection tasks in humans, with all tasks using direction of moving stimuli: electrophysiological correlates of the same pair of vertical and oblique gratings. The hierarchical feature selection, Percept. Psychophys. 58 (2) (1996) subtraction of detection from simultaneous discrimination [2] L. Anllo-Vento, S.J. Luck, S.A. 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