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Early involvement of the temporal area in attentional selection of grating orientation: an ERP study
Cognitive Brain Research 13 (2002) 139–151 www.elsevier.com / locate / bres
Research report
Early involvement of the temporal area in attentional selection of grating orientation: an ERP study Alice Mado Proverbio b
a,b,c ,
*, Paola Esposito c , Alberto Zani b
a Department of Psychology, University of Milano-Bicocca, Piazza dell’ Ateneo Nuovo, 1, 20126 Milan, Italy Institute of Bioimaging and Molecular Physiology in Humans, Consiglio Nazionale delle Ricerche, Via Fratelli Cervi 93, 20090 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 (80–140 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. 2002 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 Several functional neuroimaging studies have shown that visual attention selection modulates activity of the dorsal and ventral streams of the visual system [4,14,35]. This modulation has been also observed by measuring changes in amplitude, latency and scalp topography of event-related potentials (ERPs) to visual stimuli as a function of task relevance and attention condition (e.g. Refs. [1,22,38]). A large number of ERP studies have attempted to *Corresponding author. Department of Psychology, University of Milano-Bicocca, Piazza dell’Ateneo Nuovo, 1, 20126 Milano, Italy. Tel.: 139-02-2171-7511. E-mail addresses: [email protected] or [email protected] (A.M. Proverbio).
investigate the neurofunctional bases of feature selection, and to determine the stage at which top-down processes such as attention can affect sensory processing. The effect of selective attention to spatial frequency and orientation on ERPs in humans was first measured in the pioneering studies of Harter and co-workers [11,12,26]. They found that attention enhanced N1 and N2 components of ERPs, giving rise to a broad negative response called selection negativity which peaked at about 250 ms post-stimulus. Later electrophysiological studies described modulation 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] and color [2]. However, relatively few studies provided evidence of an early modulation of surface sensory evoked activity recorded at visual areas during selective attention to non-spatial features (e.g. Refs. [8,17,30]). These differ-
0926-6410 / 02 / $ – see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S0926-6410( 01 )00103-3
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ences across findings reported in the electrophysiological literature might be due to a series of methodological factors, including differences in stimulus presentation rate: a fast presentation rate along with a very short presentation duration is associated with small early effects (see for example the study by Annlo-Vento and Hillyard [1] adopting a SOA of only 150 ms, and a presentation duration of only 32 ms). Again, differences in ERP quantification methods may be responsible for different experimental results. For example, measuring at fixed latency intervals (as in Ref. [26]) may not be the best way to detect early amplitude modulations of responses to gratings of different spatial frequencies, since VEP morphology is strongly affected by the latter. In addition, it should be borne in mind that V1-related activity is much smaller than that due to the activity of other associative visual areas (i.e. V2, V4, etc.), as shown by neurophysiological literature [23]. This implies that, in order to appreciate any attention modulation effect at sensory component level, it is crucial for ERP waveforms to have a good signal-to-noise ratio. To this end, it is necessary to provide good sensory stimulation (in terms of luminance, contrast and presentation duration of stimuli) in order to obtain sensory-evoked responses of appreciable amplitude. An example of this effect may be appreciated by comparing the amplitude of evoked responses to spatial frequency gratings presented for 10 ms at 5% contrast (as in Ref. [16]) with those presented for 100 ms at 50% contrast (as in Ref. [38]). It is obvious that an increase of 10% in the amplitude of the evoked response (as for the attentional modulation of the N115 reported in Ref. [38]) would be more consistent if the recorded response was sufficiently large (e.g. several microvolts instead of 1 mV). Another effect which might contribute to reducing the presence of attention effects on early sensory responses is the combined use of symbolic cues (alphanumeric characters) with other, selected, non-spatial features. Several 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 material failed to produce any attention effect earlier than 150 ms [15,36,37]. As far as the attentional selection of stimulus orientation in particular is concerned, in classical literature this nonspatial feature has been described as one of the latest physical features (in terms of ERP latency) to be attentionally selected by human observers, following location, color and spatial frequency. However, in all previous studies, with the exception of O’Donnel et al. [25], who adopted gratings of 458 and 908, only vertical and horizontal orientations, which are of course easily distinguishable from each other, were used as stimuli [11,18,20,21,26,29]. We believe that the use of stimuli so macroscopically different in terms of luminance distribution and local spatial frequency spectrum, compared to stimuli differing only slightly in spatial frequency, size or shape, might have contributed to reducing the need for an accurate
sensory gating. This might have slowed down the latency of the earliest sign of attentional modulation for stimulus orientation. Having found evidence of early attentional modulation for spatial frequency [38,39], which is processed by visual neurons selectively tuned to both spatial frequency and orientation, we sought to further investigate orientation selection mechanisms by adopting a task requiring difficult levels of orientation discrimination compared to previous ERP studies dealing with this stimulus feature. We therefore endeavoured to improve as far as possible the quality of the ERP waveforms recorded (especially the earliest VEP responses). Briefly, the goal of the present study was to shed some light on the mechanisms subserving attentional selection of orientation by adopting task conditions aimed at producing ERP waveforms (and especially early responses) with as good a signal-to-noise ratio as possible. In this study, we adopted large gratings, foveally presented for 80 ms with a contrast of 60%. To guarantee a good signal-to-noise ratio each of five differently oriented gratings were presented 600 times. The inter-stimulus interval was relatively long (850–1000 ms), and instructions were given at the beginning of each block of trials in a sustained attention condition. Overall, the investigation was aimed at determining the timing of attentional selection for a nonspatial feature, which is well known to engage mainly the ventral visual pathway. To make orientation discrimination challenging enough for visual selection mechanisms, so as to make the highest demands on attentional resources, five gratings differing only by 208 in orientation were adopted as stimuli in the present study. Four of them were oblique with respect to the vertical meridian. The use of oblique vs. orthogonal gratings produced a difference in perceptual difficulty of discrimination that is strongly reflected in ERP and behavioral measures, and is described in the literature as the ‘oblique effect’ [3,5,9,13,28].
2. Materials and methods
2.1. Participants Ten young persons (five males and five females; mean age, 23 years) participated in this experiment as volunteers. All were right handed and had a normal or corrected-tonormal vision. Two of them were rejected for excessive muscular and / or ocular artifacts before ERP averaging.
2.2. Stimuli and procedure Participants were seated in a dimly lit, acoustically and electrically shielded cubicle situated 114 cm from a TV screen. They were instructed to fixate a cross at the center of the screen and avoid any kind of eye or body movement. Stimuli were equiprobable, isoluminant black-andwhite square-wave gratings (3 cpd of spatial frequency)
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having 508, 708, 908 (vertical), 1108 and 1308 orientation with respect to the horizontal meridian. The gratings’ average luminance was about 33 cd / m 2 , and their stimulus contrast was 60%. Stimuli were randomly presented for 80 ms in the foveal portion (28 of visual angle) of the central visual field. The interstimulus interval (ISI) was varied randomly between 850 and 1000 ms. Each grating was presented 600 times for a total number of 3000 gratings presented to each of the 10 subjects. For each of the five attention conditions and five stimulus orientations the ERP were averaged across about 120 trial repetitions. The task consisted in selectively attending and responding to a given orientation by pressing a button as accurately and fast as possible with the index finger while ignoring the other stimuli. The two hands were used alternatively during the recording session, and the hand order was counterbalanced across subjects.
2.3. Electrophysiological recording The electroencephalogram (EEG) was continuously recorded from 28 scalp sites using tiny Ag /AgCl electrodes mounted on an elastic cap (Electro-cap, Inc.). The electrodes were located at frontal (Fp1, Fp2, FZ, F3, F4, F7, F8), central (CZ, C3, C4), temporal (T3, T4), posterior-temporal (T5, T6), parietal (PZ, P3, P4), and occipital scalp sites (OZ, O1, O2) of the International 10-20 System. Additional electrodes were placed half way between the anterior-temporal and central sites (FTC1, FTC2), the central and parietal sites (CP1, CP2), the anterior-temporal and parietal sites (TCP1, TCP2), and the posterior-temporal and occipital sites (OL, OR). Blinks and vertical eye movements (i.e. EOG) were monitored by means of two electrodes placed below and above the right eye, while horizontal movements were recorded by electrodes placed at the outer canthi of the eyes. Linked ears served as reference lead. The EEG and the EOG were amplified with a half-amplitude band pass of 0.01–70 Hz and 0.1–70 Hz, respectively. Electrode impedance was kept below 5 kV. Continuous EEG and EOG were digitized at a rate of 512 samples per second. Computerized artifact rejection was performed before averaging to discard epochs in which eye movements, blinks, excessive muscle potentials or amplifier blocking occurred. The artifact rejection criterion was: peak to peak amplitude exceeding 650 mV. The artifact rejection rate 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 excluded from further analysis. For each subject, distinct ERP averages were obtained as a function of grating orientation and attention condition. The major ERP components were identified and measured automatically by a computer program with reference to the baseline voltage averages over the interval from 2100 to 0 ms. ERP components were labeled according to a polarity-latency
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convention and quantified by measuring peak latency and baseline-to-peak amplitude values within a specific latency range centered approximately on the peak latency of the deflection observed in the grand average waveforms. At posterior sites (O1, O2, OL, OR, T5, T6) P1 positive deflection was identified in the time window between 90 and 140 ms. Additionally, an early P1 positivity was measured at the temporal area at T3 and T4 electrode sites, and quantified by means of mean area computing between 80 and 140 ms of post-stimulus latency. N1 and N2 negative deflections were identified in the time windows between 100 and 200 ms, and 200 and 300 ms, respectively. An anterior positivity was identified in the time window between 270 and 430 ms at temporal (T3, T4), central (C3, C4), frontal (F3, F4), centro-parietal (CP1, CP2), centrotemporal parietal (TCP1, TCP2) electrode sites. In the same time window P300 was measured at midline sites Cz, Fz, Pz, Oz. A posterior positivity was recorded and measured at O1, O2, OL, OR, T5, T6 occipito-temporal sites. In the same time window a frontal positivity was measured at F3, F4, F7, F8, FTC1, FTC2 electrode sites. ERP amplitude and latency measures were analyzed using repeated-measure analyses of variance (ANOVAs), separately for each ERP component. ERPs to oblique and vertical gratings were analyzed separately. For oblique gratings, factors were ‘orientation’ (508, 708, 908, 1108 and 1308), ‘attention’ (target and non-target), ‘electrode site’ (depending on the ERP component of interest) and ‘cerebral hemisphere’ (left and right). For vertical gratings the orientation factor was omitted (see Electrophysiological data for an explanation of these separate analyses). Greenhouse–Geisser corrections were employed to reduce the positive bias resulting from repeated factors with more than two levels. Post-hoc Tukey testing was carried out for multiple mean comparisons. Topographical voltage maps of ERP components were obtained by plotting color-coded iso-potential contour lines obtained by interpolation of voltage values between scalp electrodes at specific latencies. For each subject, hit and false alarm (FAs) percentages were converted to arcsine values and subjected to a twoway repeated-measures ANOVA. Reaction times not faster than 140 ms, and not exceeding the mean value 62 standard deviations were subjected to a three-way repeated-measures ANOVA. Factors were ‘orientation’ (508, 708, 908, 1108 and 1308), ‘attention’ (target and nontarget), and ‘response hand’ (left and right).
3. Results
3.1. Behavioral data The mean percentage of correct responses (independent of stimulus orientation) was 93%, whereas the mean percentage of false alarms (FAs) was 3.23%. Fig. 1a and b show hit and FA percentages as a function of stimulus
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difference in response time to vertical than oblique orientation (P,0.01), with a strong bias towards the former.
3.2. Electrophysiological data
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.
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 (P,0.05) for oblique stimuli of 1308 orientation than for 1108 orientation. Mean reaction time (RT) to gratings was about 460 ms (see Fig. 1c). The ANOVA performed on RT data showed a significant effect of stimulus orientation (F4,10549.5; P,0.0000). Post-hoc comparisons indicated a significant
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.
3.3. Vertical gratings 3.3.1. P1 deflection Table 1 reports all significant factors found in the various ANOVAs performed in the present study on ERP values recorded for vertical target and non-target gratings. ANOVA performed on P1 mean amplitude values
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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.
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
hemisphere. While P1 was larger at posterior occipital sites, the effect of attention, as revealed by the differencewave 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
Fig. 3. Grand average (N58) ERP waveforms recorded at right lateral occipital sites in response to stimuli of different orientations independent of task relevance.
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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 Hemisphere Electrode3hemisphere Attention Hemisphere Hemisphere Attention Hemisphere Attention3hemisphere Attention3elec.3hem. Attention Electrode Electrode3hemisphere Attention Attention3hemisphere Electrode Attention Attention3electrode Electrode Attention Attention3hemisphere Attention Electrode Attention3electrode Attention3hemisphere Electrode3hemisphere
2,14 1,7 2,14 4,28 1,13 1,7 4,28 4,28 4,28 8,56 4,28 5,35 5,35 4,28 4,28 3.21 4,28 12.84 2,14 4,28 4,28 4,28 2,14 8,56 8,56 2,14
5.6 5.26 6.8 3.3 12.2 5.69 2.7 8.23 8.23 4.05 2.9 6.67 3.12 12.23 2.8 13.28 9.65 2 7.5 6.36 5.46 9.64 21.51 2.98 2.98 7.02
,0.02 ,0.05 ,0.01 ,0.025 ,0.01 ,0.05 ,0.05 ,0.0002 ,0.0002 ,0.007 ,0.05 ,0.0002 ,0.02 ,0.0000 ,0.05 ,0.0000 ,0.0000 ,0.03 ,0.007 ,0.001 ,0.02 ,0.0000 ,0.0001 ,0.007 ,0.004 ,0.01
Temporal P1 Occipital N1 Occipital N2
Occipital N2 latency Anterior P300
Midline P300
Posterior P300
Temporal P300
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 80–140 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.
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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.
3.3.2. 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).
3.3.3. 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.
T3 20.728 1
508 non-target T4 0.45 1.1
T3 21.402 0.9
708 non-target T4 0.197 1
T3 21.509 0.5
1108 non-target T4 20.303 1.2
T3 21.165 0.9
1308 non-target T4 0.185 1
T3 21.369 0.9
T4 20.368 0.7
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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 of attention3electrode3hemisphere. Post-hoc comparisons indicated that N2 was larger to attended than to unattended gratings at mesial occipital and lateral occipital sites. At the latter sites the attention effect was larger on the right hemisphere (P,0.05). This hemispheric asymmetry for the attention effect is visible in waveforms in Fig. 4 and the maps in Fig. 6. The ANOVA performed on mean latency values of N2 component yielded the significant effect of attention, indicating faster latencies for N2 to attended (241 ms) than to unattended (252 ms) gratings.
3.3.4. P300 deflection An anterior late positive response, larger at centroparietal and central sites, was measured in the time interval between 270 and 430 ms. Attention had a very significant effect in this latency range. Post-hoc comparisons showed that selectively paying attention to the vertical gratings
produced a much larger P300 response compared to when the same stimuli were unattended (P,0.01). This anterior P300 was asymmetrically distributed as indicated by the significant interaction of electrode3hemisphere. Post-hoc tests proved that anterior P300 was larger at left than right parietal sites (P,0.01). A further interaction of attention3 hemisphere showed that P300 to targets was of greater amplitude over the left than the right hemisphere (P, 0.01), whereas no hemispheric asymmetry was present for P300 to unattended gratings. P300 recorded at midline sites was also subjected to an ANOVA. Consistent with previous analyses, the electrode effect reflected larger P300 at central sites, while the attention effect reflected larger responses to attended than to unattended gratings. The significant interaction of attention3electrode showed that attention significantly affected P300 responses at more anterior (Fz and Cz) than posterior (Pz and Oz) sites (P,0.01).
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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 hemisphere.
P300 recorded at posterior sites in the same time window was maximally distributed at lateral occipital and posterior temporal sites (P,0.01). The effect of attention reflected larger P300 responses to target than non-target stimuli, while the significant interaction of attention3 hemisphere reflected a hemispheric asymmetry in the attention effect. Post-hoc comparisons indicated larger attention effects and P300 to targets at left than right hemispheric sites (P,0.01), as is shown in Fig. 7.
3.4. Oblique gratings The significant results of the separate ANOVAs carried out on mean area amplitude, peak amplitude and latency of
3.4.1. P1 deflection The ANOVA performed on mean area recorded at temporal areas in the 80–140 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. 3.4.2. N1 and N2 deflections The ANOVAs performed on later negative peaks (N1 and N2) failed to show any effect of attention on these components: no selection negativity was observed for oblique gratings, which probably activated partially overlapping neural channels tuned to similar orientations and the same spatial frequency of targets (see Fig. 8). 3.4.3. P300 deflection P300 measured at anterior sites was larger at centroparietal and central sites (P,0.01). The effect of attention was also significant, although it was smaller than observed in the attend-vertical condition. In fact, post-hoc comparisons among means showed greater P300s to target than 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 Hemisphere Electrode Hemisphere3electrode Attention Attention3electrode Orientation3attent.3elec. Attention Electrode Electrode Attention Attention3electrode Attention3orientation Attention Electrode Attention Attention3hemisphere Attention3orientation Electrode Attention
1,7 1,7 1,7 5,35 2,14 10,70 10,70 2,14 5,35 3,21 2,14 6,42 6,42 2,14 2,14 2,14 2,14 6,42 2,14 2,14
12.21 15.98 16 3.97 3.63 5.42 1.7 3.8 4.8 13.48 3.8 4.87 3.8 18.14 5.82 7.6 4.7 4.31 9.18 7.66
,0.01 ,0.01 ,0.0001 ,0.006 ,0.05 ,0.0000 ,0.01 ,0.0002 ,0.002 ,0.0000 ,0.05 ,0.0001 ,0.05 ,0.0001 ,0.02 ,0.002 ,0.03 ,0.002 ,0.003 ,0.006
Anterior P300
Anterior P300 latency Midline P300
Midline P300 latency Posterior P300
Posterior P300 latency
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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 interestingly, P300s to target oblique gratings were smaller than that elicited by the same stimuli when non-targets because vertical gratings were attended (P,0.05). Moreover, the significant interaction of attention3electrode showed greater attention effects at centro-parietal and frontal (P, 0.01) than other electrode sites. Again, the ANOVA displayed a significant hemisphere3electrode interaction, reflecting a hemispheric asymmetry in P300 distribution that was larger at left sites over the parietal area (P,0.01). Very interestingly, the ANOVA also yielded the significant effect of orientation3attention3electrode. Post-hoc comparisons indicated larger P300s to target than nontarget stimuli, especially at centroparietal sites, and greater attention effects (larger differences between P300 to target than non-target orientations) to stimuli oriented to 508 (P,0.05) or 1308 (P,0.01) rather than to 708 or 1108. This piece of data might reflect a slight advantage in discriminating these extreme orientations — consistent with behavioral data (namely hit and FA rates) — which were less confused with similar orientations than 708 or 1108 stimuli. As for P300 latency, it was earlier at anterior than posterior sites, and to target than non-target stimuli. A separate ANOVA was performed on P300 values recorded at midline sites in the same temporal interval. Consistent with previous data, the P300 was larger at central electrode sites, and to oblique targets than oblique non-targets. Again, post-hoc comparisons proved that P300 to oblique targets was actually smaller than to the same stimuli when a vertical grating was attended (P,0.05). The interaction of attention3electrode was also significant,
indicating greater attention effects for oblique gratings at frontal (P,0.01) but not centroparietal sites (as in the case of vertical gratings), as shown in the maps in Fig. 7. The interaction of attention3orientation indicated greater P300 amplitudes to target stimuli having extreme orientations, i.e. 508 (P,0.05) and especially 1308 (P,0.01). At midline sites P300 latency was also affected by attention being earlier to target than to non-target stimuli (P,0.01). The posterior P300 was larger at lateral occipital and posterior temporal sites. Again, it was larger to targets than non-targets, except for the case in which vertical gratings were attended. Also significant was the interaction of orientation3attention, which showed larger attention effects (P,0.01) for extreme orientations of 508 and 1308. Consistent with data obtained for vertical gratings, P300 amplitude was significantly affected by attention in interaction with the factor hemisphere. Indeed, attention effects were larger at left recording sites (P,0.05). The analyses of latency showed earlier P300 responses to targets than to non-targets and earlier P300 at lateral occipital (than more temporal) sites.
3.5. Oblique vs. vertical gratings Notwithstanding the macroscopic differences in VEPs as a function of stimulus orientation (especially at P300 level, as visible from waveforms of Fig. 3), a separate repeatedmeasures four-way ANOVA was performed on P300 values recorded at frontal and centro-temporal sites (F3, F4, F7, F8, FTC1, FTC2) to vertical and oblique gratings, in order directly to compare the brain processing of these two kinds of stimuli, which are very different in terms of
A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) 139 – 151 Table 4 Statistical significances of ANOVAs performed on P300 mean amplitudes recorded to oblique and vertical gratings at anterior sites in the P300 latency range as a function of attention condition, electrode site and hemisphere ERP deflection
Factors
df
F
P value
Frontal P300
Attention Electrode Hemisphere Attention3hem.3orient.
1,7 1,7 1,7 1,7
46 18 9.2 5.2
,0.0003 ,0.005 ,0.02 ,0.05
perceptual saliency. Table 4 reports all the statistical significances obtained in this ANOVA. Overall, the ANOVA revealed a significant electrode effect, with P300 being larger at frontal sites. Again, attention significantly affected P300 independent of stimulus orientation, as reflected by larger responses to targets than non-targets (P,0.01). Very interestingly, while P300 was larger at right frontal sites, as indicated by the significant main factor hemisphere, the attention effect tended to be larger at left sites, as shown by the interaction of attention3hemisphere. More importantly, the ANOVA showed an effect of orientation in interaction with attention and hemisphere. Post-hoc comparisons showed larger P300s to vertical than oblique orientations (see Fig. 7), and greater attention effects at left frontal sites for both types of stimuli, this asymmetry being larger for vertical (P, 0.01) than for oblique (P,0.05) stimuli.
4. Discussion In this experiment macroscopic differences in the morphology of visual evoked potentials and magnitude of attention effects were found between vertical and oblique gratings. Very interestingly, a posterior selection negativity to attended gratings was absent in response to oblique orientations, and attention effects were smaller in the attend-oblique than attend-vertical condition. Surprisingly, the anterior P300 was even larger to vertical non-target than oblique target gratings. In other words, the perceptual oblique effect (i.e. the advantage of orthogonal vs. oblique gratings) was more powerful than top-down attentional processes in determining an enhanced neural processing. Overall, our findings indicate the crucial role of physical features, such as stimulus orientation, in affecting the activity of attention selection mechanisms. Indeed, the amplitude modulation of ERP components depended strongly on stimulus orientation in relation to the oblique effect. This effect is well known in psychophysical and neurophysiological literature [5,13,24], which extensively reports a better visual acuity and performance in discrimination tasks with orthogonal than oblique gratings. This effect has also been investigated by means of electrophysiological recordings. For example, the visual evoked potential (VEP) studies by Rabin [28] and Arawaka [3]
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reported shorter VEP latencies for horizontal and vertical than for oblique gratings (308 and 608 in the former study, 458 and 1358 in the latter study). The fMRI study by Furmanski and Egel [9] revealed the probable neurofunctional basis of this effect in humans, demonstrating that the activation of neurons in V1 is greater to horizontal and vertical than to oblique orientations (458 or 1358). In our study, P1 and P300 components were larger to vertical than oblique gratings independent of the attention condition. Behavioral data were consistent with electrophysiological data, showing faster RTs and a better discrimination to vertical than oblique stimuli. We also found an interesting correlation between behavioral (hits and FAs) and electrophysiological data, as indexed by P300 amplitude. In more detail, the performance was better for stimuli having the extreme oblique orientation (i.e. 508 and 1308) compared to other oblique stimuli, and this effect was related to the arising of larger P300s to these than other targets with intermediate oblique orientations (i.e. 708 and 1108). In our view, this effect was probably related to the subject’s certainty in discriminating target from non-target patterns: the greater the certainty, the larger and earlier the P3 and relative attention effects. This finding is very similar to other findings reported in the ERP literature. For example, Zani and Proverbio [38] in a study adopting an attention to check-size paradigm found higher hit rates, faster RTs and larger P3 responses to the 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 spatial frequency than the intermediate ones. This was probably due to the fact that the extreme check sizes were easier to recognize at sensory / perceptual level as they were not accompanied by confusing non-target distractors at the lower and higher size scale. Interestingly, as in the study cited, in our investigation P300 differences in amplitude and topography affected the prefrontal area (see maps of Fig. 6), which is related somehow or other to cingulate activity and task difficulty factors. To our knowledge, the present ERP study is the only one in the literature which has adopted spatial frequency gratings so close in orientation (208 difference between one and the next) in a selective discrimination task. Several previous studies adopted only vertical and horizontal orientations [11,18,20,21,26,29], which of course are readily distinguishable from each other, whereas O’Donnel and co-workers [25] adopted 458 and 908 gratings. With the exception of Karayanidis and Michie [18], who found an attention modulation of a posterior P125 component, all the other studies reported attention effects indexed by a posterior selection negativity not earlier than 150 ms. The main findings of the present experiment concern the timing of attentional selection and the scalp distribution of attention-related ERP activity. All in all, our data showed an early attention modulation of P1 response at temporal area (80–140 ms) for both vertical and oblique gratings.
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The timing of this early attention effect is pretty much in line with Karayanidis and Michie’s [18] findings. As for the scalp topography of this early attention effect, the present results indicate an activation of temporal areas during orientation selection. Although ERPs do not provide a direct knowledge of the intracerebral sources of the various foci of activation recorded at scalp surface, these findings are substantially consistent with recent neurophysiological 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 it too is specifically involved in orientation processing. This, in our view, lends support to the robustness of our results notwithstanding the ERP limitations in neural source localization. For example, Vogels and Orban [34] and Tanaka [33] found that cells of the inferior temporal cortex in monkey were strongly activated during orientation discrimination and object discrimination, respectively, whereas Kawashima [19], when measuring regional cerebral blood flow with PET, found a specific activation of the left inferior temporal cortex during object discrimination in humans. Our ERP findings indicate that temporal area activity may be modulated by visual attention processes at a very early stage of processing. In this regard, Schroeder et al. [31] described an early modulatory effect in V4 and in the inferior temporal regions of monkeys (IT), which bypassed V1 and preceded the excitatory feedforward 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 areas) may be modulated by top-down attentional processes. Certainly, further investigations are needed before any definitive conclusion can be reached, especially as far as electrophysiological studies on humans are concerned. The present ERP findings also support the hypothesis of a special involvement of the left hemisphere in object discrimination, as suggested also by a very recent neuroimaging study [10], as well as some ERP attention studies [7,38]. For example, Dupont et al. [6] used PET during tasks involving simultaneous orientation discrimination, identification and detection tasks in humans, with all tasks using the same pair of vertical and oblique gratings. The subtraction of detection from simultaneous discrimination revealed an activation of right fusiform, right lingual, left precentral, left cingulate and left temporal cortex. Both waveform data and topographical maps obtained in our study suggest a left-sided hemispheric asymmetry for the attention effect. Although it did not reach statistical significance at an early processing stage, as reflected by P1 and N2 components, probably because of some variability across subjects, the hemispheric asymmetry was very strong at P300 level. It occurred in the form of larger P300 responses and attentional effects of the left hemisphere to target than non-target stimuli both at posterior and anterior sites.
A further bold hypothesis is that the hemispheric asymmetry found in both performance and amplitude measures of ERP components for oblique gratings of 508 (‘pointing’ to the left) with respect to those of 1308 (‘pointing’ to the right) is related to the fact that the latter were actually preferred by the left hemisphere. For the time being, however, this hypothesis is still pure speculation.
5. Summary In conclusion, the present data do not support the view that the first effect of attention to non-spatial features (such as grating orientation) is represented by the occipital selection negativity (SN), as reported for example by Hillyard [17] or Schroeder et al. [30]. Instead, they indicate an early increase in positivity to target stimuli (both verticals an oblique) in the P1 latency range (80–140 ms). Topographic mapping of our ERP data indicates that this early attentional increase in positivity is focused at temporal scalp sites. Last but not least, our data also show the strong interdependence between stimulus physical features and attentional processes, which result in a very different pattern of results as a function of stimulus orientation (both in terms of visual event-related potentials and their attentional modulation).
Acknowledgements This work was supported by a 40% MURST grant to Alice Mado Proverbio. We are grateful to Ian McGilvray for revising the manuscript, and to two anonymous referees for their comments on and criticism of a previous version of this paper.
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Research report
Early involvement of the temporal area in attentional selection of grating orientation: an ERP study Alice Mado Proverbio b
a,b,c ,
*, Paola Esposito c , Alberto Zani b
a Department of Psychology, University of Milano-Bicocca, Piazza dell’ Ateneo Nuovo, 1, 20126 Milan, Italy Institute of Bioimaging and Molecular Physiology in Humans, Consiglio Nazionale delle Ricerche, Via Fratelli Cervi 93, 20090 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 (80–140 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. 2002 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 Several functional neuroimaging studies have shown that visual attention selection modulates activity of the dorsal and ventral streams of the visual system [4,14,35]. This modulation has been also observed by measuring changes in amplitude, latency and scalp topography of event-related potentials (ERPs) to visual stimuli as a function of task relevance and attention condition (e.g. Refs. [1,22,38]). A large number of ERP studies have attempted to *Corresponding author. Department of Psychology, University of Milano-Bicocca, Piazza dell’Ateneo Nuovo, 1, 20126 Milano, Italy. Tel.: 139-02-2171-7511. E-mail addresses: [email protected] or [email protected] (A.M. Proverbio).
investigate the neurofunctional bases of feature selection, and to determine the stage at which top-down processes such as attention can affect sensory processing. The effect of selective attention to spatial frequency and orientation on ERPs in humans was first measured in the pioneering studies of Harter and co-workers [11,12,26]. They found that attention enhanced N1 and N2 components of ERPs, giving rise to a broad negative response called selection negativity which peaked at about 250 ms post-stimulus. Later electrophysiological studies described modulation 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] and color [2]. However, relatively few studies provided evidence of an early modulation of surface sensory evoked activity recorded at visual areas during selective attention to non-spatial features (e.g. Refs. [8,17,30]). These differ-
0926-6410 / 02 / $ – see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S0926-6410( 01 )00103-3
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ences across findings reported in the electrophysiological literature might be due to a series of methodological factors, including differences in stimulus presentation rate: a fast presentation rate along with a very short presentation duration is associated with small early effects (see for example the study by Annlo-Vento and Hillyard [1] adopting a SOA of only 150 ms, and a presentation duration of only 32 ms). Again, differences in ERP quantification methods may be responsible for different experimental results. For example, measuring at fixed latency intervals (as in Ref. [26]) may not be the best way to detect early amplitude modulations of responses to gratings of different spatial frequencies, since VEP morphology is strongly affected by the latter. In addition, it should be borne in mind that V1-related activity is much smaller than that due to the activity of other associative visual areas (i.e. V2, V4, etc.), as shown by neurophysiological literature [23]. This implies that, in order to appreciate any attention modulation effect at sensory component level, it is crucial for ERP waveforms to have a good signal-to-noise ratio. To this end, it is necessary to provide good sensory stimulation (in terms of luminance, contrast and presentation duration of stimuli) in order to obtain sensory-evoked responses of appreciable amplitude. An example of this effect may be appreciated by comparing the amplitude of evoked responses to spatial frequency gratings presented for 10 ms at 5% contrast (as in Ref. [16]) with those presented for 100 ms at 50% contrast (as in Ref. [38]). It is obvious that an increase of 10% in the amplitude of the evoked response (as for the attentional modulation of the N115 reported in Ref. [38]) would be more consistent if the recorded response was sufficiently large (e.g. several microvolts instead of 1 mV). Another effect which might contribute to reducing the presence of attention effects on early sensory responses is the combined use of symbolic cues (alphanumeric characters) with other, selected, non-spatial features. Several 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 material failed to produce any attention effect earlier than 150 ms [15,36,37]. As far as the attentional selection of stimulus orientation in particular is concerned, in classical literature this nonspatial feature has been described as one of the latest physical features (in terms of ERP latency) to be attentionally selected by human observers, following location, color and spatial frequency. However, in all previous studies, with the exception of O’Donnel et al. [25], who adopted gratings of 458 and 908, only vertical and horizontal orientations, which are of course easily distinguishable from each other, were used as stimuli [11,18,20,21,26,29]. We believe that the use of stimuli so macroscopically different in terms of luminance distribution and local spatial frequency spectrum, compared to stimuli differing only slightly in spatial frequency, size or shape, might have contributed to reducing the need for an accurate
sensory gating. This might have slowed down the latency of the earliest sign of attentional modulation for stimulus orientation. Having found evidence of early attentional modulation for spatial frequency [38,39], which is processed by visual neurons selectively tuned to both spatial frequency and orientation, we sought to further investigate orientation selection mechanisms by adopting a task requiring difficult levels of orientation discrimination compared to previous ERP studies dealing with this stimulus feature. We therefore endeavoured to improve as far as possible the quality of the ERP waveforms recorded (especially the earliest VEP responses). Briefly, the goal of the present study was to shed some light on the mechanisms subserving attentional selection of orientation by adopting task conditions aimed at producing ERP waveforms (and especially early responses) with as good a signal-to-noise ratio as possible. In this study, we adopted large gratings, foveally presented for 80 ms with a contrast of 60%. To guarantee a good signal-to-noise ratio each of five differently oriented gratings were presented 600 times. The inter-stimulus interval was relatively long (850–1000 ms), and instructions were given at the beginning of each block of trials in a sustained attention condition. Overall, the investigation was aimed at determining the timing of attentional selection for a nonspatial feature, which is well known to engage mainly the ventral visual pathway. To make orientation discrimination challenging enough for visual selection mechanisms, so as to make the highest demands on attentional resources, five gratings differing only by 208 in orientation were adopted as stimuli in the present study. Four of them were oblique with respect to the vertical meridian. The use of oblique vs. orthogonal gratings produced a difference in perceptual difficulty of discrimination that is strongly reflected in ERP and behavioral measures, and is described in the literature as the ‘oblique effect’ [3,5,9,13,28].
2. Materials and methods
2.1. Participants Ten young persons (five males and five females; mean age, 23 years) participated in this experiment as volunteers. All were right handed and had a normal or corrected-tonormal vision. Two of them were rejected for excessive muscular and / or ocular artifacts before ERP averaging.
2.2. Stimuli and procedure Participants were seated in a dimly lit, acoustically and electrically shielded cubicle situated 114 cm from a TV screen. They were instructed to fixate a cross at the center of the screen and avoid any kind of eye or body movement. Stimuli were equiprobable, isoluminant black-andwhite square-wave gratings (3 cpd of spatial frequency)
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having 508, 708, 908 (vertical), 1108 and 1308 orientation with respect to the horizontal meridian. The gratings’ average luminance was about 33 cd / m 2 , and their stimulus contrast was 60%. Stimuli were randomly presented for 80 ms in the foveal portion (28 of visual angle) of the central visual field. The interstimulus interval (ISI) was varied randomly between 850 and 1000 ms. Each grating was presented 600 times for a total number of 3000 gratings presented to each of the 10 subjects. For each of the five attention conditions and five stimulus orientations the ERP were averaged across about 120 trial repetitions. The task consisted in selectively attending and responding to a given orientation by pressing a button as accurately and fast as possible with the index finger while ignoring the other stimuli. The two hands were used alternatively during the recording session, and the hand order was counterbalanced across subjects.
2.3. Electrophysiological recording The electroencephalogram (EEG) was continuously recorded from 28 scalp sites using tiny Ag /AgCl electrodes mounted on an elastic cap (Electro-cap, Inc.). The electrodes were located at frontal (Fp1, Fp2, FZ, F3, F4, F7, F8), central (CZ, C3, C4), temporal (T3, T4), posterior-temporal (T5, T6), parietal (PZ, P3, P4), and occipital scalp sites (OZ, O1, O2) of the International 10-20 System. Additional electrodes were placed half way between the anterior-temporal and central sites (FTC1, FTC2), the central and parietal sites (CP1, CP2), the anterior-temporal and parietal sites (TCP1, TCP2), and the posterior-temporal and occipital sites (OL, OR). Blinks and vertical eye movements (i.e. EOG) were monitored by means of two electrodes placed below and above the right eye, while horizontal movements were recorded by electrodes placed at the outer canthi of the eyes. Linked ears served as reference lead. The EEG and the EOG were amplified with a half-amplitude band pass of 0.01–70 Hz and 0.1–70 Hz, respectively. Electrode impedance was kept below 5 kV. Continuous EEG and EOG were digitized at a rate of 512 samples per second. Computerized artifact rejection was performed before averaging to discard epochs in which eye movements, blinks, excessive muscle potentials or amplifier blocking occurred. The artifact rejection criterion was: peak to peak amplitude exceeding 650 mV. The artifact rejection rate 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 excluded from further analysis. For each subject, distinct ERP averages were obtained as a function of grating orientation and attention condition. The major ERP components were identified and measured automatically by a computer program with reference to the baseline voltage averages over the interval from 2100 to 0 ms. ERP components were labeled according to a polarity-latency
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convention and quantified by measuring peak latency and baseline-to-peak amplitude values within a specific latency range centered approximately on the peak latency of the deflection observed in the grand average waveforms. At posterior sites (O1, O2, OL, OR, T5, T6) P1 positive deflection was identified in the time window between 90 and 140 ms. Additionally, an early P1 positivity was measured at the temporal area at T3 and T4 electrode sites, and quantified by means of mean area computing between 80 and 140 ms of post-stimulus latency. N1 and N2 negative deflections were identified in the time windows between 100 and 200 ms, and 200 and 300 ms, respectively. An anterior positivity was identified in the time window between 270 and 430 ms at temporal (T3, T4), central (C3, C4), frontal (F3, F4), centro-parietal (CP1, CP2), centrotemporal parietal (TCP1, TCP2) electrode sites. In the same time window P300 was measured at midline sites Cz, Fz, Pz, Oz. A posterior positivity was recorded and measured at O1, O2, OL, OR, T5, T6 occipito-temporal sites. In the same time window a frontal positivity was measured at F3, F4, F7, F8, FTC1, FTC2 electrode sites. ERP amplitude and latency measures were analyzed using repeated-measure analyses of variance (ANOVAs), separately for each ERP component. ERPs to oblique and vertical gratings were analyzed separately. For oblique gratings, factors were ‘orientation’ (508, 708, 908, 1108 and 1308), ‘attention’ (target and non-target), ‘electrode site’ (depending on the ERP component of interest) and ‘cerebral hemisphere’ (left and right). For vertical gratings the orientation factor was omitted (see Electrophysiological data for an explanation of these separate analyses). Greenhouse–Geisser corrections were employed to reduce the positive bias resulting from repeated factors with more than two levels. Post-hoc Tukey testing was carried out for multiple mean comparisons. Topographical voltage maps of ERP components were obtained by plotting color-coded iso-potential contour lines obtained by interpolation of voltage values between scalp electrodes at specific latencies. For each subject, hit and false alarm (FAs) percentages were converted to arcsine values and subjected to a twoway repeated-measures ANOVA. Reaction times not faster than 140 ms, and not exceeding the mean value 62 standard deviations were subjected to a three-way repeated-measures ANOVA. Factors were ‘orientation’ (508, 708, 908, 1108 and 1308), ‘attention’ (target and nontarget), and ‘response hand’ (left and right).
3. Results
3.1. Behavioral data The mean percentage of correct responses (independent of stimulus orientation) was 93%, whereas the mean percentage of false alarms (FAs) was 3.23%. Fig. 1a and b show hit and FA percentages as a function of stimulus
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difference in response time to vertical than oblique orientation (P,0.01), with a strong bias towards the former.
3.2. Electrophysiological data
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.
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 (P,0.05) for oblique stimuli of 1308 orientation than for 1108 orientation. Mean reaction time (RT) to gratings was about 460 ms (see Fig. 1c). The ANOVA performed on RT data showed a significant effect of stimulus orientation (F4,10549.5; P,0.0000). Post-hoc comparisons indicated a significant
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.
3.3. Vertical gratings 3.3.1. P1 deflection Table 1 reports all significant factors found in the various ANOVAs performed in the present study on ERP values recorded for vertical target and non-target gratings. ANOVA performed on P1 mean amplitude values
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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.
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
hemisphere. While P1 was larger at posterior occipital sites, the effect of attention, as revealed by the differencewave 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
Fig. 3. Grand average (N58) ERP waveforms recorded at right lateral occipital sites in response to stimuli of different orientations independent of task relevance.
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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 Hemisphere Electrode3hemisphere Attention Hemisphere Hemisphere Attention Hemisphere Attention3hemisphere Attention3elec.3hem. Attention Electrode Electrode3hemisphere Attention Attention3hemisphere Electrode Attention Attention3electrode Electrode Attention Attention3hemisphere Attention Electrode Attention3electrode Attention3hemisphere Electrode3hemisphere
2,14 1,7 2,14 4,28 1,13 1,7 4,28 4,28 4,28 8,56 4,28 5,35 5,35 4,28 4,28 3.21 4,28 12.84 2,14 4,28 4,28 4,28 2,14 8,56 8,56 2,14
5.6 5.26 6.8 3.3 12.2 5.69 2.7 8.23 8.23 4.05 2.9 6.67 3.12 12.23 2.8 13.28 9.65 2 7.5 6.36 5.46 9.64 21.51 2.98 2.98 7.02
,0.02 ,0.05 ,0.01 ,0.025 ,0.01 ,0.05 ,0.05 ,0.0002 ,0.0002 ,0.007 ,0.05 ,0.0002 ,0.02 ,0.0000 ,0.05 ,0.0000 ,0.0000 ,0.03 ,0.007 ,0.001 ,0.02 ,0.0000 ,0.0001 ,0.007 ,0.004 ,0.01
Temporal P1 Occipital N1 Occipital N2
Occipital N2 latency Anterior P300
Midline P300
Posterior P300
Temporal P300
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 80–140 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.
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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.
3.3.2. 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).
3.3.3. 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.
T3 20.728 1
508 non-target T4 0.45 1.1
T3 21.402 0.9
708 non-target T4 0.197 1
T3 21.509 0.5
1108 non-target T4 20.303 1.2
T3 21.165 0.9
1308 non-target T4 0.185 1
T3 21.369 0.9
T4 20.368 0.7
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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 of attention3electrode3hemisphere. Post-hoc comparisons indicated that N2 was larger to attended than to unattended gratings at mesial occipital and lateral occipital sites. At the latter sites the attention effect was larger on the right hemisphere (P,0.05). This hemispheric asymmetry for the attention effect is visible in waveforms in Fig. 4 and the maps in Fig. 6. The ANOVA performed on mean latency values of N2 component yielded the significant effect of attention, indicating faster latencies for N2 to attended (241 ms) than to unattended (252 ms) gratings.
3.3.4. P300 deflection An anterior late positive response, larger at centroparietal and central sites, was measured in the time interval between 270 and 430 ms. Attention had a very significant effect in this latency range. Post-hoc comparisons showed that selectively paying attention to the vertical gratings
produced a much larger P300 response compared to when the same stimuli were unattended (P,0.01). This anterior P300 was asymmetrically distributed as indicated by the significant interaction of electrode3hemisphere. Post-hoc tests proved that anterior P300 was larger at left than right parietal sites (P,0.01). A further interaction of attention3 hemisphere showed that P300 to targets was of greater amplitude over the left than the right hemisphere (P, 0.01), whereas no hemispheric asymmetry was present for P300 to unattended gratings. P300 recorded at midline sites was also subjected to an ANOVA. Consistent with previous analyses, the electrode effect reflected larger P300 at central sites, while the attention effect reflected larger responses to attended than to unattended gratings. The significant interaction of attention3electrode showed that attention significantly affected P300 responses at more anterior (Fz and Cz) than posterior (Pz and Oz) sites (P,0.01).
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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 hemisphere.
P300 recorded at posterior sites in the same time window was maximally distributed at lateral occipital and posterior temporal sites (P,0.01). The effect of attention reflected larger P300 responses to target than non-target stimuli, while the significant interaction of attention3 hemisphere reflected a hemispheric asymmetry in the attention effect. Post-hoc comparisons indicated larger attention effects and P300 to targets at left than right hemispheric sites (P,0.01), as is shown in Fig. 7.
3.4. Oblique gratings The significant results of the separate ANOVAs carried out on mean area amplitude, peak amplitude and latency of
3.4.1. P1 deflection The ANOVA performed on mean area recorded at temporal areas in the 80–140 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. 3.4.2. N1 and N2 deflections The ANOVAs performed on later negative peaks (N1 and N2) failed to show any effect of attention on these components: no selection negativity was observed for oblique gratings, which probably activated partially overlapping neural channels tuned to similar orientations and the same spatial frequency of targets (see Fig. 8). 3.4.3. P300 deflection P300 measured at anterior sites was larger at centroparietal and central sites (P,0.01). The effect of attention was also significant, although it was smaller than observed in the attend-vertical condition. In fact, post-hoc comparisons among means showed greater P300s to target than 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 Hemisphere Electrode Hemisphere3electrode Attention Attention3electrode Orientation3attent.3elec. Attention Electrode Electrode Attention Attention3electrode Attention3orientation Attention Electrode Attention Attention3hemisphere Attention3orientation Electrode Attention
1,7 1,7 1,7 5,35 2,14 10,70 10,70 2,14 5,35 3,21 2,14 6,42 6,42 2,14 2,14 2,14 2,14 6,42 2,14 2,14
12.21 15.98 16 3.97 3.63 5.42 1.7 3.8 4.8 13.48 3.8 4.87 3.8 18.14 5.82 7.6 4.7 4.31 9.18 7.66
,0.01 ,0.01 ,0.0001 ,0.006 ,0.05 ,0.0000 ,0.01 ,0.0002 ,0.002 ,0.0000 ,0.05 ,0.0001 ,0.05 ,0.0001 ,0.02 ,0.002 ,0.03 ,0.002 ,0.003 ,0.006
Anterior P300
Anterior P300 latency Midline P300
Midline P300 latency Posterior P300
Posterior P300 latency
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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 interestingly, P300s to target oblique gratings were smaller than that elicited by the same stimuli when non-targets because vertical gratings were attended (P,0.05). Moreover, the significant interaction of attention3electrode showed greater attention effects at centro-parietal and frontal (P, 0.01) than other electrode sites. Again, the ANOVA displayed a significant hemisphere3electrode interaction, reflecting a hemispheric asymmetry in P300 distribution that was larger at left sites over the parietal area (P,0.01). Very interestingly, the ANOVA also yielded the significant effect of orientation3attention3electrode. Post-hoc comparisons indicated larger P300s to target than nontarget stimuli, especially at centroparietal sites, and greater attention effects (larger differences between P300 to target than non-target orientations) to stimuli oriented to 508 (P,0.05) or 1308 (P,0.01) rather than to 708 or 1108. This piece of data might reflect a slight advantage in discriminating these extreme orientations — consistent with behavioral data (namely hit and FA rates) — which were less confused with similar orientations than 708 or 1108 stimuli. As for P300 latency, it was earlier at anterior than posterior sites, and to target than non-target stimuli. A separate ANOVA was performed on P300 values recorded at midline sites in the same temporal interval. Consistent with previous data, the P300 was larger at central electrode sites, and to oblique targets than oblique non-targets. Again, post-hoc comparisons proved that P300 to oblique targets was actually smaller than to the same stimuli when a vertical grating was attended (P,0.05). The interaction of attention3electrode was also significant,
indicating greater attention effects for oblique gratings at frontal (P,0.01) but not centroparietal sites (as in the case of vertical gratings), as shown in the maps in Fig. 7. The interaction of attention3orientation indicated greater P300 amplitudes to target stimuli having extreme orientations, i.e. 508 (P,0.05) and especially 1308 (P,0.01). At midline sites P300 latency was also affected by attention being earlier to target than to non-target stimuli (P,0.01). The posterior P300 was larger at lateral occipital and posterior temporal sites. Again, it was larger to targets than non-targets, except for the case in which vertical gratings were attended. Also significant was the interaction of orientation3attention, which showed larger attention effects (P,0.01) for extreme orientations of 508 and 1308. Consistent with data obtained for vertical gratings, P300 amplitude was significantly affected by attention in interaction with the factor hemisphere. Indeed, attention effects were larger at left recording sites (P,0.05). The analyses of latency showed earlier P300 responses to targets than to non-targets and earlier P300 at lateral occipital (than more temporal) sites.
3.5. Oblique vs. vertical gratings Notwithstanding the macroscopic differences in VEPs as a function of stimulus orientation (especially at P300 level, as visible from waveforms of Fig. 3), a separate repeatedmeasures four-way ANOVA was performed on P300 values recorded at frontal and centro-temporal sites (F3, F4, F7, F8, FTC1, FTC2) to vertical and oblique gratings, in order directly to compare the brain processing of these two kinds of stimuli, which are very different in terms of
A.M. Proverbio et al. / Cognitive Brain Research 13 (2002) 139 – 151 Table 4 Statistical significances of ANOVAs performed on P300 mean amplitudes recorded to oblique and vertical gratings at anterior sites in the P300 latency range as a function of attention condition, electrode site and hemisphere ERP deflection
Factors
df
F
P value
Frontal P300
Attention Electrode Hemisphere Attention3hem.3orient.
1,7 1,7 1,7 1,7
46 18 9.2 5.2
,0.0003 ,0.005 ,0.02 ,0.05
perceptual saliency. Table 4 reports all the statistical significances obtained in this ANOVA. Overall, the ANOVA revealed a significant electrode effect, with P300 being larger at frontal sites. Again, attention significantly affected P300 independent of stimulus orientation, as reflected by larger responses to targets than non-targets (P,0.01). Very interestingly, while P300 was larger at right frontal sites, as indicated by the significant main factor hemisphere, the attention effect tended to be larger at left sites, as shown by the interaction of attention3hemisphere. More importantly, the ANOVA showed an effect of orientation in interaction with attention and hemisphere. Post-hoc comparisons showed larger P300s to vertical than oblique orientations (see Fig. 7), and greater attention effects at left frontal sites for both types of stimuli, this asymmetry being larger for vertical (P, 0.01) than for oblique (P,0.05) stimuli.
4. Discussion In this experiment macroscopic differences in the morphology of visual evoked potentials and magnitude of attention effects were found between vertical and oblique gratings. Very interestingly, a posterior selection negativity to attended gratings was absent in response to oblique orientations, and attention effects were smaller in the attend-oblique than attend-vertical condition. Surprisingly, the anterior P300 was even larger to vertical non-target than oblique target gratings. In other words, the perceptual oblique effect (i.e. the advantage of orthogonal vs. oblique gratings) was more powerful than top-down attentional processes in determining an enhanced neural processing. Overall, our findings indicate the crucial role of physical features, such as stimulus orientation, in affecting the activity of attention selection mechanisms. Indeed, the amplitude modulation of ERP components depended strongly on stimulus orientation in relation to the oblique effect. This effect is well known in psychophysical and neurophysiological literature [5,13,24], which extensively reports a better visual acuity and performance in discrimination tasks with orthogonal than oblique gratings. This effect has also been investigated by means of electrophysiological recordings. For example, the visual evoked potential (VEP) studies by Rabin [28] and Arawaka [3]
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reported shorter VEP latencies for horizontal and vertical than for oblique gratings (308 and 608 in the former study, 458 and 1358 in the latter study). The fMRI study by Furmanski and Egel [9] revealed the probable neurofunctional basis of this effect in humans, demonstrating that the activation of neurons in V1 is greater to horizontal and vertical than to oblique orientations (458 or 1358). In our study, P1 and P300 components were larger to vertical than oblique gratings independent of the attention condition. Behavioral data were consistent with electrophysiological data, showing faster RTs and a better discrimination to vertical than oblique stimuli. We also found an interesting correlation between behavioral (hits and FAs) and electrophysiological data, as indexed by P300 amplitude. In more detail, the performance was better for stimuli having the extreme oblique orientation (i.e. 508 and 1308) compared to other oblique stimuli, and this effect was related to the arising of larger P300s to these than other targets with intermediate oblique orientations (i.e. 708 and 1108). In our view, this effect was probably related to the subject’s certainty in discriminating target from non-target patterns: the greater the certainty, the larger and earlier the P3 and relative attention effects. This finding is very similar to other findings reported in the ERP literature. For example, Zani and Proverbio [38] in a study adopting an attention to check-size paradigm found higher hit rates, faster RTs and larger P3 responses to the 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 spatial frequency than the intermediate ones. This was probably due to the fact that the extreme check sizes were easier to recognize at sensory / perceptual level as they were not accompanied by confusing non-target distractors at the lower and higher size scale. Interestingly, as in the study cited, in our investigation P300 differences in amplitude and topography affected the prefrontal area (see maps of Fig. 6), which is related somehow or other to cingulate activity and task difficulty factors. To our knowledge, the present ERP study is the only one in the literature which has adopted spatial frequency gratings so close in orientation (208 difference between one and the next) in a selective discrimination task. Several previous studies adopted only vertical and horizontal orientations [11,18,20,21,26,29], which of course are readily distinguishable from each other, whereas O’Donnel and co-workers [25] adopted 458 and 908 gratings. With the exception of Karayanidis and Michie [18], who found an attention modulation of a posterior P125 component, all the other studies reported attention effects indexed by a posterior selection negativity not earlier than 150 ms. The main findings of the present experiment concern the timing of attentional selection and the scalp distribution of attention-related ERP activity. All in all, our data showed an early attention modulation of P1 response at temporal area (80–140 ms) for both vertical and oblique gratings.
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The timing of this early attention effect is pretty much in line with Karayanidis and Michie’s [18] findings. As for the scalp topography of this early attention effect, the present results indicate an activation of temporal areas during orientation selection. Although ERPs do not provide a direct knowledge of the intracerebral sources of the various foci of activation recorded at scalp surface, these findings are substantially consistent with recent neurophysiological 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 it too is specifically involved in orientation processing. This, in our view, lends support to the robustness of our results notwithstanding the ERP limitations in neural source localization. For example, Vogels and Orban [34] and Tanaka [33] found that cells of the inferior temporal cortex in monkey were strongly activated during orientation discrimination and object discrimination, respectively, whereas Kawashima [19], when measuring regional cerebral blood flow with PET, found a specific activation of the left inferior temporal cortex during object discrimination in humans. Our ERP findings indicate that temporal area activity may be modulated by visual attention processes at a very early stage of processing. In this regard, Schroeder et al. [31] described an early modulatory effect in V4 and in the inferior temporal regions of monkeys (IT), which bypassed V1 and preceded the excitatory feedforward 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 areas) may be modulated by top-down attentional processes. Certainly, further investigations are needed before any definitive conclusion can be reached, especially as far as electrophysiological studies on humans are concerned. The present ERP findings also support the hypothesis of a special involvement of the left hemisphere in object discrimination, as suggested also by a very recent neuroimaging study [10], as well as some ERP attention studies [7,38]. For example, Dupont et al. [6] used PET during tasks involving simultaneous orientation discrimination, identification and detection tasks in humans, with all tasks using the same pair of vertical and oblique gratings. The subtraction of detection from simultaneous discrimination revealed an activation of right fusiform, right lingual, left precentral, left cingulate and left temporal cortex. Both waveform data and topographical maps obtained in our study suggest a left-sided hemispheric asymmetry for the attention effect. Although it did not reach statistical significance at an early processing stage, as reflected by P1 and N2 components, probably because of some variability across subjects, the hemispheric asymmetry was very strong at P300 level. It occurred in the form of larger P300 responses and attentional effects of the left hemisphere to target than non-target stimuli both at posterior and anterior sites.
A further bold hypothesis is that the hemispheric asymmetry found in both performance and amplitude measures of ERP components for oblique gratings of 508 (‘pointing’ to the left) with respect to those of 1308 (‘pointing’ to the right) is related to the fact that the latter were actually preferred by the left hemisphere. For the time being, however, this hypothesis is still pure speculation.
5. Summary In conclusion, the present data do not support the view that the first effect of attention to non-spatial features (such as grating orientation) is represented by the occipital selection negativity (SN), as reported for example by Hillyard [17] or Schroeder et al. [30]. Instead, they indicate an early increase in positivity to target stimuli (both verticals an oblique) in the P1 latency range (80–140 ms). Topographic mapping of our ERP data indicates that this early attentional increase in positivity is focused at temporal scalp sites. Last but not least, our data also show the strong interdependence between stimulus physical features and attentional processes, which result in a very different pattern of results as a function of stimulus orientation (both in terms of visual event-related potentials and their attentional modulation).
Acknowledgements This work was supported by a 40% MURST grant to Alice Mado Proverbio. We are grateful to Ian McGilvray for revising the manuscript, and to two anonymous referees for their comments on and criticism of a previous version of this paper.
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