This study aimed at characterizing whether the egocentric position of a visual target affects the event-related potentials (ERPs) recorded in EEG. In particular, we wanted (1) to determine if there is a privileged cortical processing of the straight-ahead direction, as previously reported in publications based on single-cell recordings in macaque (Durand et al. 2010) and neuroimaging data in human (Strappini et al. 2015) and (2) to exploit the high temporal resolution of EEG to characterize the dynamics of the underlying neural mechanisms. Our two experiments were designed to elicit strong visual ERPs with components that corresponded to those that are usually reported in EEG vision studies.
EEG responses to visual stimulations along the horizontal meridian
In the first experiment, we analyzed the ERPs to visual stimuli displayed along the horizontal meridian (either to the left of to the right of ocular fixation) in 29 subjects. Figure 2a shows the grand average (across subjects, across the left and right retinal positions and across the straight-ahead and eccentric conditions) ERP in black. The green time-course corresponds to the associated Global Field Power (GFP). From these time-courses, we can extract three components: (1) the positive, bilateral and occipital P1 that peaks around 140 ms after stimulus onset, (2) the negative, occipital and bilateral N1 that peaks around 198 ms and (3) the positive and central P2-P3 that peaks around 299 ms (Fig. 2b). Those latencies are, respectively, marked by red, blue and magenta vertical lines in the figure. They were used to define time-windows of interest that constrained our research of the components corresponding to straight-ahead and eccentric stimulations at the individual level (see the materials and methods).
The components were extracted when the signal-to-noise ratio (SNR) was sufficient to permit a robust estimation of the peak (see the materials and methods). It was the case in 21 subjects for the bilateral P1 (3.3 μV of average amplitude across these subjects), in 14 subjects for the bilateral N1 (4.7 μV) and in 26 subjects for the central P2–P3 (5.6 μV). For these subjects, the differences in amplitude between straight-ahead and eccentric stimulations are shown in Fig. 2b at the average latencies across these two conditions. Straight-ahead amplitude enhancement of the P1, N1 and P2/3 components were, respectively, equal to 0.2 μV (7% of increase), 0.3 μV (7%) and 0.2 μV (3%).
The electrode utilization frequency in the definition of those peaks across subjects is shown in the leftward topographies (Fig. 2b). The crosses indicate the 95% bootstrap confidence interval for these amplitude difference and average latencies at the population level. We can observe that straight-ahead stimulations led to significantly stronger amplitudes than eccentric stimulations for these three components, as the lower bounds of the associated confidence intervals are greater than 0. To complete our analyses, we also look for differences between the latencies associated with our two conditions. We did not find significant effects in this case as the latencies for straight-ahead and eccentric stimulations were generally in the same range.
As an additional analysis, we compared the GFPs between our two conditions (see Fig. 2c). We found two time-windows during which straight-ahead stimulations led to stronger GFPs than eccentric stimulations. Those time-windows are outlined in pale gray and overlap well with the bilateral P1 and N1 components reported above. This analysis did not permit to define a time-window with significant differences between our two conditions around the peak of the P2–P3 component. This is mostly due to the important variability of this component latency across subject (see Fig. 2b). Overall, our results demonstrate that straight-ahead stimulations lead to stronger ERP amplitudes as early as 140 ms after stimulus onset (i.e. around the bilateral P1 component).
To determine whether earlier effects could be detected in our data, we computed the grand average difference-wave ERPs across subjects and conditions corresponding to left vs right retinal stimulations (see the materials and methods). This subtraction permits to discard contributions from overlapping ERPs and thereby to define two additional components that were previously shown to peak around 80 and 160 ms after stimulus onset: the contralateral P1 and N1 (Luck 2012). The grand average differential ERP is shown in Fig. 3a following the same convention as in Fig. 2a.
In our time-courses, the contralateral P1 and N1 peak around 80 and 162 ms, respectively (see the color lines). Based on these latencies, we were able to define individual peaks in 18 subjects for the contralateral P1 and in 25 subjects for the contralateral N1 (see Fig. 3b). Statistical analysis at the individual level showed that straight-ahead stimulations led to stronger contralateral P1. This effect in early contralateral P1 was 0.16 μV on average (6%). This result was confirmed by our GFP analysis (see Fig. 3c) that detected significant difference as early as 68 ms and for a duration of around 18 ms. We did not find significant differences between amplitudes in our two conditions at the level of the contralateral N1 component. Contralateral P1 and N1 latencies for straight-ahead versus eccentric stimulations were not significantly different neither.
EEG responses to visual stimulations in the quadrants
To investigate whether the straight-ahead direction could affect the earliest measurable EEG responses from primary visual cortex (i.e. from areas V1, V2 and V3), we ran a second experiment in another group of 29 subjects. In this case, stimuli were displayed either in the upper or in the lower visual field (see Fig. 1b and the materials and methods section) so as to elicit strong responses with opposite polarities from neural populations along the lower and upper banks of the calcarine sulcus. The subtraction between EEG responses to these top versus bottom stimulations permits to optimize the extraction of two components, C1 and C2, that peak around 70 and 130 ms after stimulus onset, respectively (Di Russo et al. 2003; Miller et al. 2015).
Before the difference-wave analysis on these specific components, we controlled as a proof of robustness that the effects observed in our first experiment were also detectable in this second dataset. We, therefore, computed the mean-wave grand average (by pooling across subjects and experimental conditions) ERP and reproduced the analyses described above. The results of this analysis are shown in Fig. 4. At the individual level, the bilateral P1 and N1 components were measurable in 22 subjects. The central P2-P3 was obtained in 23 subjects. As in the first experiment, the amplitudes of these peaks were significantly stronger for straight-ahead stimulations (see the 95% confidence interval for the difference between conditions in Fig. 4b). Straight-ahead stimulations, respectively, enhanced the amplitudes of the P1, N1 and P2/3 by 0.3 μV (7% of increase), 0.3 μV (5%) and 0.3 μV (3%).
The GFP analysis confirmed these results for the bilateral N1 (see Fig. 4c). GFP for straight-ahead responses were also stronger around the peak of the bilateral P1 but the difference with GFP for peripheral stimulations did not reach significance. This absence of significance might be explained by the greater heterogeneity in stimulus positions for this second experiment. In general, latencies and amplitudes of all detected components parallel those of the first experiment.
Then we computed across subjects and conditions the grand average difference-wave ERPs for upper vs lower visual field stimulations. Upper grand average ERP was the mean of upper-left and upper-right retinal stimulations while lower grand average ERP was the mean of lower-left and lower-right retinal stimulations (see the materials and methods). This method permits to assess the C1 and C2 components (Di Russo et al. 2003, 2012; Miller et al. 2015). The grand average differential ERP is shown in Fig. 5a following the same convention as in the previous figures.
In these time-courses, the C1 and C2 components peaked at 73 and 130 ms after stimulus onset and had occipital topographies, in agreement with previous reports (Di Russo et al. 2012). At the individual level, the C1 component was measurable in 21 subjects and the C2 in 22 subjects (see the materials and methods). We did not find any significant difference between straight-ahead and eccentric stimuli at the level of the C1 component. However, our bootstrap analysis revealed that the C2 amplitude was significantly stronger for straight-ahead than for eccentric stimulations (see the corresponding confidence interval in Fig. 5b). Straight-ahead stimuli produced an increase in the individual amplitudes of the C2 equal to 0.41 μV (10%).
GFP analyses confirmed these results by showing that the earliest difference between our two conditions emerged around 130 ms after stimulus onset, i.e. around the peak of the C2 component (see Fig. 5c). As in all previous analyses, we did not detect any significant differences between the peak latencies in our two conditions. In this second experiment, the earliest measurable EEG responses were, therefore, unaffected by the spatial position of the stimulus. The first observable straight-ahead effects were observed for the bilateral P1 component around 150 ms after stimulus onset.
Spatio-temporal consistency of C1/C2 components across subjects allowed us to perform an additional analysis in SPM (see the ‘Materials and methods’ section). In Fig. 6, the first row shows spatio-temporal distribution of the T-scores for the differences between stimulations in the upper versus lower visual field (thresholded at p < 0.05, FWER). Significant differences are observed in parieto-occipital electrodes with polarities and latencies that correspond to the C1 and C2 components, in agreement with the results shown in Fig. 5. The second row shows the spatio-temporal distribution of the T-scores for the differences between straight-ahead versus eccentric stimulations (thresholded at p < 0.001, uncorrected). The earliest significant effects are observed around 150 ms after stimulus onset and are generated in centro-parietal electrodes. It matches well with the enhanced responses to straight-ahead stimulation shown in Fig. 5. Here as well, we did not find significant straight-ahead effects at earlier latencies. This result, obtained through different approaches, confirms that in our experience, straight-ahead stimulations did not lead to measurable modifications of the C1 component.
Alpha power spectral analysis
A previous study showed that gaze direction could modulate spontaneous EEG activity in the alpha band (De Toffol et al. 1992). To test whether the same effects are observable in our measurements and also whether they can be related to the straight-ahead direction, we performed a Fourier analysis of the 600 ms pre-stimulus baseline (see the ‘Materials and methods’ section). Because this analysis is based on single-trials and, therefore, more susceptible to noise, it was done on all the data from experiments 1 and 2 to increase the statistical power. Figure 7 shows the difference in pre-stimulus alpha power for a rightward versus a leftward gaze.
Significant differences are observed in the left and right occipito-parietal cortex (see the leftward panel). The rightward panel provides the average values and associated 95% intervals for all the left (L) and right (R) occipito-parietal electrodes (see the red and blue boxes in the leftward panel). Each dot corresponds to one individual subject. Note that here, we preferred to group electrodes together rather than to explore the effects at the maxima of the statistical analysis to avoid the ‘double dipping’ that arises when the same data are used both for identifying sites of interest and for characterizing their activity. The difference between effects in left versus right occipito-parietal electrodes is highly significant (p < 0.001, permutation tests) and reflects a reduction in alpha power in the hemisphere ipsilateral to gaze direction (and thus contralateral to the straight-ahead direction). We also analyzed the data from experiments 1 and 2 separately and found significant effects for experiment 1 (p < 0.001) as well but only a trend for experiment 2 (p = 0.075). This difference might reflect an additional effect of stimulus position, e.g. via expectation mechanisms. Altogether, this analysis confirms that gaze direction affects pre-stimulus preparatory activity and suggests that this modification could be directly related to the straight-ahead direction, as consistent alpha power reductions are found in the hemisphere contralateral to this spatial position.
The average RT did not differed between the two experiments. The group medians and 95% confidence intervals were, respectively 344 [330:356] and 345 [331:355] ms for the first and second experiment. The RT difference between the straight-ahead and eccentric condition was not significant in both experiments: +1 [− 1:2] ms and 0 [− 1:2] ms.