Abstract
For decades, researchers have assumed that shifts of covert attention mandatorily occur prior to eye movements to improve perceptual processing of objects before they are fixated. However, recent research suggests that the N2pc component—a neural measure of covert attentional allocation—does not always precede eye movements. The current study investigated whether the N2pc component mandatorily precedes eye movements and assessed its role in the accuracy of gaze control. In three experiments, participants searched for a letter of a specific color (e.g., red) and directed gaze to it as a response. Electroencephalograms and eye movements were coregistered to determine whether neural markers of covert attention preceded the initial shift of gaze. The results showed that the presaccadic N2pc only occurred under limited conditions: when there were many potential target locations and distractors. Crucially, there was no evidence that the presence or magnitude of the presaccadic N2pc was associated with improved eye movement accuracy in any of the experiments. Interestingly, ERP decoding analyses were able to classify the target location well before the eyes started to move, which likely reflects a presaccadic cognitive process that is distinct from the attentional process measured by the N2pc. Ultimately, we conclude that the covert attentional mechanism indexed by the N2pc is not necessary for precise gaze control.
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Notes
We had initially planned on assessing ERP decoding of the target and distractor letter identity, and the memory probe task was meant to make the letter identity task relevant. However, we found that decoding accuracy for letter identity was very low, so the letter decoding accuracy results are found in the Supplemental Materials.
We realize that Experiment 3 differed from Experiment 2 in other ways as well. In particular, the location of the targets differed in respect to the horizontal meridian. However, this should have no effect on the ability to detect an N2pc. The magnitude of the N2pc is increased for targets below the horizontal meridian but reduced for those above the meridian (Luck et al., 1997; Perron et al., 2009). Thus, when averaged together, this should be equivalent to presenting the target on the horizontal midline. Another change was the addition of new colors. However, this likely increased the efficiency of color search from Experiment 2 and may have slightly reduced demands on gaze control. Thus, we believe these changes were unlikely to induce a presaccadic N2pc component in Experiment 3.
References
Bacigalupo, F., & Luck, S. J. (2015). The allocation of attention and working memory in visual crowding. Journal of Cognitive Neuroscience, 27(6), 1180–1193. https://doi.org/10.1162/jocn_a_00771
Bae, G.-Y., & Luck, S. J. (2018). Dissociable decoding of spatial attention and working memory from EEG oscillations and sustained potentials. Journal of Neuroscience, 38(2), 409–422. https://doi.org/10.1523/JNEUROSCI.2860-17.2017
Bae, G.-Y., & Luck, S. J. (2019). Decoding motion direction using the topography of sustained ERPs and alpha oscillations. NeuroImage, 184, 242–255. https://doi.org/10.1016/j.neuroimage.2018.09.029
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological), 57(1), 289–300.
Benjamini, Y., & Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics, 29(4), 1165–1188.
Brainard, D. H. (1997). The psychophysics toolbox. Spatial Vision, 10, 433–436.
Brisson, B., Robitaille, N., & Jolicœur, P. (2007). Stimulus intensity affects the latency but not the amplitude of the N2pc. NeuroReport, 18(15), 1627. https://doi.org/10.1097/WNR.0b013e3282f0b559
Cornelissen, F. W., Peters, E. M., & Palmer, J. (2002). The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox. Behavior Research Methods, Instruments, & Computers, 34(4), 613–617. https://doi.org/10.3758/BF03195489
Dafoe, J. M., Armstrong, I. T., & Munoz, D. P. (2007). The influence of stimulus direction and eccentricity on pro- and anti-saccades in humans. Experimental Brain Research, 179(4), 563–570. https://doi.org/10.1007/s00221-006-0817-8
Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Deubel, H., & Schneider, W. X. (1996). Saccade target selection and object recognition: Evidence for a common attentional mechanism. Vision Research, 36(12), 1827–1837. https://doi.org/10.1016/0042-6989(95)00294-4
Dimigen, O., Sommer, W., Hohlfeld, A., Jacobs, A. M., & Kliegl, R. (2011). Coregistration of eye movements and EEG in natural reading: Analyses and review. Journal of Experimental Psychology: General, 140(4), 552. https://doi.org/10.1037/a0023885
Drisdelle, B. L., Aubin, S., & Jolicoeur, P. (2017). Dealing with ocular artifacts on lateralized ERPs in studies of visual-spatial attention and memory: ICA correction versus epoch rejection. Psychophysiology, 54(1), 83–99. https://doi.org/10.1111/psyp.12675
Eriksen, C. W., & Hoffman, J. E. (1972). Temporal and spatial characteristics of selective encoding from visual displays. Perception & Psychophysics, 12(2-B), 201–204.
Fahrenfort, J. J., Grubert, A., Olivers, C. N. L., & Eimer, M. (2017). Multivariate EEG analyses support high-resolution tracking of feature-based attentional selection. Scientific Reports, 7(1), 1. https://doi.org/10.1038/s41598-017-01911-0
Gaspelin, N., & Luck, S. J. (2018). Combined electrophysiological and behavioral evidence for the suppression of salient distractors. Journal of Cognitive Neuroscience, 30(9), 1265–1280. https://doi.org/10.1162/jocn_a_01279
Hanes, D. P., Thompson, K. G., & Schall, J. D. (1995). Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis. Experimental Brain Research, 103(1), 85–96. https://doi.org/10.1007/BF00241967
Hickey, C., Di Lollo, V., & McDonald, J. J. (2009). Electrophysiological indices of target and distractor processing in visual search. Journal of Cognitive Neuroscience, 21(4), 760–775. https://doi.org/10.1162/jocn.2009.21039
Hickey, C., Pollicino, D., Bertazzoli, G., & Barbaro, L. (2019). Ultrafast object detection in naturalistic vision relies on ultrafast distractor suppression. Journal of Cognitive Neuroscience, 31(10), 1563–1572. https://doi.org/10.1162/jocn_a_01437
Hoffman, J. E., & Subramaniam, B. (1995). The role of visual attention in saccadic eye movements. Perception & Psychophysics, 57(6), 787–795. https://doi.org/10.3758/BF03206794
Hollingworth, A., Richard, A. M., & Luck, S. J. (2008). Understanding the function of visual short-term memory: Transsaccadic memory, object correspondence, and gaze correction. Journal of Experimental Psychology: General, 137(1), 163. https://doi.org/10.1037/0096-3445.137.1.163
Huber-Huber, C., Ditye, T., Fernández, M. M., & Ansorge, U. (2016). Using temporally aligned event-related potentials for the investigation of attention shifts prior to and during saccades. Neuropsychologia, 92, 129–141. https://doi.org/10.1016/j.neuropsychologia.2016.03.035
Huber-Huber, C., Steininger, J., Grüner, M., Ansorge, U. (2021). Psychophysical dual-task setups do not measure pre-saccadic attention but saccade-related strengthening of sensory representations. Psychophysiology, 58(5), e13787. https://doi.org/10.1111/psyp.13787
Hunt, A. R., & Kingstone, A. (2003). Covert and overt voluntary attention: Linked or independent? Cognitive Brain Research, 18(1), 102–105. https://doi.org/10.1016/j.cogbrainres.2003.08.006
Hunt, A. R., & Kingstone, A. (2003). Inhibition of return: Dissociating attentional and oculomotor components. Journal of Experimental Psychology: Human Perception and Performance, 29, 1068–1074. https://doi.org/10.1037/0096-1523.29.5.1068
Hunt, A. R., Reuther, J., Hilchey, M. D., & Klein, R. M. (2019). The relationship between spatial attention and eye movements. In T. Hodgson (Ed.), Processes of visuospatial attention and working memory (pp. 255–278). Springer.
Irwin, D. E., Carlson-Radvansky, L. A., & Andrews, R. V. (1995). Information processing during saccadic eye movements. Acta Psychologica, 90(1–3), 261–273.
Klein, R. M. (1980). Does oculomotor readiness mediate cognitive control of visual attention? In E. Nickerson (Ed.), Attention & performance VIII (pp. 259–276). Erlbaum.
Klein, R. M., & Pontefract, A. (1994). Does oculomotor readiness mediate cognitive control of visual attention? Revisited! In C. Umiltà & M. Moscovitch (Eds.), Attention and performance 15: Conscious and nonconscious information processing (pp. 333–350). MIT Press.
Kowler, E., Anderson, E., Dosher, B., & Blaser, E. (1995). The role of attention in the programming of saccades. Vision Research, 35(13), 1897–1916. https://doi.org/10.1016/0042-6989(94)00279-U
Krebs, R. M., Boehler, C. N., Zhang, H. H., Schoenfeld, M. A., & Woldorff, M. G. (2012). Electrophysiological recordings in humans reveal reduced location-specific attentional-shift activity prior to recentering saccades. Journal of Neurophysiology, 107(5), 1393–1402. https://doi.org/10.1152/jn.00912.2010
Li, H.-H., Hanning, N. M., & Carrasco, M. (2021a). To look or not to look: Dissociating presaccadic and covert spatial attention. Trends in Neurosciences, 44(8), 669–686. https://doi.org/10.1016/j.tins.2021.05.002
Li, H.-H., Pan, J., Carrasco, M. (2021b). Different computations underlie overt presaccadic and covert spatial attention. Nature Human Behaviour.https://doi.org/10.1038/s41562-021-01099-4
Lins, O. G., Picton, T. W., Berg, P., & Scherg, M. (1993). Ocular artifacts in EEG and event-related potentials I: Scalp topography. Brain Topography, 6(1), 51–63. https://doi.org/10.1007/BF01234127
Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: An open-source toolbox for the analysis of event-related potentials. Frontiers in Human Neuroscience, 8, 213. https://doi.org/10.3389/fnhum.2014.00213
Luck, S. J. (2009). The spatiotemporal dynamics of visual-spatial attention. In F. Aboitiz & D. Cosmelli (Eds.), From attention to goal-directed behavior (pp. 51–66). Springer.
Luck, S. J. (2012). Electrophysiological correlates of the focusing of attention within complex visual scenes: N2pc and related ERP components. In S. J. Luck & E. S. Kappenman (Eds.), The Oxford handbook of event-related potential components (pp. 329–360). Oxford University Press. https://doi.org/10.1093/oxfordhb/9780195374148.013.0161
Luck, S. J., & Ford, M. A. (1998). On the role of selective attention in visual perception. Proceedings of the National Academy of Sciences, 95(3), 825–830. https://doi.org/10.1073/pnas.95.3.825
Luck, S. J., & Gaspelin, N. (2017). How to get statistically significant effects in any ERP experiment (and why you shouldn’t). Psychophysiology, 54(1), 146–157.
Luck, S. J., & Hillyard, S. A. (1994). Electrophysiological correlates of feature analysis during visual search. Psychophysiology, 31(3), 291–308.
Luck, S. J., & Hillyard, S. A. (1994). Spatial filtering during visual search: Evidence from human electrophysiology. Journal of Experimental Psychology: Human Perception and Performance, 20(5), 1000–1014. https://doi.org/10.1037/0096-1523.20.5.1000
Luck, S. J., Girelli, M., McDermott, M. T., & Ford, M. A. (1997). Bridging the gap between monkey neurophysiology and human perception: An ambiguity resolution theory of visual selective attention. Cognitive Psychology, 33(1), 64–87. https://doi.org/10.1006/cogp.1997.0660
Luck, S. J., Vecera, S. P. (2002). Attention. In Pashler, H., Yantis, S. (eds.), Steven’s handbook of experimental psychology. Vol. 1: Sensation and perception (3rd ed., pp. 235–286). John Wiley & Sons Inc. https://doi.org/10.1002/0471214426.pas0106
MacLean, G. H., Klein, R. M., & Hilchey, M. D. (2015). Does oculomotor readiness mediate exogenous capture of visual attention? Journal of Experimental Psychology: Human Perception and Performance, 41(5), 1260. https://doi.org/10.1037/xhp0000064
Milligan, S., Antúnez, M., Barber, H. A., & Schotter, E. R. (2023). Are eye movements and EEG on the same page?: A coregistration study on parafoveal preview and lexical frequency. Journal of Experimental Psychology: General, 152, 188–210. https://doi.org/10.1037/xge0001278
Munoz, D. P., & Everling, S. (2004). Look away: The anti-saccade task and the voluntary control of eye movement. Nature Reviews Neuroscience, 5(3), 218. https://doi.org/10.1038/nrn1345
Perron, R., Lefebvre, C., Robitaille, N., Brisson, B., Gosselin, F., Arguin, M., & Jolicœur, P. (2009). Attentional and anatomical considerations for the representation of simple stimuli in visual short-term memory: Evidence from human electrophysiology. Psychological Research, 73(2), 222–232. https://doi.org/10.1007/s00426-008-0214-y
Plöchl, M., Ossandón, J. P., & König, P. (2012). Combining EEG and eye tracking: Identification, characterization, and correction of eye movement artifacts in electroencephalographic data. Frontiers in Human Neuroscience, 6, 278.
Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32(1), 3–25. https://doi.org/10.1093/acprof:oso/9780199791217.003.0003
Posner, M. I., Snyder, C. R., & Davidson, B. J. (1980). Attention and the detection of signals. Journal of Experimental Psychology: General, 109(2), 160.
Prinzmetal, W., McCool, C., & Park, S. (2005). Attention: Reaction time and accuracy reveal different mechanisms. Journal of Experimental Psychology: General, 134(1), 73–92. https://doi.org/10.1037/0096-3445.134.1.73
Remington, R. W. (1980). Attention and saccadic eye movements. Journal of Experimental Psychology: Human Perception and Performance, 6(4), 726. https://doi.org/10.1037/0096-1523.6.4.726
Reynolds, J. H., & Heeger, D. J. (2009). The normalization model of attention. Neuron, 61(2), 168–185.
Rizzolatti, G., Riggio, L., Dascola, I., & Umiltá, C. (1987). Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention. Neuropsychologia, 25(1), 31–40.
Rouder, J. N., Speckman, P. L., Sun, D., Morey, R. D., & Iverson, G. (2009). Bayesian t tests for accepting and rejecting the null hypothesis. Psychonomic Bulletin & Review, 16(2), 225–237. https://doi.org/10.3758/PBR.16.2.225
Schneider, W. X., & Deubel, H. (1995). Visual attention and saccadic eye movements: Evidence for obligatory and selective spatial coupling. In J. M. Findlay, R. Walker, & R. W. Kentridge (Eds.), Eye movement research: Mechanisms, processes and applications (pp. 317–324). Elsevier Science.
Schotter, E. R. (2018). Reading ahead by hedging our bets on seeing the future: Eye tracking and electrophysiology evidence for parafoveal lexical processing and saccadic control by partial word recognition. In K. D. Federmeier & D. G. Watson (Eds.), Psychology of learning and motivation (68th ed., pp. 263–298). Academic Press. https://doi.org/10.1016/bs.plm.2018.08.011
Shepherd, M., Findlay, J. M., & Hockey, R. J. (1986). The relationship between eye movements and spatial attention. The Quarterly Journal of Experimental Psychology, 38(3), 475–491.
Talcott, T. N., Gaspelin, N. (2021). Eye movements are not mandatorily preceded by the N2pc component. Psychophysiology, e13821. https://doi.org/10.1111/psyp.13821
Tan, M., & Wyble, B. (2015). Understanding how visual attention locks on to a location: Toward a computational model of the N2pc component. Psychophysiology, 52(2), 199–213. https://doi.org/10.1111/psyp.12324
Thaler, L., Schütz, A. C., Goodale, M. A., & Gegenfurtner, K. R. (2013). What is the best fixation target? The effect of target shape on stability of fixational eye movements. Vision Research, 76, 31–42. https://doi.org/10.1016/j.visres.2012.10.012
Töllner, T., Rangelov, D., & Müller, H. J. (2012). How the speed of motor-response decisions, but not focal-attentional selection, differs as a function of task set and target prevalence. Proceedings of the National Academy of Sciences, 109(28), E1990–E1999. https://doi.org/10.1073/pnas.1206382109
Van der Stigchel, S., & de Vries, J. P. (2015). There is no attentional global effect: Attentional shifts are independent of the saccade endpoint. Journal of Vision, 15(15), 17. https://doi.org/10.1167/15.15.17
van Driel, J., Olivers, C. N. L., & Fahrenfort, J. J. (2021). High-pass filtering artifacts in multivariate classification of neural time series data. Journal of Neuroscience Methods, 352, 109080. https://doi.org/10.1016/j.jneumeth.2021.109080
van Zoest, W., Huber-Huber, C., Weaver, M., & Hickey, C. (2021). Strategic distractor suppression improves selective control in human vision. The Journal of Neuroscience, 41(33), 7120–7135. https://doi.org/10.1523/JNEUROSCI.0553-21.2021
Weaver, M. D., van Zoest, W., & Hickey, C. (2017). A temporal dependency account of attentional inhibition in oculomotor control. NeuroImage, 147, 880–894. https://doi.org/10.1016/j.neuroimage.2016.11.004
Woodman, G. F., & Luck, S. J. (1999). Electrophysiological measurement of rapid shifts of attention during visual search. Nature, 400(6747), 867. https://doi.org/10.1038/23698
Woodman, G. F., & Luck, S. J. (2003). Serial deployment of attention during visual search. Journal of Experimental Psychology: Human Perception and Performance, 29(1), 121–138. https://doi.org/10.1037/0096-1523.29.1.121
Zivony, A., & Eimer, M. (2022). The diachronic account of attentional selectivity. Psychonomic Bulletin & Review, 29, 1118–1142. https://doi.org/10.3758/s13423-021-02023-7
Zivony, A., & Lamy, D. (2018). Contingent attentional engagement: Stimulus- and goal-driven capture have qualitatively different consequences. Psychological Science, 29(12), 1930–1941. https://doi.org/10.1177/0956797618799302
Zivony, A., Allon, A. S., Luria, R., & Lamy, D. (2018). Dissociating between the N2pc and attentional shifting: An attentional blink study. Neuropsychologia, 121, 153–163. https://doi.org/10.1016/j.neuropsychologia.2018.11.003
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This project was made possible by the National Science Foundation Grant BCS-2045624 to Nicholas Gaspelin.
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Talcott, T.N., Kiat, J.E., Luck, S.J. et al. Is covert attention necessary for programming accurate saccades? Evidence from saccade-locked event-related potentials. Atten Percept Psychophys (2023). https://doi.org/10.3758/s13414-023-02775-5
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DOI: https://doi.org/10.3758/s13414-023-02775-5