Abstract
Manual response times to peripherally presented targets have been reported to be greater in the presence of task-irrelevant pictorial faces at fixation which establish an eye contact with the observer. This effect is interpreted as evidence that direct-gaze faces hold attention. In three experiments, we investigated whether this attention-holding effect is also reflected in saccadic response times. Participants were asked to make a saccade towards a symbolic target that could appear rightwards or leftwards, in the presence of a task-irrelevant centrally placed face with either direct gaze or closed eyes. Unexpectedly, saccadic response times did not show any consistent response pattern as a function of whether the faces were presented with direct gaze vs. closed eyes. Interestingly, saccadic peak velocities were found to be lower in the presence of faces with direct gaze rather than closed eyes (Experiment 1). This effect emerged even in the presence of non-human primate faces (Experiment 2), and no differences between direct gaze and closed eyes emerged when the faces were presented inverted rather than upright (Experiment 3). Overall, these findings suggest that eye contact can have an impact on the saccadic generation system.
Similar content being viewed by others
Notes
For completeness, Bonferroni-corrected t tests confirmed that no significant differences emerged between open vs. closed eyes at each SOA (ts < 1.2, ps > .755). Bayes Factor scores (BF10) were also computed through JASP software (JASP Team 2017), in order to provide further support to this pattern. The results indicated that H1 (a difference between open and closed eyes) was never preferable over H0 (no difference between open and closed eyes) in any of these comparisons (all BF10 < 1).
For completeness, we report here that the main effect of SOA approached significance, F(1, 24) = 4.081, p = .055, η p 2 = .145, in line with a foreperiod effect.
Even if the eyes × SOA × species interaction was non-significant, F(1, 24) = 2.306, p = .142, n 2 p = .088, for completeness Bonferroni-corrected t tests were also carried out. The only significant results emerged at the 100-ms SOA, indicating that peak velocity was smaller in the presence of a face with open eyes than closed eyes, for both humans, t(24) = 4.282, p = .001, d = .858, BF10 = 116.893, and non-human primate faces, t(24) = 3.057, p = .02, d = .611, BF10 = 8.042. No other significant results emerged (ts < 1, ps > .999, BF10s < 1; see also Fig. 3).
For completeness, t tests were performed between open and closed eyes for each face orientation and at each SOA. No significant results emerged (ts < 1.049, ps > .304, BF10s < 1). Because we hypothesized a null effect in the case of inverted faces, no Bonferroni correction was applied as this would have resulted in an increased likelihood of detecting exactly such null effect. In so doing, we followed a more conservative approach.
For completeness, we report here that the main effect of eyes approached significance, F(1, 25) = 3.374, p = .078, \(\eta^{2}_{p}\) = .119, suggesting a trend towards lower velocities in the presence of faces with open eyes than closed eyes. The main effect of face orientation also approached significance, F(1, 25) = 3.037, p = .094, \(\eta^{2}_{p}\) = .108, suggesting a trend towards lower velocities in the presence of upright faces than inverted faces.
Even if the eyes × SOA × face orientation interaction was non-significant, F(1, 25) = 2.161, p = .154, \(\eta^{2}_{p}\) = .080, for completeness t tests were conducted. The only significant result emerged at the 100-ms SOA for upright faces, t(25) = 2.451, p = .022, d = .481, BF10 = 2.490, indicating that peak velocity was smaller in the presence of a face with open eyes than closed eyes. No other comparisons were significant (ts < 1, ps > .475, BF10s < 1; see also Fig. 4).
References
Bayliss AP, Schuch S, Tipper SP (2010) Gaze cueing elicited by emotional faces is influenced by affective context. Vis Cogn 18:1214–1232. doi:10.1080/13506285.2010.484657
Böckler A, van der Wel RP, Welsh TN (2014) Catching eyes: effects of social and nonsocial cues on attention capture. Psychol Sci 25:720–727. doi:10.1177/0956797613516147
Böckler A, van der Wel RP, Welsh TN (2015) Eyes only? Perceiving eye contact is neither sufficient nor necessary for attentional capture by face direction. Acta Psychol 160:134–140. doi:10.1016/j.actpsy.2015.07.009
Carraro L, Dalmaso M, Castelli L, Galfano G (2015) The politics of attention contextualized: gaze but not arrow cuing of attention is moderated by political temperament. Cogn Process 16:309–314. doi:10.1007/s10339-015-0661-5
Carraro L, Dalmaso M, Castelli L, Galfano G, Bobbio A, Mantovani G (2017) The appeal of the devil’s eye: social evaluation affects social attention. Cogn Process 18:97–103. doi:10.1007/s10339-016-0785-2
Ciardo F, Marino BFM, Actis-Grosso R, Rossetti A, Ricciardelli P (2014) Face age modulates gaze following in young adults. Sci Rep 4:4746. doi:10.1038/srep04746
Cole GG, Skarratt PA, Kuhn G (2016) Real person interaction in visual attention research. Eur Psychol 21:141–149. doi:10.1027/1016-9040/a000243
Conty L, Tijus C, Hugueville L, Coelho E, George N (2006) Searching for asymmetries in the detection of gaze contact versus averted gaze under different head views: a behavioural study. Spat Vis 19:529–545. doi:10.1163/156856806779194026
Conty L, George N, Hietanen JK (2016) Watching Eyes effects: when others meet the self. Consc Cogn 45:184–197. doi:10.1016/j.concog.2016.08.016
Conway CA, Jones BC, DeBruine LM, Little AC, Sahraie A (2008) Transient pupil constrictions to faces are sensitive to orientation and species. J Vis 8:1–11. doi:10.1167/8.3.17
Cooper RM, Law AS, Langton SR (2013) Looking back at the stare-in-the-crowd effect: staring eyes do not capture attention in visual search. J Vis 13:1–10. doi:10.1167/13.6.10
Dalmaso M, Pavan G, Castelli L, Galfano G (2012) Social status gates social attention in humans. Biol Lett 8:450–452. doi:10.1098/rsbl.2011.0881
Dalmaso M, Galfano G, Coricelli C, Castelli L (2014) Temporal dynamics underlying the modulation of social status on social attention. PLoS One 9:e93139. doi:10.1371/journal.pone.0093139
Dalmaso M, Galfano G, Castelli L (2015) The impact of same- and other-race gaze distractors on the control of saccadic eye movements. Perception 44:1020–1028. doi:10.1177/0301006615594936
Dalmaso M, Edwards SG, Bayliss AP (2016) Re-encountering individuals who previously engaged in joint attention modulates subsequent gaze cueing. J Exp Psychol Learn Mem Cogn 42:271–284. doi:10.1037/xlm0000159
Dalmaso M, Castelli L, Scatturin P, Galfano G (2017) Trajectories of social vision: Eye contact increases saccadic curvature. Vis Cogn. doi: 10.1080/13506285.2017.1290727 (in press)
de Haan M, Pascalis O, Johnson MH (2002) Specialization of neural mechanisms underlying face recognition in human infants. J Cogn Neurosci 14:199–209. doi:10.1162/089892902317236849
de Hamilton AFC (2016) Gazing at me: the importance of social meaning in understanding direct-gaze cues. Phil Trans R Soc B 371:20150080. doi:10.1098/rstb.2015.0080
Di Stasi LL, Catena A, Cañas JJ, Macknik SL, Martinez-Conde S (2013) Saccadic velocity as an arousal index in naturalistic tasks. Neurosci Biobehav Rev 37:968–975. doi:10.1016/j.neubiorev.2013.03.011
Dodd MD, Hibbing JR, Smith KB (2011) The politics of attention: gaze cuing effects are moderated by political temperament. Atten Percept Psychophys 73:24–29. doi:10.3758/s13414-010-0001-x
Doi H, Shinohara K (2013) Task-irrelevant direct gaze facilitates visual search for deviant facial expression. Vis Cogn 21:72–98. doi:10.1080/13506285.2013.779350
Driver J, Davis G, Ricciardelli P, Kidd P, Maxwell E, Baron-Cohen S (1999) Gaze perception triggers reflexive visuospatial orienting. Vis Cogn 6:509–540. doi:10.1080/135062899394920
Edelman JA, Valenzuela N, Barton JJ (2006) Antisaccade velocity, but not latency, results from a lack of saccade visual guidance. Vis Res 46:1411–1421. doi:10.1016/j.visres.2005.09.013
Edwards SG, Stephenson L, Dalmaso M, Bayliss AP (2015) Social orienting in gaze leading: a mechanism for shared attention. Proc R Soc Lond B Biol Sci 282:20151141. doi:10.1098/rspb.2015.1141
Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604. doi:10.1016/S0149-7634(00)00025-7
Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20:387–400
Farroni T, Csibra G, Simion F, Johnson MH (2002) Eye contact detection in humans from birth. Proc Natl Acad Sci USA 99:9602–9605. doi:10.1073/pnas.152159999
Farroni T, Massaccesi S, Pividori D, Johnson MH (2004) Gaze following in newborns. Infancy 5:39–60. doi:10.1207/s15327078in0501_2
Fimm B, Blankenheim A (2016) Effect of sleep deprivation and low arousal on eye movements and spatial attention. Neuropsychologia 92:115–128. doi:10.1016/j.neuropsychologia.2016.03.021
Framorando D, George N, Kerzel D, Burra N (2017) Straight gaze facilitates face processing but does not cause involuntary attentional capture. Vis Cogn 24:381–391. doi:10.1080/13506285.2017.1285840
Friesen CK, Kingstone A (1998) The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychon Bull Rev 5:490–495. doi:10.3758/BF03208827
Frischen A, Bayliss AP, Tipper SP (2007) Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychol Bull 133:694–724. doi:10.1037/0033-2909.133.4.694
Galfano G, Dalmaso M, Marzoli D, Pavan G, Coricelli C, Castelli L (2012) Eye gaze cannot be ignored (but neither can arrows). Q J Exp Psychol 65:1895–1910. doi:10.1080/17470218.2012.663765
Gallup AC, Chong A, Couzin ID (2012) The directional flow of visual information transfer between pedestrians. Biol Lett 8:520–522. doi:10.1098/rsbl.2012.0160
Gilchrist I (2011) Saccades. In: Liversedge S, Gilchrist I, Everling S (eds) The Oxford handbook of eye movements. Oxford University Press, Oxford, pp 85–94
Hattori Y, Kano F, Tomonaga M (2010) Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: a comparative eye-tracking study. Biol Lett 6:610–613. doi:10.1098/rsbl.2010.0120
Hietanen JK, Myllyneva A, Helminen TM, Lyyra P (2016) The effects of genuine eye contact on visuospatial and selective attention. J Exp Psychol Gen 145:1102–1106. doi:10.1037/xge0000199
Hikosaka O, Nakamura K, Nakahara H (2006) Basal ganglia orient eyes to reward. J Neurophysiol 95:567–584. doi:10.1152/jn.00458.2005
Jarosz AF, Wiley J (2014) What are the odds? A practical guide to computing and reporting Bayes factors. J Probl Solving 7:2–9. doi:10.7771/1932-6246.1167
JASP Team (2017). JASP (Version 0.8.1.2) [Computer software]
Johnson MH, Senju A, Tomalski P (2015) The two-process theory of face processing: modifications based on two decades of data from infants and adults. Neurosci Biobehav Rev 50:169–179. doi:10.1016/j.neubiorev.2014.10.009
Jones BC, DeBruine LM, Main JC, Little AC, Welling LL, Feinberg DR, Tiddeman BP (2010) Facial cues of dominance modulate the short-term gaze-cuing effect in human observers. Proc R Soc Lond B Biol Sci 277:617–624. doi:10.1098/rspb.2009.1575
Kampe KK, Frith CD, Dolan RJ, Frith U (2001) Reward value of attractiveness and gaze. Nature 413:589. doi:10.1038/35098149
Kano F, Call J (2014) Cross-species variation in gaze following and conspecific preference among great apes, human infants and adults. Anim Behav 91:137–150. doi:10.1016/j.anbehav.2014.03.011
Kristjánsson A (2011) The intriguing interactive relationship between visual attention and saccadic eye movements. In: Liversedge SP, Gilchrist ID, Everling S (eds) The Oxford handbook of eye movements. Oxford University Press, Oxford, pp 455–470
Kuhn G, Benson V (2007) The influence of eye-gaze and arrow pointing distractor cues on voluntary eye movements. Atten Percept Psychophys 69:966–971. doi:10.3758/BF03193934
Kuhn G, Pagano A, Maani S, Bunce D (2015) Age-related decline in the reflexive component of overt gaze following. Q J Exp Psychol 68:1073–1081. doi:10.1080/17470218.2014.975257
Lachat F, Conty L, Hugueville L, George N (2012) Gaze cueing effect in a face-to-face situation. J Nonverbal Behav 36:177–190. doi:10.1007/s10919-012-0133-x
Lee C, Rohrer WH, Sparks DL (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332:357–360. doi:10.1038/332357a0
Macrae CN, Hood BM, Milne AB, Rowe AC, Mason MF (2002) Are you looking at me? Eye gaze and person perception. Psychol Sci 13:460–464. doi:10.1111/1467-9280.00481
Mares I, Smith ML, Johnson MH, Senju A (2016) Direct gaze facilitates rapid orienting to faces: evidence from express saccades and saccadic potentials. Biol Psychol 121:84–90. doi:10.1016/j.biopsycho.2016.10.003
Mason MF, Hood BM, Macrae CN (2004) Look into my eyes: gaze direction and person memory. Memory 12:637–643. doi:10.1080/09658210344000152
Maurer D, Le Grand R, Mondloch CJ (2002) The many faces of configural processing. Trends Cogn Sci 6:255–260. doi:10.1016/S1364-6613(02)01903-4
Mondloch CJ, Maurer D, Ahola S (2006) Becoming a face expert. Psychol Sci 17:930–934. doi:10.1098/rstb.1992.0012
Montagnini A, Chelazzi L (2005) The urgency to look: prompt saccades to the benefit of perception. Vis Res 45:3391–3401. doi:10.1016/j.visres.2005.07.013
Niemi P, Näätänen R (1981) Foreperiod and simple reaction time. Psychol Bull 89:133. doi:10.1037/0033-2909.89.1.133
Palanica A, Itier RJ (2011) Searching for a perceived gaze direction using eye tracking. J Vis 11:1–13. doi:10.1167/11.2.19
Pascalis O, de Haan M, Nelson CA (2002) Is face processing species specific during the first year of life? Science 296:1321–1323. doi:10.1126/science.1070223
Pavan G, Dalmaso M, Galfano G, Castelli L (2011) Racial group membership is associated to gaze-mediated orienting in Italy. PLoS One 6:e25608. doi:10.1371/journal.pone.0025608
Pfeiffer UJ, Schilbach L, Jording M, Timmermans B, Bente G, Vogeley K (2012) Eyes on the mind: investigating the influence of gaze dynamics on the perception of others in real-time social interaction. Front Psychol 3:337. doi:10.3389/fpsyg.2012.00537
Pfeiffer UJ, Vogeley K, Schilbach L (2013) From gaze cueing to dual eye-tracking: novel approaches to investigate the neural correlates of gaze in social interaction. Neurosci Biobehav Rev 37:2516–2528. doi:10.1016/j.neubiorev.2013.07.017
Porciello G, Liuzza MT, Minio-Paluello I, Caprara GV, Aglioti SM (2016) Fortunes and misfortunes of political leaders reflected in the eyes of their electors. Exp Brain Res 234:733–740. doi:10.1007/s00221-015-4496-1
Quaia C, Lefèvre P, Optican LM (1999) Model of the control of saccades by superior colliculus and cerebellum. J Neurophys 82:999–1018
Ramchandran RS, Manoach DS, Cherkasova MV, Lindgren KA, Goff DC, Barton JJ (2004) The relationship of saccadic peak velocity to latency: evidence for a new prosaccadic abnormality in schizophrenia. Exp Brain Res 159:99–107. doi:10.1007/s00221-004-1940-z
Ricciardelli P, Bricolo E, Aglioti SM, Chelazzi L (2002) My eyes want to look where your eyes are looking: exploring the tendency to imitate another individuals’ gaze. NeuroReport 13:2259–2264. doi:10.1097/01.wnr.0000044227.79663.2e
Risko EF, Richardson DC, Kingstone A (2016) Breaking the fourth wall of cognitive science: real-world social attention and the dual function of gaze. Curr Dir Psychol Sci 25:70–74. doi:10.1177/0963721415617806
Segraves MA, Park K (1993) The relationship of monkey frontal eye field activity to saccade dynamics. J Neurophysiol 69:1880–1889
Senju A, Hasegawa T (2005) Direct gaze captures visuospatial attention. Vis Cogn 12:127–144. doi:10.1080/13506280444000157
Senju A, Johnson MH (2009) The eye contact effect: mechanisms and development. Trends Cogn Sci 13:127–134. doi:10.1016/j.tics.2008.11.009
Senju A, Hasegawa T, Tojo Y (2005) Does perceived direct gaze boost detection in adults and children with and without autism? The stare-in-the-crowd effect revisited. Vis Cogn 12:1474–1496. doi:10.1080/13506280444000797
Senju A, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H (2008) Is anyone looking at me? direct gaze detection in children with and without autism. Brain Cogn 67:127–139. doi:10.1016/j.bandc.2007.12.001
Sessa P, Dalmaso M (2016) Race perception and gaze direction differently impair visual working memory for faces: an event-related potential study. Soc Neurosci 11:97–107. doi:10.1080/17470919.2015.1040556
Shepherd SV (2010) Following gaze: gaze-following behavior as a window into social cognition. Front Integr Neurosci 4:5. doi:10.3389/fnint.2010.00005
Sommer MA, Tehovnik EJ (1997) Reversible inactivation of macaque frontal eye field. Exp Brain Res 116:229–249. doi:10.1007/PL00005752
Takikawa Y, Kawagoe R, Itoh H, Nakahara H, Hikosaka O (2002) Modulation of saccadic eye movements by predicted reward outcome. Exp Brain Res 142:284–291. doi:10.1007/s00221-001-0928-1
Ueda H, Takahashi K, Watanabe K (2014) Effects of direct and averted gaze on the subsequent saccadic response. Atten Percept Psychophys 76:1085–1092. doi:10.3758/s13414-014-0660-0
Van der Stigchel S (2010) Recent advances in the study of saccade trajectory deviations. Vis Res 50:1619–1627. doi:10.1016/j.visres.2010.05.028
Vernetti A, Smith TJ, Senju A (2017) Gaze-contingent reinforcement learning reveals incentive value of social signals in young children and adults. Proc R Soc Lond B Biol Sci 284:20162747. doi:10.1098/rspb.2016.2747
von Grünau M, Anston C (1995) The detection of gaze direction: a stare-in-the-crowd effect. Perception 24:1297–1313. doi:10.1068/p241297
Wagenmakers EJ (2007) A practical solution to the pervasive problems of p values. Psychon Bull Rev 14:779–804. doi:10.1007/s10339-015-0661-5
Willenbockel V, Sadr J, Fiset D, Horne GO, Gosselin F, Tanaka JW (2010) Controlling low-level image properties: the SHINE toolbox. Behav Res Methods 42:671–684. doi:10.3758/brm.42.3.671
Xu-Wilson M, Zee DS, Shadmehr R (2009) The intrinsic value of visual information affects saccade velocities. Exp Brain Res 196:475–481. doi:10.1007/s00221-009-1879-1
Yokoyama T, Ishibashi K, Hongoh Y, Kita S (2011) Attentional capture by change in direct gaze. Perception 40:785–797. doi:10.1068/p7003
Acknowledgements
The authors are grateful to Marta Pugliese for her assistance during data collection and to two anonymous reviewers for their helpful comments on a previous version of this paper.
This study was funded by the Italian Ministry of Education, University, and Research (Futuro in Ricerca 2012, grant number RBFR12F0BD to Giovanni Galfano) and by the University of Padova (Bando Giovani Ricercatori 2015 “Assegno Senior”, grant number GRIC15QDDH to Mario Dalmaso).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Dalmaso, M., Castelli, L. & Galfano, G. Attention holding elicited by direct-gaze faces is reflected in saccadic peak velocity. Exp Brain Res 235, 3319–3332 (2017). https://doi.org/10.1007/s00221-017-5059-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-017-5059-4