Effect of distracting faces on visual selective attention in the monkey
Open accessAbstract
In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade velocity and reduced pupillary reflex. Our results indicate that the attraction of attention by emotional faces in the monkey takes a considerable amount of processing time, possibly involving cortical-subcortical interactions. Intranasal application of the hormone oxytocin ameliorated the interfering effects of faces. Together these results provide evidence for slow modulation of attention by emotional distracters, which likely involves oxytocinergic brain circuits.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Intranasal administration of 24 IU OT modulates social behavior in nonhuman primates.
“This dose, administered intranasally, has been shown in nonhuman primates to increase OT levels in cerebrospinal fluid significantly (54) and to modulate social behavior (65), as well as to affect brain activity (66) and phasic activity of the parasympathetic nervous system (67) in humans.”
From Oxytocin under opioid antagonism leads to supralinear enhancement of social attention (2017) · cites this paper as [65]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Brainard, D. H. (1997) · Spatial Vision · doi:10.1163/156856897x00357 · Cited by 19,308 · see citing works
Egeth, H. E., & Kahneman, D. J. (1975) · The American Journal of Psychology · doi:10.2307/1421603 · Cited by 6,976 · see citing works
Simultaneous Statistical Inference
Miller, R. G. (1981) · Springer series in statistics · doi:10.1007/978-1-4613-8122-8 · Cited by 5,608 · see citing works
Ratcliff, R. (1978) · Psychological Review · doi:10.1037/0033-295x.85.2.59 · Cited by 4,513 · see citing works
Procedures for Detecting Outlying Observations in Samples
Grubbs, F. E. (1969) · Technometrics · doi:10.1080/00401706.1969.10490657 · Cited by 4,105 · see citing works
The Neurology of Eye Movements
Leigh, R. J., & Zee, D. S. (2015) · Oxford University Press eBooks · doi:10.1093/med/9780199969289.001.0001 · Cited by 3,829 · see citing works
(1996) · Cited by 3,692 · see citing works
The aligned rank transform for nonparametric factorial analyses using only anova procedures
Wobbrock, J. O., Findlater, L., Gergle, D., & Higgins, J. J. (2011) · CHI Conference on Human Factors in Computing Systems · doi:10.1145/1978942.1978963 · Cited by 3,005 · see citing works
Emotion drives attention: Detecting the snake in the grass.
Öhman, A., Flykt, A., & Esteves, F. (2001) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.130.3.466 · Cited by 2,542 · see citing works
Emotion drives attention: Detecting the snake in the grass.
Öhman, A., Flykt, A., & Esteves, F. G. (2001) · Journal of Experimental Psychology General · doi:10.1037//0096-3445.130.3.466 · Cited by 2,527 · see citing works
Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00411.1998 · Cited by 2,205 · see citing works
How brains beware: neural mechanisms of emotional attention
Vuilleumier, P. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.10.011 · Cited by 2,162 · see citing works
The pupil as a measure of emotional arousal and autonomic activation
Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00654.x · Cited by 1,919 · see citing works
Pessoa, L., & Adolphs, R. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2920 · Cited by 1,794 · see citing works
Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review
Cisler, J. M., & Koster, E. H. W. (2010) · Clinical Psychology Review · doi:10.1016/j.cpr.2009.11.003 · Cited by 1,753 · see citing works
Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans
Kirsch, P., Esslinger, C., Chen, Q., Mier, D., Lis, S., Siddhanti, S., Gruppe, H., Mattay, V. S., Gallhofer, B., & Meyer-Lindenberg, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3984-05.2005 · Cited by 1,639 · see citing works
Top-down versus bottom-up attentional control: a failed theoretical dichotomy
Awh, E., Belopolsky, A. V., & Theeuwes, J. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.06.010 · Cited by 1,557 · see citing works
The face in the crowd revisited: A threat advantage with schematic stimuli.
Öhman, A., Lundqvist, D., & Esteves, F. (2001) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.80.3.381 · Cited by 1,366 · see citing works
A subcortical pathway to the right amygdala mediating “unseen” fear
Morris, J. S., Öhman, A., & Dolan, R. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1680 · Cited by 1,349 · see citing works
Speed-accuracy tradeoff and information processing dynamics
Wickelgren, W. A. (1977) · Acta Psychologica · doi:10.1016/0001-6918(77)90012-9 · Cited by 1,304 · see citing works
Oxytocin improves “mind-reading” in humans
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.015 · Cited by 1,298 · see citing works
A neuromodulatory role for the human amygdala in processing emotional facial expressions
Morris, J. (1998) · Brain · doi:10.1093/brain/121.1.47 · Cited by 1,291 · see citing works
Affective Discrimination of Stimuli That Cannot Be Recognized
Kunst-Wilson, W. R., & Zajonc, R. B. (1980) · Science · doi:10.1126/science.7352271 · Cited by 1,213 · see citing works
Neural processing of emotional faces requires attention
Pessoa, L., McKenna, M., Gutierrez, E., & Ungerleider, L. G. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172403899 · Cited by 1,155 · see citing works
Eye tracking of attention in the affective disorders: a meta-analytic review and synthesis
Armstrong, T., & Olatunji, B. O. (2012) · Clinical Psychology Review · doi:10.1016/j.cpr.2012.09.004 · Cited by 1,049 · see citing works
The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox
Cornelissen, F. W., Peters, E. M., & Palmer, J. C. (2002) · Behavior Research Methods, Instruments, & Computers · doi:10.3758/bf03195489 · Cited by 1,049 · see citing works
Evoked axonal oxytocin release in the central amygdala attenuates fear response
Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., Osten, P., Schwarz, M. K., Seeburg, P. H., Stoop, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.030 · Cited by 1,049 · see citing works
Neural bases of the non-conscious perception of emotional signals
Tamietto, M., & de Gelder, B. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2889 · Cited by 1,042 · see citing works
Proceedings of the Conference on Human Factors in Computing Systems
Moore, J. E. (1989) · ACM eBooks · Cited by 960 · see citing works
Attentional bias for threat: evidence for delayed disengagement from emotional faces
Fox, E., Russo, R., & Dutton, K. (2002) · Cognition & Emotion · doi:10.1080/02699930143000527 · Cited by 954 · see citing works
Oxytocin increases gaze to the eye region of human faces
Guastella, A. J., Mitchell, P. B., & Dadds, M. R. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.06.026 · Cited by 798 · see citing works
An EZ-diffusion model for response time and accuracy
Wagenmakers, E., van der Maas, H. L. J., & Grasman, R. P. P. P. (2007) · Psychonomic Bulletin & Review · doi:10.3758/bf03194023 · Cited by 544 · see citing works
Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice
Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., & Landgraf, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.03.003 · Cited by 511 · see citing works
Neuromodulation by Oxytocin and Vasopressin
Stoop, R. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.025 · Cited by 506 · see citing works
Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans
Gamer, M., Zurowski, B., & Büchel, C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000985107 · Cited by 487 · cited 1× · see citing works
“In humans (57) and in monkeys (58), OT has been shown to reduce responses to negative facial expressions not only in the amygdala, but also in inferior temporal cortex and prefrontal cortex (58).”
BackgroundUnseen facial and bodily expressions trigger fast emotional reactions
Tamietto, M., Castelli, L., Vighetti, S., Perozzo, P., Geminiani, G., Weiskrantz, L., & de Gelder, B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908994106 · Cited by 385 · see citing works
Langton, S., Law, A. S., Burton, A. M., & Schweinberger, S. R. (2007) · Cognition · doi:10.1016/j.cognition.2007.07.012 · Cited by 348 · see citing works
Mogg, K., & Bradley, B. P. (1999) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(98)00158-2 · Cited by 336 · see citing works
The Role of Perceptual Load in Processing Distractor Faces
Lavie, N., Ro, T., & Russell, C. (2003) · Psychological Science · doi:10.1111/1467-9280.03453 · Cited by 313 · see citing works
A comparative view of face perception.
Leopold, D. A., & Rhodes, G. (2010) · Journal of Comparative Psychology · doi:10.1037/a0019460 · Cited by 311 · see citing works
Negative facial expression captures attention and disrupts performance
Eastwood, J. D., Smilek, D., & Merikle, P. M. (2003) · Perception & Psychophysics · doi:10.3758/bf03194566 · Cited by 274 · see citing works
Chang, S. W. C., Barter, J. W., Ebitz, R. B., Watson, K. K., & Platt, M. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114621109 · Cited by 252 · cited 2× · see citing works
“The latency of our behavioral effect of OT (∼70 min) is in line with previously reported behavioral effects (peaking at 110 min) using the same nebulization method (50).”
BackgroundResultThe Neurology of Eye Movements
Sanders, M. D. (1984) · British Journal of Ophthalmology · doi:10.1136/bjo.68.5.370-b · Cited by 229 · see citing works
Saccadic velocity as an arousal index in naturalistic tasks
Stasi, L. L. D., Catena, A., Cañas, J. J., Macknik, S. L., & Martínez‐Conde, S. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.011 · Cited by 211 · see citing works
Intact rapid detection of fearful faces in the absence of the amygdala
Tsuchiya, N., Moradi, F., Felsen, C. N., Yamazaki, M., & Adolphs, R. (2009) · Nature Neuroscience · doi:10.1038/nn.2380 · Cited by 210 · see citing works
Tracking the allocation of attention using human pupillary oscillations
Naber, M., Alvarez, G. A., & Nakayama, K. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00919 · Cited by 188 · see citing works
Attentional capture by irrelevant emotional distractor faces.
Hodsoll, S., Viding, E. M., & Nilli Lavie, C. (2011) · Emotion · doi:10.1037/a0022771 · Cited by 165 · see citing works
The evolution of face processing in primates
Parr, L. A. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0358 · Cited by 163 · see citing works
Threat Prompts Defensive Brain Responses Independently of Attentional Control
Pichon, S., de Gelder, B., & Grèzes, J. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr060 · Cited by 152 · see citing works
Oxytocin blunts social vigilance in the rhesus macaque
Ebitz, R. B., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305230110 · Cited by 132 · see citing works
Intranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions
Parr, L. A., Modi, M., Siebert, E., & Young, L. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.011 · Cited by 124 · see citing works
Dynamics of emotional effects on spatial attention in the human visual cortex
Pourtois, G., & Vuilleumier, P. O. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)56004-2 · Cited by 123 · see citing works
Humans and Macaques Employ Similar Face-Processing Strategies
Dahl, C. D., Wallraven, C., Bülthoff, H., & Logothetis, N. K. (2009) · Current Biology · doi:10.1016/j.cub.2009.01.061 · Cited by 121 · see citing works
Can new objects override attentional control settings?
Folk, C. L., & Remington, R. W. (1999) · Perception & Psychophysics · doi:10.3758/bf03205541 · Cited by 113 · see citing works
Attentional Capture Does Not Depend on Feature Similarity, but on Target-Nontarget Relations
Becker, S. I., Folk, C. L., & Remington, R. W. (2013) · Psychological Science · doi:10.1177/0956797612458528 · Cited by 103 · see citing works
Does emotion processing require attention? The effects of fear conditioning and perceptual load
Yates, A., Ashwin, C., & Fox, E. (2010) · Emotion · doi:10.1037/a0020325 · Cited by 88 · see citing works
Affiliative and submissive communication in rhesus macaques
Maestripieri, D., & Wallen, K. (1997) · Primates · doi:10.1007/bf02382003 · Cited by 85 · see citing works
Oxytocin enhances attention to the eye region in rhesus monkeys
Dal Monte, O., Noble, P. L., Costa, V. D., & Averbeck, B. B. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00041 · Cited by 80 · see citing works
Bitsios, P., Szabadi, E., & Bradshaw, C. M. (1996) · Journal of Psychopharmacology · doi:10.1177/026988119601000404 · Cited by 79 · see citing works
Sustained Preferential Processing of Social Threat Cues: Bias without Competition?
Wieser, M. J., McTeague, L. M., & Keil, A. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21566 · Cited by 75 · see citing works
Oxytocin modulates fMRI responses to facial expression in macaques
Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. B., & Ungerleider, L. G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508097112 · Cited by 65 · see citing works
Task-irrelevant angry faces capture attention in visual search while modulated by resources.
Huang, S.-L., Chang, Y.-C., & Chen, Y.-J. (2011) · Emotion · doi:10.1037/a0022763 · Cited by 53 · see citing works
PUPILLARY DILATATION INDUCED BY STIMULATION OF AMYGDALOID NUCLEI
Koikegami, H., & Yoshida, K. (1953) · Psychiatry and Clinical Neurosciences · doi:10.1111/j.1440-1819.1953.tb00600.x · Cited by 50 · see citing works
Perceptual load modulates attentional capture by abrupt onsets
Cosman, J. D., & Vecera, S. P. (2009) · Psychonomic Bulletin & Review · doi:10.3758/pbr.16.2.404 · Cited by 49 · see citing works
Automatic relevance detection in the absence of a functional amygdala
Bach, D. R., Talmi, D., Hurlemann, R., Patin, A., & Dolan, R. J. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.02.032 · Cited by 45 · see citing works
Oculomotor Guidance and Capture by Irrelevant Faces
Devue, C., Belopolsky, A. V., & Theeuwes, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034598 · Cited by 40 · see citing works
Oxytocin enhances the inhibitory effects of diazepam in the rat central medial amygdala
Viviani, D., Terrettaz, T., Magara, F., & Stoop, R. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.039 · Cited by 40 · see citing works
Attentional capture by emotional stimuli is preserved in patients with amygdala lesions
Piech, R. M., McHugo, M., Smith, S. D., Dukic, M. S., Meer, J. V. D., Abou-Khalil, B. W., Most, S. B., & Zald, D. H. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.08.004 · Cited by 37 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Oxytocin modulates fMRI responses to facial expression in macaques
Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. B., & Ungerleider, L. G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508097112 · Cited by 65 · see citing works
Oxytocin reduces amygdala responses during threat approach
Radke, S., Volman, I., Kokal, I., Roelofs, K., de Bruijn, E. R. A., & Toni, I. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.02.028 · Cited by 67 · see citing works
Oxytocin under opioid antagonism leads to supralinear enhancement of social attention
Dal Monte, O., Piva, M., Anderson, K. M., Tringides, M., Holmes, A. J., & Chang, S. W. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702725114 · Cited by 55 · see citing works
An integrated framework for the role of oxytocin in multistage social decision‐making
Piva, M., & Chang, S. W. C. (2018) · American Journal of Primatology · doi:10.1002/ajp.22735 · Cited by 38 · see citing works
“Finally, as mentioned in the previous section, work across humans and nonhuman primates indicates that the effects of OT are likely valencespecific (Chang et al., 2012; Ebitz et al., 2013; Evans et al., 2010; Landman et al., 2014; Marsh et al., 2010; Unkelbach et al., 2008).”
BackgroundInfluentialEffects of chronic oxytocin on attention to dynamic facial expressions in infant macaques
Parr, L. A., Brooks, J. M., Jonesteller, T., Moss, S., Jordano, J. O., & Heitz, T. R. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.08.028 · Cited by 23 · see citing works
- Authors
- Landman, R., Sharma, J., Sur, M., & Desimone, R.
- Affiliations
- McGovern Institute for Brain Research (US)
- Harvard University (US)
- Massachusetts Institute of Technology (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-12-03
- Volume
- 111
- Issue
- 50
- Pages
- 18037-18042
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4273369
- OpenAlex
- W2024068621
- Cited by
- 43
- References
- 68
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 1 · 2022: 6 · 2021: 2 · 2020: 1 · 2019: 5 · 2018: 6 · 2017: 6 · 2016: 5 · 2015: 3 · 2012: 1
- FWCI
- 2.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- HHS | National Institutes of Health (NIH) (EY017292)
- Simons Foundation (SF) (none)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Keywords
- visual selective attention, emotional face processing, attentional capture, distractor interference, covert attention, macaque, saccade velocity, pupillary reflex, oxytocin, attentional modulation, social attention, spatial proximity
- MeSH terms
- Analysis of Variance, Animals, Attention, Emotions, Eye Movements, Face, Facial Expression, Macaca mulatta, Pattern Recognition, Visual, Photic Stimulation, Psychomotor Performance
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review