Neural processing of imminent collision in humans
Open accessAbstract
Detecting a looming object and its imminent collision is imperative to survival. For most humans, it is a fundamental aspect of daily activities such as driving, road crossing and participating in sport, yet little is known about how the brain both detects and responds to such stimuli. Here we use functional magnetic resonance imaging to assess neural response to looming stimuli in comparison with receding stimuli and motion-controlled static stimuli. We demonstrate for the first time that, in the human, the superior colliculus and the pulvinar nucleus of the thalamus respond to looming in addition to cortical regions associated with motor preparation. We also implicate the anterior insula in making timing computations for collision events.
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Preferential activation in response to looming stimuli has been observed in the pulvinar, putatively located in the medial pulvinar.
“In line with these findings, preferential activation in response to looming stimuli has been observed in the pulvinar, and putatively located in the medial pulvinar (Billington et al. 2011; Huang et al. 2018).”
From Neuroanatomical correlates of peripersonal space: bridging the gap between perception, action, emotion and social cognition (2024) · cites this paper as Billington et al. 2011
The superior colliculus responds to looming visual stimuli, which have to be recognized as immediately salient for the individual.
“In line with this role, SC also has been shown to respond to looming visual stimuli, which have to be recognized as immediately salient for the individual (Billington et al. 2011; Vieira et al. 2020).”
From Neuroanatomical correlates of peripersonal space: bridging the gap between perception, action, emotion and social cognition (2024) · cites this paper as Billington et al. 2011
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Cites
How do you feel — now? The anterior insula and human awareness
(Bud) Craig, A. D. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2555 · Cited by 6,657 · cited 1× · see citing works
“…in making duration judgments (Livesey et al., 2007), error detection (Klein et al., 2007) and interoceptive awareness on a variety of tasks (Craig, 2009). y Our current findings, taken together this research suggests that this cortical region may be particularly attuned to making timing…”
A Theory of Visual Control of Braking Based on Information about Time-to-Collision
Lee, D. N. (1976) · Perception · doi:10.1068/p050437 · Cited by 2,094 · see citing works
Jeurgen, K., Assheuer, J., & Paxinos, G. (1997) · Medical Entomology and Zoology · Cited by 1,403 · see citing works
The basal ganglia: a vertebrate solution to the selection problem?
Redgrave, P., Prescott, T. J., & Gurney, K. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00319-4 · Cited by 1,199 · see citing works
VISUALLY CONTROLLED LOCOMOTION AND VISUAL ORIENTATION IN ANIMALS*
Gibson, J. J. (1958) · British Journal of Psychology · doi:10.1111/j.2044-8295.1958.tb00656.x · Cited by 806 · see citing works
Human parietal cortex in action
Culham, J. C., & Valyear, K. F. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.03.005 · Cited by 654 · see citing works
Comparative Neurology of the Optic Tectum
(1984) · doi:10.1007/978-1-4899-5376-6 · Cited by 478 · see citing works
Persistent Fear Responses in Rhesus Monkeys to the Optical Stimulus of "Looming"
Schiff, W., Caviness, J. A., & Gibson, J. J. (1962) · Science · doi:10.1126/science.136.3520.982 · Cited by 411 · see citing works
Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons
Sun, H., & Frost, B. J. (1998) · Nature Neuroscience · doi:10.1038/1110 · Cited by 394 · see citing works
Neural correlates of error awareness
Klein, T. A., Endraß, T., Kathmann, N., Neumann, J., von Cramon, D. Y., & Ullsperger, M. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.11.014 · Cited by 387 · see citing works
Pulvinar contributions to the dorsal and ventral streams of visual processing in primates
Kaas, J. H., & Lyon, D. C. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.02.008 · Cited by 344 · see citing works
Time to collision is signalled by neurons in the nucleus rotundus of pigeons
Wang, Y., & Frost, B. J. (1992) · Nature · doi:10.1038/356236a0 · Cited by 309 · see citing works
A direct projection from superior colliculus to substantia nigra for detecting salient visual events
Comoli, E., Coizet, V., Boyes, J., Bolam, J. P., Canteras, N. S., Quirk, R. H., Overton, P. G., & Redgrave, P. (2003) · Nature Neuroscience · doi:10.1038/nn1113 · Cited by 295 · see citing works
The primate pulvinar nuclei: vision and action
Grieve, K. L., Acuña, C., & Cudeiro, J. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01482-4 · Cited by 290 · see citing works
Visual attention as a multilevel selection process
Kästner, S., & Pinsk, M. A. (2004) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.4.4.483 · Cited by 258 · see citing works
Livesey, A., Wall, M. B., & Smith, A. T. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.06.033 · Cited by 227 · see citing works
Neural substrate of defensive behavior in the midbrain tectum
Brandão, M. L., Cardoso, S. H., Melo, L. L., Motta, V., & Coimbra, N. C. (1994) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)90047-7 · Cited by 175 · see citing works
Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron
Peron, S., & Gabbiani, F. (2009) · Nature Neuroscience · doi:10.1038/nn.2259 · Cited by 149 · see citing works
Bell, A. H., Meredith, M. A., Opstal, A. J. V., & Munoz, D. P. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0420-z · Cited by 133 · see citing works
Perceiving Time to Collision Activates the Sensorimotor Cortex
Field, D. T., & Wann, J. P. (2005) · Current Biology · doi:10.1016/j.cub.2004.12.081 · Cited by 128 · see citing works
Self-citationDevelopment of sensitivity to information for impending collision
Yonas, A., Bechtold, A. G., Frankel, D., Gordon, F. R., McRoberts, G. W., Norcia, A. M., & Sternfels, S. (1977) · Perception & Psychophysics · doi:10.3758/bf03198713 · Cited by 89 · see citing works
Coull, J. T. (2008) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.010.2008 · Cited by 77 · see citing works
Tectal neurons signal impending collision of looming objects in the pigeon
Wu, L., Niu, Y., Yang, J., & Wang, S. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04397.x · Cited by 76 · see citing works
Multimodal Representation in the Superior Colliculus and Optic Tectum
Stein, B. E. (1984) · Springer eBooks · doi:10.1007/978-1-4899-5376-6_20 · Cited by 68 · see citing works
Spatiotopic Organization in Human Superior Colliculus Observed with fMRI
DuBois, R. M., & Cohen, M. S. (2000) · NeuroImage · doi:10.1006/nimg.2000.0590 · Cited by 60 · see citing works
Functional imaging of the human superior colliculus: An optimised approach
Wall, M. B., Walker, R., & Smith, A. T. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.094 · Cited by 57 · see citing works
Behavior evoked by electrical stimulation of the hamster superior colliculus
NORTHMORE, D. P. M., Levine, E. S., & Schneider, G. E. (1988) · Experimental Brain Research · doi:10.1007/bf00406619 · Cited by 55 · see citing works
The neuroanatomist's dream, the problems and solutions, and the ultimate aim
DeFelipe, J. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.018.2008 · Cited by 16 · see citing works
Judgements of time to contact are affected by rate of appearance of visible texture
Jacobs, D. M., & Díaz, A. (2010) · Quarterly Journal of Experimental Psychology · doi:10.1080/17470211003703475 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Neural circuits underlying visually evoked escapes in larval zebrafish
Dunn, T. W., Gebhardt, C., Naumann, E. A., Riegler, C., Ahrens, M. B., Engert, F., & Del Bene, F. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.021 · Cited by 347 · see citing works
Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice
Shang, C., Chen, Z., Liu, A., Li, Y., Zhang, J., Qu, B., Yan, F., Zhang, Y., Liu, W., Liu, Z., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03580-7 · Cited by 250 · see citing works
Comoli, E., Favaro, P. D., Vautrelle, N., Leriche, M., Overton, P. G., & Redgrave, P. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00009 · Cited by 169 · see citing works
“Potentially harmful looming stimuli activate the SC in a range of species (Westby et al., 1990; Liu et al., 2011) including humans (Billington et al., 2011), while stimulation of the SC can evoke defensive reactions extending from immediate arrest and freezing to violent defense-like locomotor…”
BackgroundFrom affective blindsight to emotional consciousness
Celeghin, A., de Gelder, B., & Tamietto, M. (2015) · Consciousness and Cognition · doi:10.1016/j.concog.2015.05.007 · Cited by 137 · see citing works
The Neural Basis of Escape Behavior in Vertebrates
Branco, T., & Redgrave, P. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100219-122527 · Cited by 129 · see citing works
The Superior Colliculus: Cell Types, Connectivity, and Behavior
Liu, X., Huang, H., Snutch, T. P., Cao, P., Wang, L., & Wang, F. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-022-00858-1 · Cited by 107 · see citing works
“There is also accumulating evidence that the SC/OT is activated in response to unexpected aversive events and looming stimuli to initiate defensive behaviors in other species, including humans [200, 205], monkeys [201], cats [202], pigeons [206], amphibians [207, 208], and zebrafish [122, 209, 210].”
BackgroundA retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour
Huang, L., Yuan, T., Tan, M., Xi, Y., Hu, Y., Tao, Q., Zhao, Z., Zheng, J., Han, Y., Xu, F., et al. (2017) · Nature Communications · doi:10.1038/ncomms14908 · Cited by 100 · see citing works
Classification of Object Size in Retinotectal Microcircuits
Preuß, S., Trivedi, C. A., Berg, C. V., Ryu, S., & Bollmann, J. H. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.012 · Cited by 100 · see citing works
Soares, S. C., Maior, R. S., Isbell, L. A., Tomaz, C. A. B., & Nishijo, H. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00067 · Cited by 100 · see citing works
“The SC-PUL visual system is responsive to such stimuli (e.g., looming objects; Billington et al., 2011).”
BackgroundComparative approaches to escape
Peek, M. Y., & Card, G. M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.09.012 · Cited by 88 · see citing works
Neuronal Responses to Looming Objects in the Superior Colliculus of the Cat
Liu, Y., Wang, Q., & Li, B. (2011) · Brain Behavior and Evolution · doi:10.1159/000327045 · Cited by 76 · see citing works
“, 2005], and has recently been shown to respond to looming stimuli by functional magnetic resonance imaging of the human brain [Billington et al., 2011].”
BackgroundInfluentialPredictive encoding of motion begins in the primate retina
Liu, B., Hong, A. S., Rieke, F. M., & Manookin, M. B. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00899-1 · Cited by 72 · see citing works
Is there anybody out there? Neural circuits of threat detection in vertebrates.
Pereira, A. G., & Moita, M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.09.011 · Cited by 70 · see citing works
Teghil, A., Boccia, M., D’Antonio, F., Vita, A. D., de Lena, C., & Guariglia, C. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.10.003 · Cited by 69 · see citing works
The endophenotype and the phenotype: Temporal discrimination and adult‐onset dystonia
Hutchinson, M., Kimmich, O., Molloy, A., Whelan, R., Molloy, F. M., Lynch, T., Healy, D. G., Walsh, C., Edwards, M. J., Ozelius, L. J., et al. (2013) · Movement Disorders · doi:10.1002/mds.25676 · Cited by 68 · see citing works
“In an fMRI study in humans, whereas timing computations for collision events were functions of the anterior insula, the detection of the looming stimulus (opposed to a receding stimulus) was associated with activation of both superior colliculi.(86) It is possible that the association of peripheral trauma with later d…”
BackgroundAllen, A. E., Procyk, C. A., Howarth, M., Walmsley, L., & Brown, T. M. (2016) · The Journal of Physiology · doi:10.1113/jp271707 · Cited by 71 · see citing works
“…LP cells are sensitive to simple or complex motion or respond to specific shapes (Godfraind et al. 1969; Benevento & Miller, 1981; Petersen et al. 1985; Chalupa & Abramson, 1989; Casanova & Molotchnikoff, 1990; Merabet et al. 1998; Boire et al. 2004; Billington et al. 2011; Van Le et al. 2013).”
BackgroundThe role of the human anterior insular cortex in time processing
Kosillo, P., & Smith, A. T. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0267-8 · Cited by 59 · see citing works
Threatening pictures induce shortened time-to-contact estimates
Brendel, E., DeLucia, P. R., Hecht, H., Stacy, R. L., & Larsen, J. T. (2012) · Attention Perception & Psychophysics · doi:10.3758/s13414-012-0285-0 · Cited by 50 · see citing works
Threat modulates neural responses to looming visual stimuli
Vagnoni, E., Lourenco, S. F., & Longo, M. R. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12998 · Cited by 46 · see citing works
Looming and receding visual networks in awake marmosets investigated with fMRI
Cléry, J. C., Schaeffer, D. J., Hori, Y., Gilbert, K. M., Hayrynen, L. K., Gati, J. S., Menon, R. S., & Everling, S. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116815 · Cited by 42 · see citing works
The effect of immersive virtual reality on proximal and conditioned threat
Rosén, J., Kastrati, G., Reppling, A., Bergkvist, K., & Åhs, F. (2019) · Scientific Reports · doi:10.1038/s41598-019-53971-z · Cited by 41 · see citing works
Feldstein, I. T. (2019) · Perception · doi:10.1177/0301006619861892 · Cited by 35 · see citing works
The influence of optic expansion rates when judging the relative time to contact of familiar objects
Hosking, S. G., & Crassini, B. (2011) · Journal of Vision · doi:10.1167/11.6.20 · Cited by 33 · see citing works
Approaching threatening stimuli cause an expansion of defensive peripersonal space
Bufacchi, R. J. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00316.2017 · Cited by 30 · see citing works
“, 2012), both of which respond to looming stimuli and are 146 involved in time-to-collision judgements (Billington et al., 2011).”
BackgroundRiskind, J. H., & Calvete, E. (2019) · Journal of Personality · doi:10.1111/jopy.12465 · Cited by 31 · see citing works
Animacy and the prediction of behaviour
Schultz, J., & Frith, C. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104766 · Cited by 32 · see citing works
Neural prediction of complex accelerations for object interception
de Rugy, A., Marinovic, W., & Wallis, G. M. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00854.2011 · Cited by 31 · see citing works
“2008) and how timing might be controlled (Billington et al. 2011; Field and Wann 2005).”
BackgroundNeural Substrates Underlying the Passive Observation and Active Control of Translational Egomotion
Huang, R., Chen, C., & Sereno, M. I. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2647-14.2015 · Cited by 30 · see citing works
“This may account for the weak activation in VIP and absent activation in the anterior insula (Billington et al., 2011).”
BackgroundCommon neural correlates of vestibular stimulation and fear learning: an fMRI meta-analysis
Neumann, N., Fullana, M. A., Raduà, J., Brandt, T., Dieterich, M., & Lotze, M. (2023) · Journal of Neurology · doi:10.1007/s00415-023-11568-7 · Cited by 36 · see citing works
“, for avoidance of imminent collisions during driving or in sports, shown by Billington and co-workers [79] in an fMRI investigation in which the SC and the pulvinar nucleus of the thalamus were activated.”
BackgroundMarkkula, G. M., Uludağ, Z., Wilkie, R. M., & Billington, J. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009096 · Cited by 27 · see citing works
“Aligning with findings in non-human species [79–82], functional magnetic resonance imaging in humans has implicated structures such as the superior colliculus and the medial pulvinar nucleus of the thalamus in processing of visual looming [60].”
MethodResultSelf-citationDisrupted superior collicular activity may reveal cervical dystonia disease pathomechanisms
McGovern, E. M., Killian, O., Narasimham, S., Quinlivan, B., Butler, J. S., Beck, R., Beiser, I., Williams, L., Killeen, R. P., Farrell, M., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17074-x · Cited by 28 · see citing works
People Favour Imperfect Catching by Assuming a Stable World
López‐Moliner, J., & Keil, M. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035705 · Cited by 26 · see citing works
“In addition, the activation of cortical and subcortical areas beyond those involved in visual motion processing [17,18] reveals a close correspondence between areas that extract ttc from expansion with the sensoriomotor systems.”
BackgroundDessing, J. C., Vesia, M., & Crawford, J. D. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00015 · Cited by 26 · see citing works
“These findings were recently confirmed in humans using fMRI (Billington et al., 2011).”
BackgroundResultHervais‐Adelman, A., Legrand, L. B., Zhan, M., Tamietto, M., de Gelder, B., & Pegna, A. J. (2015) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00051 · Cited by 26 · see citing works
“Billington et al. (2011) compared brain activation in response to a moving ball made of point lights under conditions of looming, receding and randommotion.”
BackgroundLooming motion primes the visuomotor system.
Skarratt, P. A., Gellatly, A. R. H., Cole, G. G., Pilling, M., & Hulleman, J. (2013) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037/a0034456 · Cited by 24 · see citing works
Fisher, S. D., & Reynolds, J. N. J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00115 · Cited by 24 · see citing works
Basile, G. A., Tatti, E., Bertino, S., Milardi, D., Genovese, G., Bruno, A., Muscatello, M. R. A., Ciurleo, R., Cerasa, A., Quartarone, A., et al. (2024) · Brain Structure and Function · doi:10.1007/s00429-024-02781-9 · Cited by 24 · see citing works
“…detection (such as PT, STS, POS, or at a subcortical level, SC, pulvinar and the cerebellum) (Seifritz et al. 2002; Baumann and Mattingley 2010; Billington et al. 2011; Wang et al. 2016), emotional and behavioral relevance of stimuli (such as ACC, AIC, amygdala or PAG) (Mobbs et al. 2010;…”
BackgroundCarvalho, F. M., Chaim, K. T., Sanchez, T. A., & de Araújo, D. B. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00268 · Cited by 23 · see citing works
“However, it is important to note that fMRI studies have also reported a rightlateralized/preponderant prefrontal-parietal network for perceptual prediction in time-to-contact (Billington et al., 2011) and spatiotemporal trajectory tasks (O’Reilly et al.”
BackgroundResultInfluentialRiskind, J. H. (2024) · Cognitive Therapy and Research · doi:10.1007/s10608-024-10481-1 · Cited by 23 · see citing works
“Approaching stimuli elicit different brain activity patterns than those that are static or receding (Bach et al., 2009; Billington et al., 2011; Coker-Appia et al., 2013; Mobbs et al. 2010; Van Wassenhove et al., 2011).”
Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties
Masterson, S. P., Zhou, N., Akers, B., Dang, W., & Bickford, M. E. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24538 · Cited by 22 · see citing works
Liu, X., Feng, X., Huang, H., Huang, K., Xu, Y., Ye, S., Tseng, Y.-T., Wei, P., Wang, L., & Wang, F. (2022) · BMC Biology · doi:10.1186/s12915-022-01486-x · Cited by 22 · see citing works
“Moreover, there is accumulating evidence showing that visually-evoked innate fear responses elicited during the protocol, which stem from sensory signals dynamics, are highly conserved across species, including humans [69], monkeys [70], cats [71], rodents [42], pigeons [72], amphibians [73], and zebrafish [74].”
Backgroundde Borst, A. W., & de Gelder, B. (2022) · Brain Sciences · doi:10.3390/brainsci12030391 · Cited by 21 · see citing works
“The aINS has been suggested to support judgments on the time to the collision of approaching objects in PPS [37].”
BackgroundInfluentialErrors in motion processing amongst older drivers may increase accident risk
Poulter, D. R., & Wann, J. P. (2013) · Accident Analysis & Prevention · doi:10.1016/j.aap.2013.03.031 · Cited by 21 · see citing works
Self-citationTime‐to‐contact perception in the brain
Baurès, R., Fourteau, M., Thébault, S., Gazard, C., Pasquio, L., Meneghini, G., Perrin, J., Rosito, M., Durand, J., & Roux, F. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24740 · Cited by 20 · see citing works
Neuroplasticity and crossmodal connectivity in the normal, healthy brain.
Karim, A. K. M. R., Proulx, M. J., de Sousa, A. A., & Likova, L. T. (2021) · Psychology & Neuroscience · doi:10.1037/pne0000258 · Cited by 20 · see citing works
Spatiotemporal integration of looming visual and tactile stimuli near the face
Huang, R., Chen, C., & Sereno, M. I. (2018) · Human Brain Mapping · doi:10.1002/hbm.23995 · Cited by 17 · see citing works
“While the responses in AIC were not as strong as those in other unisensory and multisensory sROIs, it could be involved in making judgments about the timing (duration) of looming objects (approaching threats) and in detecting the temporal synchrony or asynchrony of multisensory stimuli (Billington et al., 2011; Bushar…”
BackgroundMethodResultInfluentialVisual looming is a primitive for human emotion
Thieu, M. K., Ayzenberg, V., Lourenco, S. F., & Kragel, P. A. (2024) · iScience · doi:10.1016/j.isci.2024.109886 · Cited by 17 · see citing works
“32 Indeed,thehumansuperiorcolliculus responds to looming visual stimuli, 33 even in the absence of awareness.”
Young Women do it Better: Sexual Dimorphism in Temporal Discrimination
Williams, L., Butler, J. S., Molloy, A., McGovern, E. M., Beiser, I., Kimmich, O., Quinlivan, B., O’Riordan, S., Hutchinson, M., & Reilly, R. B. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00160 · Cited by 17 · see citing works
“Evidence in humans from neuroimaging studies indicates the SC is activated by multisensory looming stimuli (44, 45).”
BackgroundLooming motion and visual attention.
Rossini, J. C. (2014) · Psychology & Neuroscience · doi:10.3922/j.psns.2014.042 · Cited by 17 · see citing works
Somervail, R., Bufacchi, R. J., Guo, Y., Kilintari, M., Novembre, G., Swapp, D., Steed, A. J., & Iannetti, G. D. (2019) · Scientific Reports · doi:10.1038/s41598-019-40075-x · Cited by 17 · see citing works
The neuropathological basis of anxiety in Parkinson’s disease
Overton, P. G., & Coizet, V. (2020) · Medical Hypotheses · doi:10.1016/j.mehy.2020.110048 · Cited by 17 · see citing works
Social, proximal and conditioned threat
Rosén, J., Kastrati, G., & Åhs, F. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.05.014 · Cited by 17 · see citing works
“Whereas defensive responses to proximal and social threat depend on the superior colliculus (Billington et al., 2011; Maior et al., 2012; Rosa Salva et al., 2015; Wei et al., 2015), conditioned fear cues are dependent on the lateral geniculate body and the lateral posterior nucleus of the thalamus (Shi & Davis, 2001).”
BackgroundInfluentialLuminance and contrast in visual perception of time to collision
Landwehr, K., Brendel, E., & Hecht, H. (2013) · Vision Research · doi:10.1016/j.visres.2013.06.009 · Cited by 15 · see citing works
An ethologically based view into human fear
Coelho, C. M., Araújo, A. S., Suttiwan, P., & Zsido, A. N. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.105017 · Cited by 15 · see citing works
Brain activity during time to contact estimation: an EEG study
Daneshi, A., Azarnoush, H., Towhidkhah, F., Bernardin, D., & Faubert, J. (2019) · Cognitive Neurodynamics · doi:10.1007/s11571-019-09563-8 · Cited by 12 · see citing works
Gerb, J., Brandt, T. H., & Dieterich, M. (2022) · Journal of Neurology · doi:10.1007/s00415-022-11015-z · Cited by 12 · see citing works
Looming Auditory Collision Warnings for Semi-Automated Driving
Lahmer, M., Glatz, C., Seibold, V. C., & Chuang, L. L. (2018) · International Conference on Automotive User Interfaces and Interactive Vehicular Applications (AutomotiveUI) · doi:10.1145/3239060.3239086 · Cited by 12 · see citing works
“This finding contrasts with previous research in which an activation of motor related areas was observed for looming sounds [3, 42].”
ResultAllocentric time-to-contact and the devastating effect of perspective
Landwehr, K., Hecht, H., & Both, B. (2014) · Vision Research · doi:10.1016/j.visres.2014.08.022 · Cited by 11 · see citing works
Human subcortical pathways automatically detect collision trajectory without attention and awareness
Guo, F., Zou, J., Wang, Y., Fang, B., Zhou, H., Wang, D., He, S., & Zhang, P. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002375 · Cited by 10 · see citing works
A Brain-Inspired Visual Fear Responses Model for UAV Emergent Obstacle Dodging
Zhao, F., Kong, Q., Zeng, Y., & Xu, B. (2019) · IEEE Transactions on Cognitive and Developmental Systems · doi:10.1109/tcds.2019.2939024 · Cited by 10 · see citing works
“The SC receives the projection from direction-selective retinal ganglion cells [18], [20], [25], and has projections to the pulvinar which has been evidenced in primate brains [18], [20], [25], and rodent brains [21], [28]–[30].”
BackgroundEnhanced early ERP responses to looming angry faces
Yu, Z., Kritikos, A., & Pegna, A. J. (2022) · Biological Psychology · doi:10.1016/j.biopsycho.2022.108308 · Cited by 9 · see citing works
Gould, M. T., Poulter, D. R., Helman, S., & Wann, J. P. (2013) · Journal of Experimental Psychology Applied · doi:10.1037/a0033286 · Cited by 9 · see citing works
Self-citationGeers, L., Kozieja, P., & Coello, Y. (2024) · Cortex · doi:10.1016/j.cortex.2024.01.008 · Cited by 9 · see citing works
Learning to fear novel stimuli by observing others in the social affordance framework
Lanzilotto, M., Monte, O. D., Diano, M., Panormita, M., Battaglia, S., Celeghin, A., Bonini, L., & Tamietto, M. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106006 · Cited by 8 · see citing works
The impact of N-back-induced mental workload and time budget on takeover performance
Goodridge, C. M., Gonçalves, R. C., Arabian, A., Horrobin, A., Solernou, A., Lee, Y. T., Bruneau, A., Lee, Y. M., & Merat, N. (2025) · Accident Analysis & Prevention · doi:10.1016/j.aap.2025.108327 · Cited by 8 · see citing works
Prater, C. M., Harris, B. N., & Carr, J. A. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104707 · Cited by 8 · see citing works
Fernández‐Folgueiras, U., Méndez‐Bértolo, C., Hernández‐Lorca, M., Bódalo, C., Giménez‐Fernández, T., & Carretié, L. (2021) · Psychophysiology · doi:10.1111/psyp.13785 · Cited by 8 · see citing works
Depth Perception and Defensive System Activation in a 3-D Environment
Combe, E., & Fujii, N. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2011.00205 · Cited by 8 · see citing works
“Billington et al. (2011) has shown that the superior colliculus is specifically activated when subjects perceive an approaching (looming) object. The superior colliculus is known to be involved in eye movements, in particular in vergence movements (Guitton, 1999; Chaturvedi and Van Gisbergen, 2000). Hypothetically, th…”
BackgroundInfluentialModeling spatial navigation in the presence of dynamic obstacles: a differential games approach
Darekar, A., Goussev, V., McFadyen, B. J., Lamontagne, A., & Fung, J. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00857.2016 · Cited by 8 · see citing works
“…the dorsal stream, may be involved in the recognition of the obstacle, as well as processing its characteristics, such as shape and motion (see Andersen 1997), while looming stimuli may be detected by the superior colliculus and the medial pulvinar nucleus of the thalamus (Billington et al. 2011).”
BackgroundVisual objects approaching the body modulate subsequent somatosensory processing at 4 months of age
Orioli, G., Parisi, I., van Velzen, J. L., & Bremner, A. J. (2023) · Scientific Reports · doi:10.1038/s41598-023-45897-4 · Cited by 7 · see citing works
Forward optic flow is prioritised in visual awareness independently of walking direction
Motyka, P., Akbal, M., & Litwin, P. (2021) · PLoS ONE · doi:10.1371/journal.pone.0250905 · Cited by 7 · see citing works
“In fact, neurophysiological evidence from humans and primates implies the existence of a dedicated network of subcortical and cortical areas that responds preferentially to objects moving towards the body [97,98].”
BackgroundEvolutionary perspective on peripersonal space and perception
Froesel, M., Hamed, S. B., & Cléry, J. C. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-99193-3.00009-x · Cited by 6 · see citing works
Vitkutė, K., Borghese, F., Hut, R. A., Havekes, R., & Meerlo, P. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.06.029 · Cited by 4 · see citing works
Qin, K., Liu, Y., Liu, S., Li, Y., Li, Y., & You, X. (2023) · Psychophysiology · doi:10.1111/psyp.14425 · Cited by 4 · see citing works
Wann, J. P. (2024) · Frontiers in Psychology · doi:10.3389/fpsyg.2024.1347309 · Cited by 4 · see citing works
Self-citationTennis experience impacts time estimation within different timing processes: An ERP study
Tang, H., Zhao, Z., Lin, L., Chen, S., Han, H., & Jin, X. (2024) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2024.109059 · Cited by 4 · see citing works
Barr, J., Vangel, R., Kanel, P., Roytman, S., Pongmala, C., Albin, R. L., Scott, P. J. H., & Bohnen, N. I. (2024) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2309178 · Cited by 4 · see citing works
“Researches have demonstrated that in many animals it enables looming-collision detection behavior [56,57].”
BackgroundHand movements influence the perception of time in a prediction motion task
Li, X., Baurès, R., & Crémoux, S. (2023) · Attention Perception & Psychophysics · doi:10.3758/s13414-023-02690-9 · Cited by 4 · see citing works
“, 2013; Tomassini & D’Ausilio, 2018), including the TTC perception task (Assmus et al., 2003; Baurès et al., 2021; Billington et al., 2011; Coull et al., 2008; Field & Wann, 2005).”
BackgroundNakagawa, H., & Nishida, Y. (2012) · Biology Open · doi:10.1242/bio.20121693 · Cited by 3 · see citing works
“In the human brain, a non-invasive fMRI study revealed the neuronal correlate of motor planning in response to an approaching danger (Billington et al., 2011; Coull et al., 2008).”
BackgroundCalabro, F. J., Beardsley, S. A., & Vaina, L. M. (2019) · Experimental Brain Research · doi:10.1007/s00221-019-05613-z · Cited by 3 · see citing works
Sato, K., Fukuhara, K., & Higuchi, T. (2023) · Experimental Aging Research · doi:10.1080/0361073x.2023.2278985 · Cited by 2 · see citing works
“…an approaching object, including eye-height information, is particularly important in the perception of TTC. Brain regions involved in responding to object approach and estimating TTC include the superior colliculus and the pulvinar nucleus of the thalamus (Billington, Wilkie, Field, & Wann, 2011).”
Should I stay or should I go? The cerebral bases of street‐crossing decision
Baurès, R., Leblond, S., Dewailly, A., Cherubini, M., Subramanian, L. D., Kearney, J. K., Durand, J., & Roux, F. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25279 · Cited by 2 · see citing works
“…the lateralization of the process appears debated in the literature, which has either suggested a bilateral implication of the parietal area (Billington et al., 2011 ), a left implication (Assmus et al., 2003; Coull et al., 2008 ; Field & Wann, 2005 ) or a right implication (Baurès et al.,…”
BackgroundResultInfluentialYamasaki, D., & Nagai, M. (2024) · Frontiers in Psychology · doi:10.3389/fpsyg.2024.1414702 · Cited by 2 · see citing works
“…2005) Looming, the specific visual pattern of expansion, results in increased neural activation in the visuomotor cortex (Peron and Gabbiani, 2009; Billington et al., 2011), and superior temporal sulcus (Tyll et al., 2013), seemingly leading to faster detection and motor responses to looming…”
BackgroundBillington, J., Furlan, M., & Wann, J. P. (2012) · Displays · doi:10.1016/j.displa.2012.10.008 · Cited by 2 · see citing works
“the use of dichopic displays in an MRI scanner environment to revisit the behavioural research on cue integration [5] and neural research on looming detection [11].”
BackgroundResultInfluentialSelf-citationEffect of Acute Psychological Stress on Motion-in-Depth Perception: An Event-Related Potential Study
Wang, J., Yu, L., He, M., & Qi, C. (2020) · Advances in Cognitive Psychology · doi:10.5709/acp-0309-6 · Cited by 2 · see citing works
Subjective time dilation as a result of entropy
Zhang, D., Wang, Y., & Bao, Y. (2023) · PsyCh Journal · doi:10.1002/pchj.695 · Cited by 2 · see citing works
Yu, Z., Moses, E., Kritikos, A., & Pegna, A. J. (2024) · Brain Sciences · doi:10.3390/brainsci14010098 · Cited by 1 · see citing works
“Interestingly, other studies have shown that when contrasted with receding stimuli, looming stimuli activate the superior colliculus and the pulvinar nucleus of the thalamus [62], as in the case of emotion and threat.”
BackgroundWei, X., Wang, C., Song, Y., & Qi, C. (2025) · Scientific Reports · doi:10.1038/s41598-024-83707-7 · Cited by 1 · see citing works
“Referring to previous studies on collision time estimation 28,29 and the characteristics of individual visual processing 30 , this study establishes two collision time estimation conditions at 400ms and 800ms.”
A molecularly defined brain circuit module for regulating panic-like defensive state
Zhao, M., Zhang, L., Chen, Z., Zhang, S., Cheng, X., Huang, M., Li, X., Gu, H., Guan, X., Geng, D., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60529-3 · Cited by 2 · see citing works
Coizet, V., Tannir, R. A., Pautrat, A., & Overton, P. G. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230818154903 · Cited by 2 · see citing works
“…reported following collicular stimulation in other species, the colliculus in a wide range of species contains neurons sensitive to looming stimuli (pigeon optic tectum, [42], frog optic tectum, [43], mouse, [44], cat, [45], humans, [46]), which indirectly suggests a role in avoidance/escape.”
BackgroundPerceptual errors in predicting vehicle approach in typical and atypical populations
Purcell, C. (2012) · Royal Holloway Digital Repository (Royal Holloway University of London) · Cited by 1 · see citing works
Animacy and the prediction of behaviourPreprint
Schultz, J., & Frith, C. (2020) · doi:10.31234/osf.io/2k4mj · Cited by 1 · see citing works
“Neurons sensitive to looming are found in several animal species (Merchant and Georgopoulos, 2006) and, in primates, both subcortical and cortical sites respond to looming (Field and Wann, 2005; Maier et al., 2008; Billington et al., 2011).”
BackgroundContribution of linear and nonlinear mechanisms to predictive motion estimationPreprint
Liu, B., Hong, A. S., Rieke, F. M., & Manookin, M. B. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.09.467979 · Cited by 1 · see citing works
Preference for motion and depth in 3D film
Hartle, B., Lugtigheid, A. J., Kazimi, A., Allison, R. S., & Wilcox, L. M. (2015) · Proceedings of SPIE, the International Society for Optical Engineering/Proceedings of SPIE · doi:10.1117/12.2079330
High-density EEG study of how looming information is processed in the infant brain
Taer, N. R. M. (2015) · BIBSYS Brage (BIBSYS (Norway))
Final Synthesis and Conclusions
Riskind, J. H., & Rector, N. A. (2018) · Springer eBooks · doi:10.1007/978-1-4939-8782-5_17
Functional Neuroanatomy of Time-To-Passage Perception
Geng, Y., Şıkoğlu, E. M., Hecht, H., & Vaina, L. M. (2018) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2018.811039
“Consistent with previous research, we also found activation in bilateral superior colliculus (SC), which is an area involved in motor preparation and attention [6].”
BackgroundResultInfluentialCollicular Anatomy and Function
Gharaei, S., Stuart, G. J., & Arabzadeh, E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24253-3
Caiwen, L. I., Zang, F., Xuan, Y., & Fu, X. (2020) · Advances in Psychological Science · doi:10.3724/sp.j.1042.2020.01650
- Authors
- Billington, J., Wilkie, R. M., Field, D. T., & Wann, J. P.
- Affiliations
- Royal Holloway University of London (GB)
- University of Leeds (GB)
- University of Reading (GB)
- Corresponding author
- Wann, John P.
- Venue
- Proceedings of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2010-10-27
- Volume
- 278
- Issue
- 1711
- Pages
- 1476-1481
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC3081747
- OpenAlex
- W2095956597
- Cited by
- 111
- References
- 29
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 11 · 2023: 10 · 2022: 8 · 2021: 8 · 2020: 9 · 2019: 7 · 2018: 8 · 2017: 6 · 2016: 5 · 2015: 7 · 2014: 4 · 2013: 6 · 2012: 6
- FWCI
- 3.30
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CentAUR (University of Reading) (acceptedVersion)
- Funders
- Engineering and Physical Sciences Research Council (EP/D055342/1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- looming stimuli, collision detection, superior colliculus, pulvinar, thalamus, anterior insula, motor preparation, collision timing, threat detection, visual motion perception
- MeSH terms
- Adult, Brain Mapping, Cerebral Cortex, Female, Humans, Magnetic Resonance Imaging, Male, Motion Perception, Photic Stimulation, Reaction Time, Superior Colliculi, Pulvinar
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