Please wait a minute...
Advances in Psychological Science    2020, Vol. 28 Issue (4) : 579-587     DOI: 10.3724/SP.J.1042.2020.00579
Regular Articles |
Spatial frequencies affect the processing of fearful facial expression in neural pathways
HE Zeyu,ZHANG Ziqi,LI Kexuan,HE Weiqi()
Research Center of Brain and Cognitive Neuroscience, Liaoning Normal University, Dalian 116029, China
Download: PDF(545 KB)   HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks    
Abstract  

Fear has been often given priority to effective processing for the need to evade threatening stimuli. Most of researches have probed the influence of high and low spatial frequencies on the processing of fearful faces from the perspective of the two-channel model. Low spatial frequency components of the fearful face can be processed preferentially in the subcortical pathway. The high spatial frequency mainly processes the fearful faces through the cortical pathway. On this basis, researchers have proposed multiple pathways. The purpose of this paper is to review the subcortical, cortical and multiple pathways from the physiological perspective, and then organize the effects that high/low spatial frequencies on the processing of fearful faces in the various pathways and propose the controversies. Finally, we suggested several focuses that could be studied in the future.

Keywords spatial frequency      fearful facial expression      subcortical pathway      cortical pathway      multiple pathways     
ZTFLH:  B842  
  B845  
Corresponding Authors: Weiqi HE     E-mail: weiqi79920686@sina.com
Issue Date: 24 February 2020
Service
E-mail this article
E-mail Alert
RSS
Articles by authors
Zeyu HE
Ziqi ZHANG
Kexuan LI
Weiqi HE
Cite this article:   
Zeyu HE,Ziqi ZHANG,Kexuan LI, et al. Spatial frequencies affect the processing of fearful facial expression in neural pathways[J]. Advances in Psychological Science, 2020, 28(4): 579-587.
URL:  
http://journal.psych.ac.cn/xlkxjz/EN/10.3724/SP.J.1042.2020.00579     OR     http://journal.psych.ac.cn/xlkxjz/EN/Y2020/V28/I4/579
1 陈珊珊, 蔡厚德 . ( 2015). 丘脑枕核参与情绪信息加工的多条通路. 心理科学进展, 23( 2), 234-240.
url: http://journal.psych.ac.cn/xlkxjz/CN/article/article3225.shtml
2 Adolphs, R . ( 2008). Fear, faces, and the human amygdala. Current Opinion in Neurobiology, 18( 2), 166-172.
url: http://118.145.16.217/magsci/article/article?id=14164030
3 Adolphs R., Gosselin F., Buchanan T. W., Tranel D., Schyns P., & Damasio A. R . ( 2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433( 7021), 68-72.
url: http://dx.doi.org/10.1038/nature03086
4 Alorda C., Serrano-Pedraza I., Campos-Bueno J. J., Sierra-Vázquez V., & Montoya P . ( 2007). Low spatial frequency filtering modulates early brain processing of affective complex pictures. Neuropsychologia, 45( 14), 3223-3233.
url: http://118.145.16.217/magsci/article/article?id=14353798
5 Bar, M . ( 2003). A cortical mechanism for triggering top-down facilitation in visual object recognition. Journal of Cognitive Neuroscience, 15( 4), 600-609.
url: http://dx.doi.org/10.1162/089892903321662976
6 Bocanegra, B. R., & Zeelenberg, R . ( 2009). Emotion improves and impairs early vision. Psychological science, 20( 6), 707-713.
url: http://dx.doi.org/10.1111/j.1467-9280.2009.02354.x
7 Bridge H., Leopold D. A., & Bourne J. A . ( 2016). Adaptive pulvinar circuitry supports visual cognition. Trends in Cognitive Ssciences, 20( 2), 146-157.
url: http://dx.doi.org/10.1016/j.tics.2015.10.003
8 Bullier J., Hupé J.-M., James A. C., & Girard P . ( 2001). The role of feedback connections in shaping the responses of visual cortical neurons. Hofman, Michel A.(Ed.), Progress in Brain Research, 134, 193-204.
url: http://dx.doi.org/10.1016/S0079-6123(01)34014-1
9 Burra N., Hervais-Adelman A., Celeghin A., de Gelder B., & Pegna A. J . ( 2017). Affective blindsight relies on low spatial frequencies. Neuropsychologia, 128, 44-49.
10 Burra N., Hervais-Adelman A., Kerzel D., Tamietto M., de Gelder B., & Pegna A. J . ( 2013). Amygdala activation for eye contact despite complete cortical blindness. Journal of Neuroscience, 33( 25), 10483-10489.
url: http://dx.doi.org/10.1523/JNEUROSCI.3994-12.2013
11 Carretié L., Hinojosa J. A., López-Martín S., & Tapia M . ( 2007). An electrophysiological study on the interaction between emotional content and spatial frequency of visual stimuli. Neuropsychologia, 45( 6), 1187-1195.
url: http://118.145.16.217/magsci/article/article?id=14354075
12 Cushing C. A., Im H. Y., Adams Jr R. B., Ward N., & Kveraga K . ( 2019). Magnocellular and parvocellular pathway contributions to facial threat cue processing. Social Cognitive and Affective Neuroscience, 14( 2), 151-162.
url: http://dx.doi.org/10.1093/scan/nsz003
13 Das P., Kemp A. H., Liddell B. J., Brown K. J., Olivieri G., Peduto A., .. Williams L. M . ( 2005). Pathways for fear perception: Modulation of amygdala activity by thalamo-cortical systems. Neuroimage, 26( 1), 141-148.
url: http://dx.doi.org/10.1016/j.neuroimage.2005.01.049
14 de Cesarei, A.., & Codispoti, M., . ( 2013). Spatial frequencies and emotional perception. Reviews in the Neurosciences, 24( 1), 89-104.
url: http://118.145.16.217/magsci/article/article?id=19427799
15 de Valois R. L., Albrecht D. G., & Thorell L. G . ( 1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research, 22( 5), 545-559.
url: http://dx.doi.org/10.1016/0042-6989(82)90113-4
16 Du S., Tao Y., & Martinez A. M . ( 2014). Compound facial expressions of emotion. Proceedings of the National Academy of Sciences, 111( 15), E1454-E1462.
url: http://dx.doi.org/10.1073/pnas.1322355111
17 Fradcourt B., Peyrin C., Baciu M., & Campagne A . ( 2013). Behavioral assessment of emotional and motivational appraisal during visual processing of emotional scenes depending on spatial frequencies. Brain and Cognition, 83( 1), 104-113.
url: http://118.145.16.217/magsci/article/article?id=19632293
18 Furl N., Henson R. N., Friston K. J., & Calder A. J . ( 2013). Top-down control of visual responses to fear by the amygdala. Journal of Neuroscience, 33( 44), 17435-17443.
url: http://dx.doi.org/10.1523/JNEUROSCI.2992-13.2013
19 Garvert M. M., Friston K. J., Dolan R. J., & Garrido M. I . ( 2014). Subcortical amygdala pathways enable rapid face processing. Neuroimage, 102, 309-316.
url: http://118.145.16.217/magsci/article/article?id=23471392
20 Goffaux V., Jemel B., Jacques C., Rossion B., & Schyns P. G . ( 2003). ERP evidence for task modulations on face perceptual processing at different spatial scales. Cognitive Science, 27( 2), 313-325.
url: http://dx.doi.org/10.1207/s15516709cog2702_8
21 Hariri A. R., Mattay V. S., Tessitore A., Fera F., & Weinberger D. R . ( 2003). Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry, 53( 6), 494-501.
url: http://dx.doi.org/10.1016/S0006-3223(02)01786-9
22 Hassin R. R., Aviezer H., & Bentin S . ( 2013). Inherently ambiguous: Facial expressions of emotions, in context. Emotion Review, 5( 1), 60-65.
url: http://118.145.16.217/magsci/article/article?id=19815515
23 Holmes A., Green S., & Vuilleumier P . ( 2005). The involvement of distinct visual channels in rapid attention towards fearful facial expressions. Cognition & Emotion, 19( 6), 899-922.
url: http://dx.doi.org/tion
24 Isbell, L. A . ( 2006). Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution, 51( 1), 1-35.
url: http://dx.doi.org/10.1016/j.jhevol.2005.12.012
25 Jack R. E., Blais C., Scheepers C., Schyns P. G., & Caldara R . ( 2009). Cultural confusions show that facial expressions are not universal. Current Biology, 19( 18), 1543-1548.
url: http://118.145.16.217/magsci/article/article?id=14997203
26 Jeantet C., Caharel S., Schwan R., Lighezzolo-Alnot J., & Laprevote V . ( 2018). Factors influencing spatial frequency extraction in faces: A review. Neuroscience & Biobehavioral Reviews, 93, 123-138.
url: http://dx.doi.org/science
27 LeDoux, J . ( 1998). The emotional brain: The mysterious underpinnings of emotional life. Simon and Schuster.
28 Liu C. H., Collin C. A., Rainville S. J., & Chaudhuri A . ( 2000). The effects of spatial frequency overlap on face recognition. Journal of Experimental Psychology: Human Perception and Performance, 26( 3), 956-979.
url: http://dx.doi.org/10.1037/0096-1523.26.3.956
29 Márkus Z., Berényi A., Paróczy Z., Wypych M., Waleszczyk W. J., Benedek G., & Nagy A . ( 2009). Spatial and temporal visual properties of the neurons in the intermediate layers of the superior colliculus. Neuroscience Letters, 454( 1), 76-80.
url: http://dx.doi.org/10.1016/j.neulet.2009.02.063
30 McFadyen J., Mattingley J. B., & Garrido M. I . ( 2019). An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition. eLife, 8, e40766.
url: http://dx.doi.org/10.7554/eLife.40766
31 McFadyen J., Mermillod M., Mattingley J. B., Halász V., & Garrido M. I . ( 2017). A rapid subcortical amygdala route for faces irrespective of spatial frequency and emotion. Journal of Neuroscience, 37( 14), 3864-3874.
url: http://dx.doi.org/10.1523/JNEUROSCI.3525-16.2017
32 Méndez-Bértolo C., Moratti S., Toledano R., Lopez-Sosa F., Martínez-Alvarez R., Mah Y. H., .. Strange B. A . ( 2016). A fast pathway for fear in human amygdala. Nature Neuroscience, 19( 8), 1041-1049.
url: http://dx.doi.org/10.1038/nn.4324
33 Merigan, W. H., & Maunsell, J. H. R . ( 1993). How parallel are the primate visual pathways? Annual Review of Neuroscience, 16( 1), 369-402.
url: http://dx.doi.org/10.1146/annurev.ne.16.030193.002101
34 Mermillod M., Droit-Volet S., Devaux D., Schaefer A., & Vermeulen N . ( 2010). Are coarse scales sufficient for fast detection of visual threat? Psychological Science, 21( 10), 1429-1437.
url: http://dx.doi.org/10.1177/0956797610381503
35 Morris J. S., ?hman A., & Dolan R. J . ( 1999). A subcortical pathway to the right amygdala mediating “unseen” fear. Proceedings of the National Academy of Sciences, 96( 4), 1680-1685.
url: http://dx.doi.org/10.1073/pnas.96.4.1680
36 ?hman, A . ( 2005). The role of the amygdala in human fear: Automatic detection of threat. Psychoneuroendocrinology, 30( 10), 953-958.
url: http://dx.doi.org/10.1016/j.psyneuen.2005.03.019
37 ?hman, A., & Mineka, S . ( 2001). Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review, 108( 3), 483-522.
url: http://dx.doi.org/10.1037/0033-295X.108.3.483
38 Padmala S., Lim S.-L., & Pessoa L . ( 2010). Pulvinar and affective significance: Responses track moment-to- moment stimulus visibility. Frontiers in Human Neuroscience, 4, 64.
39 Pessoa, L . ( 2010). Emotion and attention effects: Is it all a matter of timing? Not yet. Frontiers in Human Neuroscience, 4, 172.
40 Pessoa, L., & Adolphs, R . ( 2010). Emotion processing and the amygdala: From a 'low road' to 'many roads' of evaluating biological significance. Nature Reviews Neuroscience, 11( 11), 773-782.
41 Pessoa, L., & Adolphs, R . ( 2011). Emotion and the brain: Multiple roads are better than one. Nature Reviews Neuroscience, 12( 7), 425.
42 Peyrin C., Schwartz S., Seghier M., Michel C., Landis T., & Vuilleumier P . ( 2005). Hemispheric specialization of human inferior temporal cortex during coarse-to-fine and fine-to-coarse analysis of natural visual scenes. Neuroimage, 28( 2), 464-473.
url: http://dx.doi.org/10.1016/j.neuroimage.2005.06.006
43 Phelps, E. A., & LeDoux, J. E . ( 2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48( 2), 175-187.
url: http://dx.doi.org/10.1016/j.neuron.2005.09.025
44 Pourtois G., Dan E. S., Grandjean D., Sander D., & Vuilleumier P . ( 2005). Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked‐potentials mapping. Human Brain Mapping, 26( 1), 65-79.
url: http://dx.doi.org/10.1002/hbm.20130
45 Shi, C., & Davis, M . ( 2001). Visual pathways involved in fear conditioning measured with fear-potentiated startle: Behavioral and anatomic studies. Journal of Neuroscience, 21( 24), 9844-9855.
url: http://dx.doi.org/10.1523/JNEUROSCI.21-24-09844.2001
46 Silverstein, D. N., & Ingvar, M . ( 2015). A multi-pathway hypothesis for human visual fear signaling. Frontiers in Systems Neuroscience, 9, 101.
47 Skottun, B. C . ( 2015). On the use of spatial frequency to isolate contributions from the magnocellular and parvocellular systems and the dorsal and ventral cortical streams. Neuroscience & Biobehavioral Reviews, 56, 266-275.
url: http://dx.doi.org/science
48 Stein T., Seymour K., Hebart M. N., & Sterzer P . ( 2014). Rapid fear detection relies on high spatial frequencies. Psychological Science, 25( 2), 566-574.
url: http://dx.doi.org/10.1177/0956797613512509
49 Tamietto, M., & de Gelder, B . ( 2010). Neural bases of the non-conscious perception of emotional signals. Nature Reviews Neuroscience, 11( 10), 697-709.
50 Tamietto, M., & Morrone, M. C . ( 2016). Visual plasticity: Blindsight bridges anatomy and function in the visual system. Current Biology, 26( 2), R70-R73.
url: http://dx.doi.org/10.1016/j.cub.2015.11.026
51 Tamietto M., Pullens P., de Gelder B., Weiskrantz L., & Goebel R . ( 2012). Subcortical connections to human amygdala and changes following destruction of the visual cortex. Current Biology, 22( 15), 1449-1455.
url: http://118.145.16.217/magsci/article/article?id=24439234
52 Tessari, M . ( 2012). Intracranial electrophysiological recordings of human orbitofrontal responses to emotional stimuli (Unpublished master dissertation). University of Padova, Italy.
53 Tian J., Wang J., Xia T., Zhao W., Xu Q., & He W . ( 2018). The influence of spatial frequency content on facial expression processing: An ERP study using rapid serial visual presentation. Scientific Reports, 8( 1), 2383.
url: http://dx.doi.org/10.1038/s41598-018-20467-1
54 Vlamings P. H. J. M., Goffaux V., & Kemner C . ( 2009). Is the early modulation of brain activity by fearful facial expressions primarily mediated by coarse low spatial frequency information? Journal of Vision, 9( 5), 12-12.
55 Vuilleumier, P . ( 2005). How brains beware: Neural mechanisms of emotional attention. Trends in Cognitive Sciences, 9( 12), 585-594.
url: http://dx.doi.org/10.1016/j.tics.2005.10.011
56 Vuilleumier P., Armony J. L., Driver J., & Dolan R. J . ( 2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neuroscience, 6( 6), 624-631.
url: http://dx.doi.org/10.1038/nn1057
57 Vuilleumier P., Richardson M. P., Armony J. L., Driver J., & Dolan R. J . ( 2004). Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neuroscience, 7( 11), 1271-1278.
url: http://dx.doi.org/10.1038/nn1341
58 Webster M. A., de Valois K. K., & Switkes E . ( 1990). Orientation and spatial-frequency discrimination for luminance and chromatic gratings. Josa A, 7( 6), 1034-1049.
59 Willenbockel V., Lepore F., Nguyen D. K., Bouthillier A., & Gosselin F . ( 2012). Spatial frequency tuning during the conscious and non-conscious perception of emotional facial expressions-an intracranial ERP study. Frontiers in Psychology, 3, 237.
60 You, Y., & Li, W . ( 2015). Parallel processing of general and specific threat during early stages of perception. Social Cognitive and Affective Neuroscience, 11( 3), 395-404.
61 Zhang P., Zhou H., Wen W., & He S . ( 2015). Layer- specific response properties of the human lateral geniculate nucleus and superior colliculus. Neuroimage, 111, 159-166.
url: http://dx.doi.org/10.1016/j.neuroimage.2015.02.025
[1] WANG Lili; JIA Lina; LUO Yuejia. Automatic processing of emotions: Evidence and controversy[J]. Advances in Psychological Science, 2016, 24(8): 1185-1197.
[2] CHEN Shanshan; CAI Houde. Pulvinar Involves in Multiple Pathways of Emotion Processing[J]. Advances in Psychological Science, 2015, 23(2): 234-240.
[3] DU Lei. Brain Mechanisms of Threatening Information Detection[J]. Advances in Psychological Science, 2013, 21(2): 243-251.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
Copyright © Advances in Psychological Science
Support by Beijing Magtech