Research debate: Does spatial attention modulate C1 component?

doi:10.3724/SP.J.1042.2018.01901

Abstract

Abstract:

In the event-related potential (ERP) studies of visual attention, there is a debate regarding whether the C1 component, originated in V1, is modulated by spatial attention. The majority view suggests that C1 is not directly modulated by spatial attention; however, there is a delayed-feedback in V1. The minority view, on the other hand, implies that the C1 component can be directly modulated by spatial attention at the early feed-forward processing stage. Recently there was a debate regarding this issue. In this review, we first summarize the main points and evidence for each side. Second, we listed the factors that may affect the C1 attentional effects. Third, we review and comments on the recent discussions on three aspects, including the repeatability of C1 attentional effect, the role of perceptual and attentional load in eliciting this effect, and the relationship between C1 polarity reversal and its V1-origin. Finally we proposed two points of view: the first is that we should be open and cautious towards the minority view, and the second, there are some techniques and methods that may help to reveal the potential C1 attentional effect. In conclusion, the majority view has been supported by many previous studies and the minority view needs more decisive evidence, and this debate will continue.

Key words: attention, C1, event-related potential (ERP)

CLC Number:

B842.2

FU Shimin, CHEN Xiaowen, LIU Yuqi. Research debate: Does spatial attention modulate C1 component?[J]. Advances in Psychological Science, 2018, 26(11): 1901-1914.

References 55

[1]	陈建, 袁杰, 汪海玲, 王妍, 傅世敏 . ( 2013). C1 调制效应的理论评述及影响因素. 心理科学进展, 21( 3), 407-417 doi: 10.3724/SP.J.1042.2013.00407 URL
[2]	Ales, J. M., Yates, J. L., & Norcia, A. M. ( 2010). V1 is not uniquely identified by polarity reversals of responses to upper and lower visual field stimuli. Neuroimage, 52( 4), 1401-1409. doi: 10.1016/j.neuroimage.2010.05.016 URL
[3]	Ales, J. M., Yates, J. L., & Norcia, A. M. ( 2013). On determining the intercranial sources of visual evoked potentials from scalp topography: A reply to Kelly et al. (this issue). Neuroimage, 64, 703-711. doi: 10.1016/j.neuroimage.2012.09.009 URL
[4]	Bahrami, B., Carmel, D., Walsh, V., Rees, G., & Lavie, N. ( 2008). Spatial attention can modulate unconscious orientation processing. Perception, 37( 10), 1520-1528. doi: 10.1068/p5999 URL pmid: 19065856
[5]	Baumgartner, H. M., Graulty, C. J., Hillyard, S. A., & Pitts, M. A. ( 2018). Does spatial attention modulate the C1 component? The jury continues to deliberate. Cognitive Neuroscience, 9( 1-2), 34-37. doi: 10.1080/17588928.2017.1386169 URL pmid: 28956499
[6]	Bayer, M., Rossi, V., Vanlessen, N., Grass, A., Schacht, A., & Pourtois, G. ( 2017). Independent effects of motivation and spatial attention in the human visual cortex. Social Cognitive and Affective Neuroscience, 12( 1), 146-156.
[7]	Clark, V.P., & Hillyard, S.A . ( 1996). Spatial selective attention affects early extrastriate but not striate components of the visual evoked potential. Journal of Cognitive Neuroscience, 8( 5), 387-402. doi: 10.1162/jocn.1996.8.5.387 URL
[8]	Dassanayake, T. L., Michie, P. T., & Fulham, R. ( 2016). Effect of temporal predictability on exogenous attentional modulation of feedforward processing in the striate cortex. International Journal of Psychophysiology, 105, 9-16. doi: 10.1016/j.ijpsycho.2016.04.007 URL
[9]	Desimone, R., & Duncan, J.( 1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18, 193-222. doi: 10.1146/annurev.ne.18.030195.001205 URL
[10]	Di Russo, F., Martinez, A., & Hillyard, S. A. ( 2003). Source analysis of event-related cortical activity during visuo- spatial attention. Cerebral Cortex, 13( 5), 486-499. doi: 10.1093/cercor/13.5.486 URL
[11]	Ding, Y. L., Martinez, A., Qu, Z., & Hillyard, S. A. ( 2014). Earliest stages of visual cortical processing are not modified by attentional load. Human Brain Mapping, 35( 7), 3008-3024. doi: 10.1002/hbm.22381 URL
[12]	Fu, S.M. ( 2018a). Open and cautious towards the “minority view”. Cognitive Neuroscience, 9( 1-2), 28-30.
[13]	Fu, S.M. ( 2018b). ‘Tricks’ for revealing potential attentional modulations on the C1 component. Cognitive Neuroscience, 9( 1-2), 63-64. doi: 10.1080/17588928.2017.1384376 URL pmid: 28944720
[14]	Fu, S. M., Caggiano, D. M., Greenwood, P. M., & Parasuraman, R. ( 2005b). Event-related potentials reveal dissociable mechanisms for orienting and focusing visuospatial attention. Cognitive Brain Research, 23( 2-3), 341-353. doi: 10.1016/j.cogbrainres.2004.11.014 URL
[15]	Fu, S. M.,Fan, S. L.,Chen, L., & Zhuo, Y. ( 2001). The attentional effects of peripheral cueing as revealed by two event-related potential studies. Clinical Neurophysiology, 112( 1), 172-185. doi: 10.1016/S1388-2457(00)00500-9 URL pmid: 11137676
[16]	Fu, S. M., Fedota, J., Greenwood, P. M., & Parasuraman, R. ( 2010a). Early interaction between perceptual load and involuntary attention: An event-related potential study. Neuroscience Letters, 468( 1), 68-71. doi: 10.1016/j.neulet.2009.10.065 URL
[17]	Fu, S. M., Fedota, J. R., Greenwood, P. M., & Parasuraman, R. ( 2010b). Dissociation of visual C1 and P1 components as a function of attentional load: an event-related potential study. Biological Psychology, 85( 1), 171-178. doi: 10.1016/j.biopsycho.2010.06.008 URL
[18]	Fu, S. M., Fedota, J. R., Greenwood, P. M., & Parasuraman, R. ( 2012). Attentional load is not a critical factor for eliciting C1 attentional effect - A reply to Rauss, Pourtois, Vuillenumier, and Schwartz. Biological Psychology, 91( 2), 321-324. doi: 10.1016/j.biopsycho.2012.03.012 URL
[19]	Fu, S.M.,Greenwood, P.M., & Parasuraman, R.( 2005a). Brain mechanisms of involuntary visuospatial attention: An event-related potential study. Human Brain Mapping, 25( 4), 378-390. doi: 10.1002/(ISSN)1097-0193 URL
[20]	Fu, S. M., Huang, Y. X., Luo, Y. J., Wang, Y., Fedota, J., Greenwood, P. M., & Parasuraman, R. ( 2009). Perceptual load interacts with involuntary attention at early processing stages: Event-related potential studies. Neuroimage, 48( 1), 191-199. doi: 10.1016/j.neuroimage.2009.06.028 URL
[21]	Fu, S. M., Zinni, M., Squire, P. N., Kumar, R., Caggiano, D. M., & Parasuraman, R. ( 2008). When and where perceptual load interacts with voluntary visuospatial attention: An event-related potential and dipole modeling study. Neuroimage, 39( 3), 1345-1355. doi: 10.1016/j.neuroimage.2007.09.068 URL
[22]	Heinze, H. J., Mangun, G. R., Burchert, W., Hinrichs, H., Scholz, M., Münte, T. F., ... Hillyard, S. A. ( 1994). Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature, 372, 543-546. doi: 10.1038/372543a0 URL
[23]	Herde, L., Rossi, V., Pourtois, G., & Rauss, K. ( 2018). Early retinotopic responses to violations of emotion-location associations may depend on conscious awareness. Cognitive Neuroscience, 9( 1-2), 38-55. doi: 10.1080/17588928.2017.1338250 URL
[24]	Hillyard, S. A., Vogel, E. K., & Luck, S. J. ( 1998). Sensory gain control (amplification) as a mechanism of selective attention: Electrophysiological and neuroimaging evidence. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 353( 1373), 1257-1270. doi: 10.1098/rstb.1998.0281 URL
[25]	Hopfinger, J.B., & Mangun, G.R . ( 1998). Reflexive attention modulates processing of visual stimuli in human extrastriate cortex. Psychological Science, 9( 6), 441-447. doi: 10.1111/1467-9280.00083 URL pmid: 4552358
[26]	Jeffreys, D.A., & Axford, J.G . ( 1972a). Source locations of pattern-specific components of human visual evoked potentials. I. Component of striate cortical origin. Experimental Brain Research, 16( 1), 1-21.
[27]	Jeffreys, D.A., & Axford, J.G . ( 1972b). Source locations of pattern-specific components of human visual evoked potentials. II. Component of extrastriate cortical origin. Experimental Brain Research, 16( 1), 22-40.
[28]	Jin, H., Xu, G. P., Zhang, J. X., Ye, Z., Wang, S. F., Zhao, L., ... Mo, L. ( 2010). Athletic training in badminton players modulates the early C1 component of visual evoked potentials: A preliminary investigation. International Journal of Psychophysiology, 78( 3), 308-314. doi: 10.1016/j.ijpsycho.2010.09.005 URL
[29]	Karns, C.M., & Knight, R.T . ( 2009). Intermodal auditory, visual, and tactile attention modulates early stages of neural processing. Journal of Cognitive Neuroscience, 21( 4), 669-683. doi: 10.1162/jocn.2009.21037 URL
[30]	Kelly, S. P., Gomez-Ramirez, M., & Foxe, J. J. ( 2008). Spatial attention modulates initial afferent activity in human primary visual cortex. Cerebral Cortex, 18( 11), 2629-2636. doi: 10.1093/cercor/bhn022 URL
[31]	Kelly, S. P., Vanegas, M. I., Schroeder, C. E., & Lalor, E. C. ( 2013). The cruciform model of striate generation of the early VEP, re-illustrated, not revoked: A reply to Ales et al. (2013). Neuroimage, 82, 154-159. doi: 10.1016/j.neuroimage.2013.05.112 URL
[32]	Khoe, W., Mitchell, J. F., Reynolds, J. H., & Hillyard, S. A. ( 2005). Exogenous attentional selection of transparent superimposed surfaces modulates early event-related potentials. Vision Research, 45( 24), 3004-3014. doi: 10.1016/j.visres.2005.04.021 URL
[33]	Kok, P., Rahnev, D., Jehee, J. F. M., Lau, H. C., & De Lange, F. P..( 2012). Attention reverses the effect of prediction in silencing sensory signals. Cerebral Cortex, 22( 9), 2197-2206. doi: 10.1093/cercor/bhr310 URL
[34]	Lavie, N.( 1995). Perceptual load as a necessary condition for selective attention. Journal of Experimental Psychology Human Perception and Performance, 21( 3), 451-468. doi: 10.1037/0096-1523.21.3.451 URL
[35]	Lavie, N., & Tsal, Y.( 1994). Perceptual load as a major determinant of the locus of selection in visual-attention. Perception & Psychophysics, 56( 2), 183-197. doi: 10.3758/BF03213897 URL pmid: 7971119
[36]	Luck, S. J. ( 2005). The Design and interpretation of ERP experiments. In M. S. Gazzaniga (Eds) An introduction to the event-relatedpotential technique. (51-98). Massachusetts: MIT Press,.
[37]	Martínez, A., Anllo-Vento, L., Sereno, M. I., Frank, L. R., Buxton, R. B., Dubowitz, D. J., ... Hillyard, S. A. ( 1999). Involvement of striate and extrastriate visual cortical areas in spatial attention. Nature Neuroscience, 2, 364-369. doi: 10.1038/7274 URL
[38]	Martínez, A., DiRusso, F., Anllo-Vento, L., Sereno, M. I., Buxton, R. B., & Hillyard, S. A. ( 2001a). Putting spatial attention on the map: Timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Research, 41( 10-11), 1437-1457. doi: 10.1016/S0042-6989(00)00267-4 URL
[39]	Motter, B.C. ( 1993). Focal attention produces spatially seletive processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. Journal of Neurophysiology, 70( 3), 909-919. doi: 10.1152/jn.1993.70.3.909 URL
[40]	Müller, H.J., & Rabbitt, P. M.A . ( 1989). Reflexive and voluntary orienting of visual attention: Timecourse of activation and resistance to interruption. Journal of Experimental Psychology: Human Perception & Performance, 15( 2), 315-330.
[41]	Poghosyan, V., & Ioannides, A.A. ( 2008). Attention modulates earliest responses in the primary auditory and visual cortices. Neuron, 58( 5), 802-813. doi: 10.1016/j.neuron.2008.04.013 URL
[42]	Pourtois, G., Grandjean, D., Sander, D., & Vuilleumier, P. ( 2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14( 6), 619-633. doi: 10.1093/cercor/bhh023 URL
[43]	Rauss, K. S., Pourtois, G., Vuilleumier, P., & Schwartz, S. ( 2009). Attentional load modifies early activity in human primary visual cortex. Human Brain Mapping, 30( 5), 1723-1733. doi: 10.1002/hbm.v30:5 URL
[44]	Rauss, K. S., Pourtois, G., Vuilleumier, P., & Schwartz, S. ( 2012a). Effects of attentional load on early visual processing depend on stimulus timing. Human Brain Mapping, 33( 1), 63-74. doi: 10.1002/hbm.21193 URL
[45]	Rauss, K. S., Pourtois, G., Vuilleumier, P., & Schwartz, S. ( 2012b). Voluntary attention reliably influences visual processing at the level of the C1 component: A commentary on Fu, Fedota, Greenwood, and Parasuram (2010). Biological Psychology, 91( 2), 325-327. doi: 10.1016/j.biopsycho.2012.03.013 URL
[46]	Slagter, H. A., Alilovic, J., & Van Gaal, S. ( 2017). How early does attention modulate visual information processing? The importance of experimental protocol and data analysis approach. Cognitive Neuroscience, 9( 1-2), 26-28.
[47]	Slotnick, S.D. ( 2013). The nature of attentional modulation in V1. In S. Slotnick (Eds.), Controversies in Cognitive Neuroscience ( pp. 44-69). New York, NY:Palgrave Macmillan.
[48]	Slotnick, S.D. ( 2018). The experimental parameters that affect attentional modulation of the ERP C1 component. Cognitive Neuroscience, 9( 1-2), 53-62. doi: 10.1080/17588928.2017.1369021 URL
[49]	Stănişor, L., Van Der Togt, C., Pennartz, C. M. A., & Roelfsema, P. R. ( 2013). A unified selection signal for attention and reward in primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America, 110( 22), 9136-9141. doi: 10.1073/pnas.1300117110 URL
[50]	Sylvester, C. M., Shulman, G. L., Jack, A. I., & Corbetta, M. ( 2009). Anticipatory and stimulus-evoked blood oxygenation level-dependent modulations related to spatial attention reflect a common additive signal. The Journal of Neuroscience, 29( 34), 10671-10682. doi: 10.1523/JNEUROSCI.1141-09.2009 URL
[51]	Watanabe, M., Cheng, K., Murayama, Y., Ueno, K., Asamizuya, T., Tanaka, K., & Logothetis, N. ( 2011). Attention but not awareness modulates the BOLD signal in the human V1 during binocular suppression. Science, 334( 6057), 829-831. doi: 10.1126/science.1203161 URL
[52]	Woldorff, M. G., Fox, P. T., Matzke, M., Lancaster, J. L., Veeraswamy, S., Zamarripa, F., ... Jerabek, P. ( 1997). Retinotopic organization of early visual spatial attention effects as revealed by PET and ERPs. Human Brain Mapping, 5( 4), 280-286. doi: 10.1002/(SICI)1097-0193(1997)5:4<>1.0.CO;2-T URL
[53]	Zani, A., & Proverbio, A.M. ( 2003). Chapter 1 - Cognitive electrophysiology of mind and brain. Cognitive Electrophysiology of Mind & Brain, 3-12.
[54]	Zhang, X. L., Zhao, P. L., Zhou, T. G., & Fang, F. ( 2012). Neural activities in V1 create a bottom-up saliency map. Neuron, 73( 1), 183-192. doi: 10.1016/j.neuron.2011.10.035 URL pmid: 22243756
[55]	Zhu, X.R., & Luo, Y.J . ( 2012). Fearful faces evoke a larger C1 than happy faces in executive attention task: An event-related potential study. Neuroscience Letters, 526( 2), 118-121. doi: 10.1016/j.neulet.2012.08.011 URL