Skip to main content
SpringerLink
Log in

Effects of Stimulus Size and Contrast on the Initial Primary Visual Cortical Response in Humans

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

A Commentary to this article was published on 22 June 2017

Abstract

Decades of intracranial electrophysiological investigation into the primary visual cortex (V1) have produced many fundamental insights into the computations carried out in low-level visual circuits of the brain. Some of the most important work has been simply concerned with the precise measurement of neural response variations as a function of elementary stimulus attributes such as contrast and size. Surprisingly, such simple but fundamental characterization of V1 responses has not been carried out in human electrophysiology. Here we report such a detailed characterization for the initial “C1” component of the scalp-recorded visual evoked potential (VEP). The C1 is known to be dominantly generated by initial afferent activation in V1, but is difficult to record reliably due to interindividual anatomical variability. We used pattern-pulse multifocal VEP mapping to identify a stimulus position that activates the left lower calcarine bank in each individual, and afterwards measured robust negative C1s over posterior midline scalp to gratings presented sequentially at that location. We found clear and systematic increases in C1 peak amplitude and decreases in peak latency with increasing size as well as with increasing contrast. With a sample of 15 subjects and ~180 trials per condition, reliable C1 amplitudes of −0.46 µV were evoked at as low a contrast as 3.13% and as large as −4.82 µV at 100% contrast, using stimuli of 3.33° diameter. A practical implication is that by placing sufficiently-sized stimuli to target favorable calcarine cortical loci, robust V1 responses can be measured at contrasts close to perceptual thresholds, which could greatly facilitate principled studies of early visual perception and attention.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albrecht DG, Hamilton DB (1982) Striate cortex of monkey and cat: contrast response function. J Neurophysiol 48:217–237

    CAS  PubMed  Google Scholar 

  • Albrecht DG, Geisler WS, Frazor RA, Crane AM (2002) Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. J Neurophysiol 88:888–913

    PubMed  Google Scholar 

  • Ales JM, Yates JL, Norcia AM (2010) V1 is not uniquely identified by polarity reversals of responses to upper and lower visual field stimuli. Neuroimage 52:1401–1409. doi:10.1016/j.neuroimage.2010.05.016

    Article  PubMed  PubMed Central  Google Scholar 

  • Ales JM, Yates JL, Norcia AM (2013) On determining the intracranial 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

    Article  PubMed  Google Scholar 

  • Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K (2000) Brodmann’s areas 17 and 18 brought into stereotaxic space—where and how variable? Neuroimage 11:66–84

    Article  CAS  PubMed  Google Scholar 

  • Bao M, Yang L, Rios C, He B, Engel SA (2010) Perceptual learning increases the strength of the earliest signals in visual cortex. J Neurosci 30:15080–15084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baseler H, Sutter E, Klein S, Carney T (1994) The topography of visual evoked response properties across the visual field. Electroencephalogr Clin Neurophysiol 90:65–81

    Article  CAS  PubMed  Google Scholar 

  • Buracas GT, Boynton GM (2002) Efficient design of event-related fMRI experiments using M-sequences. Neuroimage 16:801–813

    Article  PubMed  Google Scholar 

  • Carandini M, Heeger DJ (2012) Normalization as a canonical neural computation. Nat Rev Neurosci 13:51–62. doi:10.1038/nrn3136

    Article  CAS  Google Scholar 

  • Carandini M et al (2005) Do we know what the early visual system does? J Neurosci 25:10577–10597. doi:10.1523/JNEUROSCI.3726-05.2005

    Article  CAS  PubMed  Google Scholar 

  • Cavanaugh JR, Bair W, Movshon JA (2002) Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J Neurophysiol 88:2530–2546. doi:10.1152/jn.00692.2001

    Article  PubMed  Google Scholar 

  • Clark VP, Hillyard SA (1996) Spatial selective attention affects early extrastriate but not striate components of the visual evoked potential. J Cogn Neurosci 8:387–402

    Article  CAS  PubMed  Google Scholar 

  • Clark VP, Fan S, Hillyard SA (1995) Identification of early visual evoked potential generators by retinotopic and topographic analyses. Hum Brain Mapp 2:170–187

    Article  Google Scholar 

  • DeAngelis GC, Freeman RD, Ohzawa I (1994) Length and width tuning of neurons in the cat’s primary visual cortex. J Neurophysiol 71:347–374

    CAS  PubMed  Google Scholar 

  • Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. doi:10.1016/j.jneumeth.2003.10.009

    Article  PubMed  Google Scholar 

  • Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA (2002) Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp 15:95–111

    Article  PubMed  Google Scholar 

  • Foxe JJ, Simpson GV (2002) Flow of activation from V1 to frontal cortex in humans. A framework for defining “early” visual processing. Exp Brain Res 142:139–150. doi:10.1007/s00221-001-0906-7

    Article  PubMed  Google Scholar 

  • Foxe JJ, Strugstad EC, Sehatpour P, Molholm S, Pasieka W, Schroeder CE, McCourt ME (2008) Parvocellular and magnocellular contributions to the initial generators of the visual evoked potential: high-density electrical mapping of the “C1” component. Brain Topogr 21:11–21

    Article  PubMed  Google Scholar 

  • Fu S, Huang Y, Luo Y, Wang Y, Fedota J, Greenwood PM, Parasuraman R (2009) Perceptual load interacts with involuntary attention at early processing stages: event-related potential studies. Neuroimage 48:191–199

    Article  PubMed  PubMed Central  Google Scholar 

  • Gawne TJ, Kjaer TW, Richmond BJ (1996) Latency: another potential code for feature binding in striate cortex. J Neurophysiol 76:1356–1360

    CAS  PubMed  Google Scholar 

  • Hagler DJ Jr, Halgren E, Martinez A, Huang M, Hillyard SA, Dale AM (2009) Source estimates for MEG/EEG visual evoked responses constrained by multiple, retinotopically-mapped stimulus locations. Hum Brain Mapp 30:1290–1309. doi:10.1002/hbm.20597

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagler DJ Jr (2014) Optimization of retinotopy constrained source estimation constrained by prior. Hum Brain Mapp 35:1815–1833. doi:10.1002/hbm.22293

    Article  PubMed  Google Scholar 

  • Hansen BC, Haun AM, Johnson AP, Ellemberg D (2016) On the Differentiation of foveal and peripheral early visual evoked potentials. Brain Topogr 29:506–514. doi:10.1007/s10548-016-0475-5

    Article  PubMed  Google Scholar 

  • Hu M, Wang Y (2011) Rapid dynamics of contrast responses in the cat primary visual cortex. PLoS ONE 6:e25410. doi:10.1371/journal.pone.0025410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubel DH, Wiesel TN (1959) Receptive fields of single neurones in the cat’s striate cortex. J Physiol 148:574–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itthipuripat S, Ester EF, Deering S, Serences JT (2014) Sensory gain outperforms efficient readout mechanisms in predicting attention-related improvements in behavior. J Neurosci 34:13384–13398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James AC (2003) The pattern-pulse multifocal visual evoked potential. Invest Ophthalmol Vis Sci 44:879–890

    Article  PubMed  Google Scholar 

  • Jeffreys DA, Axford JG (1972) Source locations of pattern-specific components of human visual evoked potentials. I. Component of striate cortical origin. Exp Brain Res 16:1–21

    CAS  PubMed  Google Scholar 

  • Jones R, Keck MJ (1978) Visual evoked response as a function of grating spatial frequency. Invest Ophthalmol Vis Sci 17:652–659

    CAS  PubMed  Google Scholar 

  • Kelly SP, Gomez-Ramirez M, Foxe JJ (2008) Spatial attention modulates initial afferent activity in human primary visual cortex. Cereb Cortex 18:2629–2636. doi:10.1093/cercor/bhn022

    Article  PubMed  PubMed Central  Google Scholar 

  • Kelly SP, Schroeder CE, Lalor EC (2013a) What does polarity inversion of extrastriate activity tell us about striate contributions to the early VEP? A comment on Ales et al. (2010). Neuroimage 76:442–445. doi:10.1016/j.neuroimage.2012.03.081

    Article  PubMed  Google Scholar 

  • Kelly SP, Vanegas IM, Schroeder CE, Lalor EC (2013b) 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Martínez A et al (1999) Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 2:364–369. doi:10.1038/7274

    Article  PubMed  Google Scholar 

  • Mihaylova M, Stomonyakov V, Vassilev A (1999) Peripheral and central delay in processing high spatial frequencies: reaction time and VEP latency studies. Vision Res 39:699–705

    Article  CAS  PubMed  Google Scholar 

  • Miller J, Ulrich R, Schwarz W (2009) Why jackknifing yields good latency estimates. Psychophysiology 46:300–312. doi:10.1111/j.1469-8986.2008.00761.x

    Article  PubMed  Google Scholar 

  • Ohtani Y, Okamura S, Yoshida Y, Toyama K, Ejima Y (2002) Surround suppression in the human visual cortex: an analysis using magnetoencephalography. Vision Res 42:1825–1835

    Article  PubMed  Google Scholar 

  • Oram MW, Xiao D, Dritschel B, Payne KR (2002) The temporal resolution of neural codes: does response latency have a unique role? Philos Trans R Soc Lond B 357:987–1001. doi:10.1098/rstb.2002.1113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker DM, Salzen EA, Lishman JR (1982) Visual-evoked responses elicited by the onset and offset of sinusoidal gratings: latency, waveform, and topographic characteristics. Invest Ophthalmol Vis Sci 22:675–680

    CAS  PubMed  Google Scholar 

  • Pourtois G, Rauss KS, Vuilleumier P, Schwartz S (2008) Effects of perceptual learning on primary visual cortex activity in humans. Vision Res 48:55–62

    Article  PubMed  Google Scholar 

  • Rademacher J, Caviness VS Jr, Steinmetz H, Galaburda AM (1993) Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. Cereb Cortex 3:313–329

    Article  CAS  PubMed  Google Scholar 

  • Rauss KS, Pourtois G, Vuilleumier P, Schwartz S (2009) Attentional load modifies early activity in human primary visual cortex. Hum Brain Mapp 30:1723–1733. doi:10.1002/hbm.20636

    Article  PubMed  Google Scholar 

  • Rauss K, Schwartz S, Pourtois G (2011) Top-down effects on early visual processing in humans: a predictive coding framework. Neurosci Biobehav Rev 35:1237–1253

    Article  PubMed  Google Scholar 

  • Rebai M, Bernard C, Lannou J, Jouen F (1998) Spatial frequency and right hemisphere: an electrophysiological investigation. Brain Cogn 36:21–29

    Article  CAS  PubMed  Google Scholar 

  • Reich DS, Mechler F, Victor JD (2001) Temporal coding of contrast in primary visual cortex: when, what, and why. J Neurophysiol 85:1039–1050

    CAS  PubMed  Google Scholar 

  • Sceniak MP, Hawken MJ, Shapley R (2001) Visual spatial characterization of macaque V1 neurons. J Neurophysiol 85:1873–1887

    CAS  PubMed  Google Scholar 

  • Sclar G, Maunsell JH, Lennie P (1990) Coding of image contrast in central visual pathways of the macaque monkey. Vision Res 30:1–10

    Article  CAS  PubMed  Google Scholar 

  • Sit YF, Chen Y, Geisler WS, Miikkulainen R, Seidemann E (2009) Complex dynamics of V1 population responses explained by a simple gain-control model. Neuron 64:943–956. doi:10.1016/j.neuron.2009.08.041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stensaas SS, Eddington DK, Dobelle WH (1974) The topography and variability of the primary visual cortex in man. J Neurosurg 40:747–755

    Article  CAS  PubMed  Google Scholar 

  • Vanegas MI, Blangero A, Kelly SP (2013) Exploiting individual primary visual cortex geometry to boost steady state visual evoked potentials. J Neural Eng 10:036003

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanegas MI, Blangero A, Kelly SP (2015) Electrophysiological indices of surround suppression in humans. J Neurophysiol 113:1100–1109

    Article  PubMed  Google Scholar 

  • Vassilev A, Manahilov V, Mitov D (1983) Spatial frequency and the pattern onset-offset response. Vision Res 23:1417–1422

    Article  CAS  PubMed  Google Scholar 

  • Vassilev A, Mihaylova M, Bonnet C (2002) On the delay in processing high spatial frequency visual information: reaction time and VEP latency study of the effect of local intensity of stimulation. Vision Res 42:851–864

    Article  PubMed  Google Scholar 

  • Wandell BA (1995) Foundations of vision. Sinauer Associates, Incorporated, Sunderland. doi:10.1002/col.5080210213

    Google Scholar 

  • Wandell BA, Dumoulin SO, Brewer AA (2009) Visual cortex in humans. In: Encyclopedia of neuroscience, vol 10. Elsevier, Amsterdam, pp 251–257. doi:10.1016/B978-008045046-9.00241-2

    Chapter  Google Scholar 

  • Wang F et al (2016) Predicting perceptual learning from higher-order cortical processing. Neuroimage 124:682–692. doi:10.1016/j.neuroimage.2015.09.024

    Article  PubMed  Google Scholar 

  • Widmann A, Schroger E (2012) Filter effects and filter artifacts in the analysis of electrophysiological data. Front Psychol 3:233 doi:10.3389/fpsyg.2012.00233

    PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhaoping L, Zhou T, Fang F (2012) Neural activities in V1 create a bottom-up saliency map. Neuron 73:183–192

    Article  CAS  PubMed  Google Scholar 

  • Zhang GL, Li H, Song Y, Yu C (2015) ERP C1 is top-down modulated by orientation perceptual learning. J Vis 15:8. doi:10.1167/15.10.8

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Azeezat Azeez and Annabelle Blangero for helpful discussions at the outset of the project. This research was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number SC2GM099626.

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, The City College of the City University of New York, New York, NY, USA

    Nigel Gebodh, M. Isabel Vanegas & Simon P. Kelly

  2. School of Electrical and Electronic Engineering, University College Dublin, Dublin 4, Belfield, Ireland

    Simon P. Kelly

Authors
  1. Nigel Gebodh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Isabel Vanegas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simon P. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simon P. Kelly.

Ethics declarations

Conflict of interest

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gebodh, N., Vanegas, M.I. & Kelly, S.P. Effects of Stimulus Size and Contrast on the Initial Primary Visual Cortical Response in Humans. Brain Topogr 30, 450–460 (2017). https://doi.org/10.1007/s10548-016-0530-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-016-0530-2

Keywords

Search

Navigation