Abstract
The C1 component of the VEP is considered to index initial afference of retinotopic regions of human visual cortex (V1 and V2). C1 onsets over central parieto–occipital scalp between 45 and 60 ms, peaks between 70 and 100 ms, and then resolves into the following P1 component. By exploiting isoluminant and low-contrast luminance stimuli, we assessed the relative contributions of the Magnocellular (M) and Parvocellular (P) pathways to generation of C1. C1 was maximal at 88 ms in a 100% luminance contrast condition (which stimulates both P and M pathways) and at 115 ms in an isoluminant chromatic condition (which isolates contributions of the P pathway). However, in a 4% luminance contrast condition (which isolates the M pathway), where the stimuli were still clearly perceived, C1 was completely absent. Absence of C1 in this low contrast condition is unlikely to be attributable to lack of stimulus energy since a robust P1–N1 complex was evoked. These data therefore imply that C1 may be primarily parvocellular in origin. The data do not, however, rule out some contribution from the M system at higher contrast levels. Nonetheless, that the amplitude of C1 to P-isolating isoluminant chromatic stimuli is equivalent to that evoked by 100% contrast stimuli suggests that even at high contrast levels, the P system is the largest contributor. These data are related to intracranial recordings in macaque monkeys that have also suggested that the initial current sink in layer IV may not propagate effectively to the scalp surface when M-biased stimuli are used. We also discuss how this finding has implications for a long tradition of attention research that has␣used C1 as a metric of initial V1 afference in humans. C1 has been repeatedly interrogated for potential selective attentional modulations, particularly in spatial attentional designs, under the premise that modulation of this component, or lack thereof, would be evidence for or against selection at the initial inputs to visual cortex. Given the findings here, we would urge that in interpreting C1 effects, a consideration of the dominant cellular contributions will be necessary. For example, it is plausible that spatial attention mechanisms could operate primarily through the M system and that as such C1 may not always represent an adequate dependent measure in such studies.
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References
Broadbent DE (1958) Perception and communication. Pergamon, London
Butler PD, Schechter I, Zemon V, Schwartz SG, Greenstein VC, Gordon J, Schroeder CE, Javitt DC (2001) Dysfunction of early-stage visual processing in schizophrenia. Am J Psychiatry 158(7):1126–1133
Butler PD, Martinez A, Foxe JJ, Kim D, Zemon V, Silipo G, Mahoney J, Shpaner M, Jalbrzikowski M, Javitt DC (2007) Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. Brain 130(Pt 2):417–430
Calkins DJ, Sterling P (1999) Evidence that circuits for spatial and color vision segregate at the first retinal synapse. Neuron 24:313–321
Chatterjee S, Callaway EM (2003) Parallel colour-opponent pathways to primary visual cortex. Nature 426:668–671
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
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
Coull JT, Nobre AC (1998) Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. J Neurosci 18(18):7426–7435
Dale CL, Simpson GV, Foxe JJ, Luks TL, Worden MS (2008) ERP correlates of anticipatory attention: spatial and non-spatial specificity and relation to subsequent selective attention. Exp Brain Res 188:45–62
Derrington AM, Lennie P (1984) Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol 357:219–240
Deutsch JA, Deutsch D (1963) Attention: some theoretical considerations. Psychol Rev 70:80–90
Di Russo F, Martínez 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
Di Russo F, Martinez A, Hillyard SA (2003) Source analysis of event-related cortical activity during visuo-spatial attention. Cereb Cortex 13(5):486–499
Driver J (2001) A selective review of selective attention research from the past century. Br J Psychol 92(I):53–78
Driver J, Tipper SP (1989) On the nonselectivity of “selective” seeing: contrasts between interference and priming in selective attention. JEP: HPP 15:304–314
Ellemberg D, Hammarrenger B, Lepore F, Roy MS, Guillemot JP (2001) Contrast dependency of VEPs as a function of spatial frequency: the parvocellular and magnocellular contributions to human VEPs. Spat Vis 15(1):99–111
Foxe JJ, Schroeder CE (2005) The case for feedforward multisensory convergence during early cortical processing. NeuroReport 16:419–423
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 142:39–150
Foxe JJ, Simpson GV (2005) Biasing the brain’s attentional set. II. Effects of selective intersensory attentional deployments on subsequent sensory processing. Exp Brain Res 166:393–401
Foxe JJ, Simpson GV, Ahlfors SP (1998) Parieto–occipital 10 Hz activity reflects anticipatory state of visual attention mechanisms. NeuroReport 9:3929–3933
Foxe JJ, Doniger GM, Javitt DC (2001) Visual processing deficits in schizophrenia: impaired P1 generation revealed by high-density electrical mapping. NeuroReport 12(17):3815–3820
Foxe JJ, McCourt ME, Javitt DC (2003) Right hemisphere control of visuo-spatial attention: ‹Line-bisection’ judgments evaluated with high-density electrical mapping and source-analysis. NeuroImage 19:710–726
Foxe JJ, Murray MM, Javitt DC (2005a) Filling-in in schizophrenia: a high-density electrical mapping and source-analysis investigation of illusory contour processing. Cereb Cortex 15:1914–1927
Foxe JJ, Simpson GV, Ahlfors SP, Saron CD (2005b) Biasing the brain’s attentional set. I. Cue driven deployments of intersensory selective attention. Exp Brain Res 166:370–392
Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Kim YH, Meyer JR, Mesulam M (1999) A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain 122(Pt 6):1093–1106
Givre SJ, Schroeder CE, Arezzo JC (1994) Contribution of extrastriate area V4 to the surface-recorded flash VEP in the awake macaque. Vision Res 34(4):415–428
Givre SJ, Arezzo JC, Schroeder CE (1995) Effects of wavelength on the timing and laminar distribution of illuminance-evoked activity in macaque V1. Vis Neurosci 12(2):229–239
Gomez-Gonzalez CM, Clark VP, Fan S, Luck SJ, Hillyard SA (1994) Sources of attention-sensitive visual event-related potentials. Brain Topogr 7:41–51
Guthrie D, Buchwald JS (1991) Significance testing of difference potentials. Psychophysiology 28(2):240–244
Hall SD, Holliday IE, Hillebrand A, Furlong PL, Singh KD, Barnes GR (2005) Distinct contrast response functions in striate and extra-striate regions of visual cortex revealed with magnetoencephalography (MEG). Clin Neurophysiol 116:1716–1722
Heilman KM, Van Den Abell T (1980) Right hemisphere dominance for attention: the mechanism underlying hemispheric asymmetries of inattention (neglect). Neurology 30:327–330
Hillyard SA, Anllo-Vento L (1998) Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci 95: 781–787
Hillyard SA, Vogel EK, Luck SJ (1998) Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. Philos Trans R Soc Lond B Biol Sci 353:1257–1270
Hubel DH, Livingstone MS (1990) Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey. J Neurosci 10(7):2223–2237
Ikeda H, Nishijo H, Miyamoto K, Tamura R, Endo S, Ono T (1998) Generators of visual evoked potentials investigated by dipole tracing in the human occipital cortex. Neuroscience 84:723–739
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
Kaiser PK (1979) Spectral sensitivity function measured by a rapid scan flicker photometric procedure. Invest Ophthalmol Vis Sci 18:1264–1272
Kaplan E (1991) The receptive field structure of retinal ganglion cells in cat and monkey. In: Cronly-Dillon J (ed) Vision and visual dysfunction, vol 4, AG Leventhal: the neural basis of visual function. CRC Press, Boca Raton, Florida, pp 10–40
Kaplan E, Shapley RM (1986) The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc Natl Acad Sci USA 83(8):2755–2757
Kelly SP, Gomez-Ramirez M, Foxe JJ (in press) Spatial attention modulates initial afferent activity in human primary visual cortex. Cerebral Cortex Advance Access published on March 4, 2008. doi:10.1093/cercor/bhn022
Kubová Z, Kuba M, Spekreijse H, Blakemore C (1995) Contrast dependence of motion-onset and pattern-reversal evoked potentials. Vision Res 35:197–205
Lachter J, Forster KI, Ruthruff E (2004) Forty-five years after Broadbent (1958): still no identification without attention. Psychol Rev 111(4):880–913
Lalor EC, Foxe JJ (in press) Biasing responsivity of the magnocellular and parvocellular visual pathways using the Visual Evoked Spread Spectrum Analysis technique (VESPA). Vision Res
Lalor EC, Pearlmutter BA, Reilly RB, McDarby G, Foxe JJ (2006) The VESPA: a method for the rapid estimation of a visual evoked potential. Neuroimage 32:1549–1561
Lalor EC, Kelly SP, Pearlmutter B, Reilly RB, Foxe JJ (2007) Isolating endogenous visuo-spatial attentional effects using the novel Visual Evoked Spread Spectrum Analysis (VESPA) technique. Eur J NeuroSci 26:3536–3542
Lalor EC, Yeap S, Reilly RB, Pearlmutter BA, Foxe JJ (2008) Dissecting the cellular contributions to early visual sensory processing deficits in schizophrenia using the VESPA evoked response. Schizophr Res 98:256–264
Livingstone M, Hubel D (1988) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240(4853):740–749
Livingstone MS, Rosen GD, Drislane FW, Galaburda AM (1991) Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proc Natl Acad Sci 88(18): 7943–7947
Mangun GR, Hinrichs H, Scholz M, Mueller-Gaertner HW, Herzog H, Krause BJ, Tellman L, Kemna L, Heinze HJ (2001) Integrating electrophysiology and neuroimaging of spatial selective attention to simple isolated visual stimuli. Vision Res 41(10–11):1423–1435
Martinez A, Anllo-Vento L, Sereno MI, Frank LR, Buxton RB, Dubowitz DJ, Wong EC, Hinrichs H, Heinze HJ, Hillyard SA (1999) Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 2:364–369
Martinez A, DiRusso F, Anllo-Vento L, Sereno MI, Buxton RB, Hillyard SA (2001) Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Res 41(10–11):1437–1457
Maunsell JHR, Ghose GM, Assad JA, McAdams CJ, Boudreau CE, Noerager BD (1999) Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys. Vis Neurosci 16:1–14
McCourt ME, Foxe JJ (2004) Brightening prospects for “early” cortical coding of perceived luminance. NeuroReport 15:49–56
Merigan WH (1989) Chromatic and achromatic vision of macaques: role of the P pathway. J Neurosci 9(3):776–783
Merigan WH, Maunsell JR (1993) How parallel are the primate visual pathways? Annual Rev Neurosci 16:369–402
Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ (2002) Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Cogn Brain Res 14:121–134
Noesselt T, Hillyard SA, Woldorff MG, Schoenfeld A, Hagner T, Jancke L, Tempelmann C, Hinrichs H, Heinze HJ (2002) Delayed striate cortical activation during spatial attention. Neuron 35(3):575–587
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Perrin F, Pernier J, Bertrand O, Giard MH, Echallier JF (1987) Mapping of scalp potentials by surface spline interpolation. Electroencephalogr Clin Neurophysiol 66(1):75–81
Schechter I, Butler PD, Zemon VM, Revheim N, Saperstein AM, Jalbrzikowski M, Pasternak R, Silipo G, Javitt DC (2005) Impairments in generation of early-stage transient visual evoked potentials to magno- and parvocellular-selective stimuli in schizophrenia. Clin Neurophysiol 116(9):2204–2215
Schroeder CE, Tenke CE, Arezzo JC, Vaughan HG Jr (1989) Timing and distribution of flash-evoked activity in the lateral geniculate nucleus of the alert monkey. Brain Res 477(1–2):183–195
Schroeder CE, Tenke CE, Givre SJ, Arezzo JC, Vaughan HG Jr (1991) Striate cortical contribution to the surface-recorded pattern-reversal VEP in the alert monkey. Vision Res 31(7–8): 1143–1157
Schroeder CE, Javitt DC, Steinschneider M, Mehta AD, Givre SJ, Vaughan HG Jr, Arezzo JC (1997) N-methyl-D-aspartate enhancement of phasic responses in primate neocortex. Exp Brain Res 114(2):271–278
Schroeder CE, Mehta AD, Givre SJ (1998) A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. Cereb Cortex 8:575–592
Schroeder CE, Mehta AD, Foxe JJ (2001) Determinants and mechanisms of attentional modulation of neural processing. Front Biosci 6:D672–D684
Schwartz BD, Tomlin HR, Evans WJ, Ross KV (2001) Neurophysiologic mechanisms of attention: a selective review of early information processing in schizophrenics. Front Biosci 6:D120–D134
Shapley R, Kaplan E, Soodak R (1981) Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292(5823):543–545
Simpson GV, Pfleiger ME, Foxe JJ, Ahlfors SP, Vaughan HG Jr, Hrabe J, Ilmoniemi RJ, Lantos G (1995a) Dynamic neuroimaging of brain function. J Clin Neurophysiol 12(5):1–18
Simpson GV, Foxe JJ, Vaughan HG Jr, Mehta AD, Schroeder CE (1995b) Integration of electrophysiological source analyses, MRI and animal models in the study of visual processing and attention. Electroencephalogr Clin Neurophysiol Suppl 44:76–92
Tenke CE, Schroeder CE, Arezzo JC, Vaughan HG Jr (1993) Interpretation of high-resolution current source density profiles: a simulation of sublaminar contributions to the visual evoked potential. Exp Brain Res 94(2):183–192
Tootell RB, Switkes E, Silverman MS, Hamilton SL (1988a) Functional anatomy of macaque striate cortex. II. Retinotopic organization. J Neurosci 8:1531–1568
Tootell RB, Hamilton SL, Switkes E (1988b) Functional anatomy of macaque striate cortex. IV. Contrast and magno-parvo streams. J␣Neurosci 8(5):1594–609
Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW (1995) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15(4):3215–3230
Tootell RB, Hadjikhani NK, Vanduffel W, Liu AK, Mendola JD, Sereno MI, Dale AM (1998) Functional analysis of primary visual cortex (V1) in humans. Proc Natl Acad Sci USA 95(3): 811–817
Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT Press, Cambridge, MA, pp 549–585
Vallar G, Perani D (1986) The anatomy of unilateral neglect after right-hemisphere stroke lesions: a clinical/CT-scan correlation study in man. Neuropsychologia 24:609–622
Vallar G, Perani D (1987) The anatomy of spatial neglect in humans. In Jennerod (ed) Neurophysiological and neuropsychological aspects of spatial neglect. North Holland, Amsterdam, pp 235–258
Van Essen DC, Maunsell JHR (1983) Hierarchical organization and functional streams in the visual cortex. Trends Neurosci 6:370–375
Yeap S, Kelly SP, Sehatpour P, Magno E, Javitt DC, Garavan H, Thakore JH, Foxe JJ (2006) Early visual sensory deficits as endophenotypes for Schizophrenia: high-density electrical mapping in clinically unaffected first-degree relatives. Arch Gen Psychiatry 63:1180–1188
Acknowledgements
We would like to thank Dr. Vance Zemon, Dr.␣Barbara Blakeslee and Dr. Simon Kelly for very helpful discussions. We would like to especially thank Ms. Jeannette Mahoney, Ms. Marina Shpaner and Ms. Beth Higgins for their expert data collection. We would also like to acknowledge the passing of our friend and colleague, Brian “Wren” Pasieka, who is sorely missed. This work was supported by an NIMH RO1 grant to JJF (MH65350) and MEM received support from NCRR grant P20 RR020151.
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Foxe, J.J., Strugstad, E.C., Sehatpour, P. et al. 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 (2008). https://doi.org/10.1007/s10548-008-0063-4
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DOI: https://doi.org/10.1007/s10548-008-0063-4