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Cortical Sources of the Early Components of the Visual Evoked

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Cortical Sources of the Early Components of the Visual Evoked ᭜HumanBrainMapping15:95–111(2001)᭜ CorticalSourcesoftheEarlyComponentsofthe VisualEvokedPotential FrancescoDiRusso,1,2* Ant´ı gonaMart´ı nez,1 MartinI.Sereno,3 SabrinaPitzalis,2,3 andStevenA.Hillyard1 1DepartmentofNeurosciences,UCSD,LaJolla,California 2FondazioneClinicaSantaLucia,IRCCS,Rome,Italy 3DepartmentofCognitiveSciences,UCSD,LaJolla,California ᭜ ᭜ Abstract:Thisstudyaimedtocharacterizetheneuralgeneratorsoftheearlycomponentsofthevisual evokedpotential(VEP)toisoluminantcheckerboardstimuli.Multichannelscalprecordings,retinotopic mappinganddipolemodelingtechniqueswereusedtoestimatethelocationsofthecorticalsources givingrisetotheearlyC1,P1,andN1components.Dipolelocationswerematchedtoanatomicalbrain regionsvisualizedinstructuralmagneticresonanceimaging(MRI)andtofunctionalMRI(fMRI)activa- tionselicitedbythesamestimuli.TheseconvergingmethodsconfirmedpreviousreportsthattheC1 component(onsetlatency55msec;peaklatency90–92msec)wasgeneratedintheprimaryvisualarea (striatecortex;area17).TheearlyphaseoftheP1component(onsetlatency72–80msec;peaklatency 98–110msec)waslocalizedtosourcesindorsalextrastriatecortexofthemiddleoccipitalgyrus,whilethe latephaseoftheP1component(onsetlatency110–120msec;peaklatency136–146msec)waslocalized toventralextrastriatecortexofthefusiformgyrus.AmongtheN1subcomponents,theposteriorN150 couldbeaccountedforbythesamedipolarsourceastheearlyP1,whiletheanteriorN155waslocalized toadeepsourceintheparietallobe.ThesefindingsclarifytheanatomicaloriginoftheseVEPcomponents, whichhavebeenstudiedextensivelyinrelationtovisual-perceptualprocesses.Hum.BrainMapping15: 95–111,2001. ©2001Wiley-Liss,Inc. Keywords:VEP;dipoles;MRI;fMRI;retinotopicmapping;V1;ERP;C1;co-registration ᭜ ᭜ INTRODUCTION fromprimaryvisualcortex(Brodmann’sarea17,stri- atecortex).Severalauthors,however,havequestioned Theneuralgeneratorsoftheearlycomponentsof thisproposalandconcludedthattheC1arisesfrom thepattern-onsetvisualevokedpotential(VEP)are extrastriateareas18or19.TableIliststheconclusions notfullyunderstood.Sincetheoriginalobservations ofpreviousstudiesregardingthegeneratorsoftheC1 ofJeffreysandAxford(1972a),manystudieshave component.EvidencethatC1isgeneratedinthestri- obtainedevidencethatthefirstmajorVEPcomponent atecortexwithinthecalcarinefissurecomesfrom (C1),withanonsetlatencybetween40and70msec studiesshowingthattheC1reversesinpolarityfor andpeaklatencybetween60and100msec,originates uppervs.lowervisual-fieldstimulation(e.g.,Jeffreys andAxford,1972a,b;Butleretal.,1987;Clarketal., *Correspondenceto:Dr.FrancescoDiRusso,Dept.ofNeuro- 1995;Mangun,1995).Thisreversalcorrespondstothe sciences(0608),9500GilmanDrive,LaJollaCA,92093-0608. retinotopicorganizationofthestriatecortex,inwhich E-mail:[email protected] theloweranduppervisualhemifieldsaremappedin Receivedforpublication27June2001;accepted11September2001 theupperandlowerbanksofthecalcarinefissure, PublishedonlinexxMonth2001 DOI10.1002/hbm.10010 ©2001Wiley-Liss,Inc. ᭜ Di Russo et al. ᭜ TABLE I. Conclusions of previous studies regarding the differences such as number of recording sites and type cortical visual areas that generate the first (C1) and of stimuli used. In particular, a sparse electrode array second (C2/P1) component of pattern-onset VEP may not able to differentiate concurrent activities in Authors C1 C2/P1 neighboring visual areas nor obtain an accurate pic- ture of the voltage topography produced by a given Jeffreys and Axford, 1972a,b 17 18 source. Furthermore, the use of relatively large stimuli Biersdorf, 1974 17 17 extending over wide visual angles in some studies Lesevre and Joseph, 1979 19 18 might have activated widespread cortical areas, Darcey and Arj, 1980 17 17 or 18 thereby reducing the possibility of identifying the ex- Kriss and Halliday, 1980 17 act generator locations. Finally, individual differences Lesevre, 1982 17 18 in the position and extent of the striate cortex with Parker et al., 1982 17 respect to the calcarine fissure (Rademacher et al., Butler et al., 1987 17 Maier et al., 1987 18 or 19 17 and 18 1993) might have lead to variation among subjects in Srebro, 1987 17 VEP topography. Edwards and Drasdo, 1987 18 The point of departure for the present research is Ossenblok and Spekreijse, 1991 18 19 the study of Clark et al. (1995), which used dipole Bodis-Wollner et al., 1992 17 modeling to localize the C1 component to the striate Manahilov, et al., 1992 17 19 cortex and the P1 component to extrastriate areas 18/ Mangun et al., 1993 17 18 and 19 19. Clark et al. (1995) observed systematic changes in Gomez Gonzalez, et al., 1994 17 18 and 19 the orientation of the dipole corresponding to the C1 Clark et al., 1995 17 18 and 19 as function of stimulus polar angle (elevation) in the Mangun, 1995 17 18 and 19 Clark and Hillyard, 1996 17 18 and 18 visual field that were in good agreement with the Miniussi et al., 1998 17 18 or 19 cruciform model. For stimuli in the lower visual field, Martinez et al., 1999 17 18 and 19 however, they found it difficult to separate the voltage Martinez et al., 2001a,b 17 18 and 19 topography of the surface-positive C1 from that of overlapping P1, perhaps due to the limited mapping resolution achieved with only a 32-channel recording respectively. According to this “cruciform model” (Jef- array. Accordingly, Clark et al. (1995) found it neces- freys and Axford, 1972a), stimulation above and be- sary to constrain the position of the C1 and P1 dipoles low the horizontal meridian of the visual field should to observe the retinotopic polarity inversion of the C1. activate neural populations with geometrically oppo- site orientations and hence elicit surface-recorded The purpose of the present study was to separate evoked potentials of opposite polarity. Such a pattern the early C1 and P1 components and test their retino- would not be observed for VEPs generated in other topic properties with greater precision by using a visual areas that lack the special retinotopic organiza- denser electrode array (64-channels recordings) and tion of the calcarine cortex, although it cannot be dipole modeling with no position constraints. In ad- excluded that some degree of polarity shift for upper dition, the VEP sources localized by the dipole mod- versus lower field stimuli might be present for neural eling were projected onto anatomical MRI sections generators in V2 and V3 as well (Schroeder et al., 1995; and then compared to loci of cortical activations re- Simpson et al., 1994, 1995). vealed by fMRI in response to the same stimuli. The The second VEP component is a positivity termed stimuli used were flashed checkerboard patterns of P1 (called C2 by Jeffreys) with an onset latency be- relatively high spatial frequency to evoke a large C1 tween 65 and 80 msec and a peak latency of around component (e.g., Martı´nez et al., 2001b; Rebaı¨ et al., 100 and 130 msec. There is evidence that this compo- 1998). The stimuli were presented asymmetrically in nent, which does not show a polarity reversal for the upper and lower quadrants of the visual fields to upper vs. lower visual-field stimulation (Clark et al., verify the polarity reversal of the C1 in light of evi- 1995; Mangun, 1995), is mainly generated in extrastri- dence that the reversal point is not exactly at the ate visual areas, although no clear consensus has yet horizontal meridian but rather at 10–20° (polar angle) been reached regarding the exact location of its below it (Aine et al., 1996; Clark et al., 1995). Thus, the sources (see Table I). overall goal was to determine the component struc- This lack of agreement among previous studies may ture and source localization of the early (60–160 msec) be due to the low spatial resolution of the electrophys- VEP using combined electrophysiology and fMRI iological techniques employed and to methodological techniques. ᭜ 96 ᭜ ᭜ Cortical Sources of VEP ᭜ zones of the lower and upper banks of the calcarine fissure, respectively, based on findings that the hori- zontal meridian its actually represented on the lower bank rather than at the lateral recess of the calcarine fissure (Aine et al., 1996; Clark et al., 1995). In the fMRI experiment the same stimuli were pre- sented at the same locations and rate, but the stimuli were delivered in 20-sec blocks to one quadrant a time instead of in random order. Procedure In the VEP experiment, the subject was comfortably seated in a dimly lit sound-attenuated and electrically Figure 1. shielded room while stimuli were presented on a Stimuli used in this experiment. Circular sinusoidal checkerboards video monitor at a viewing distance of 70 cm. Subjects were flashed one at time in random order to the four locations. were trained to maintain stable fixation on a central dot (0.2°) throughout stimulus presentation. Each run lasted 100 sec followed by a 30 sec rest, with longer MATERIALS AND METHODS breaks interspersed. A total of 24 runs were carried out to deliver 1,400 stimuli to each quadrant. To main- Subjects tain alertness during stimulation, in both the VEP and fMRI experiments subjects were required to press a Twenty-three paid volunteer subjects (12 female, button upon detection of an infrequent and difficult to mean age 26.1, range 18–36 years) participated in the detect brightness change of the fixation dot. The sub- VEP recordings. A subset of 13 of these subjects (8 jects were given feedback on their behavioral perfor- female, mean age 26.8 range 23–35 years) additionally mance and their ability to sustain fixation. The fMRI received anatomical MRI scans. Of the latter group, a experiment consisted of five runs of 6 min each,
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