Identification of the neural sources of the pattern-reversal VEP
Introduction
Studies of transient visual-evoked potentials (VEPs) in humans have used stimulus patterns presented briefly in on–off mode (pattern onset) as well as counterphase shifts of gratings or checkerboards (pattern reversal). Pattern-onset VEPs are characterized by an initial component at 70–90 ms after stimulus onset (the C1 component) that varies in polarity according to stimulus position, followed by a positive wave at 100–130 ms (P1 component) and a negative wave complex at 140–190 ms (N1 component). Conflicting proposals have been advanced regarding the neural generators of these components in striate and extrastriate cortical areas (reviewed in Clark et al., 1995). Recent studies that combined dipole modeling with functional magnetic resonance imaging (fMRI) of activated cortical areas have provided evidence that the C1 component to pattern onset is generated in the primary visual cortex (area V1) while the early part of the P1 wave arises from generators in the dorsal extrastriate occipital cortex and the later part of the P1 from sources in ventral extrastriate cortex (Di Russo et al., 2001, Di Russo et al., 2003, Martinez et al., 1999, Martinez et al., 2001). These studies localized the generators of the early, anterior part of the N1 complex to posterior parietal cortex and the later posteriorly distributed N1 to the same occipital generators as the P1.
The VEP elicited by a reversing pattern (e.g., checkerboard) is characterized by an initial negative component peaking at around 75 ms after the reversal (N75) followed by a positive component at around 100 ms (P100) and a second negativity at around 145 ms (N145) (Halliday, 1993). As with the pattern-onset VEP, the neural generators of the pattern-reversal VEP components have been much debated. While there is widespread agreement (based on studies in both animals and humans) that the N75 of the pattern-reversal VEP originates from the primary visual cortex (see Table 1), the origin of the P100 component is controversial. Some investigators have suggested that the P100 (like the pattern-onset P1) is mainly generated in extrastriate visual areas, while the majority has proposed that the P100 is generated (like the N75) in the striate cortex. N145 has been studied less extensively than the two earlier components. Some studies have identified a source for N145 in the extrastriate visual cortex, while others concluded that the N145 arises from the calcarine cortex or from both striate and extrastriate areas. Despite uncertainties as to the neural origins of its components, the pattern-shift VEP has had wide applications in clinical studies of visual system dysfunction (Halliday, 1993).
This lack of agreement among previous studies may be due to methodological differences such as the number of recording sites and the type of stimuli used. In particular, a sparse electrode array may not be able to differentiate concurrent activity arising from neighboring visual areas nor to obtain an accurate picture of the voltage topography produced by a given source. Furthermore, the use of stimuli extending over wide visual angles in some studies might have activated widespread regions of retinotopic cortical areas, thereby reducing the possibility of identifying the exact generator locations. In particular, stimuli that span more than one visual quadrant (crossing the horizontal and vertical meridians) may lead to activation of neuronal populations with opposing geometry (as in the primary visual area) resulting in a cancellation of their electric activity and in misinterpretation of the underlying source.
The purpose of the present study was to determine the detailed component structure of the pattern-reversal VEP and to localize its neural generators by using focal stimulation of each of the visual quadrants and a dense recording array of 64 electrodes. Sources were identified using dipole modeling based on a realistic head model and were compared with loci of cortical activations revealed by fMRI in response to the same stimuli. These sources were also localized on flat map with respect to visual cortical areas identified in individual subjects by retinotopic mapping and motion stimulation.
Section snippets
Subjects
Twenty-five paid volunteer subjects (12 female, mean age 26.1, range 18–36 years) participated in the VEP recordings. A subset of six of these subjects (three female, mean age 26.8, range 23–35 years) also received anatomical MRI scans and participated in the fMRI study. All subjects were right-handed and had normal or corrected-to-normal visual acuity. Written informed consent was obtained from all subjects after the procedures had been fully explained to them.
Stimuli
The stimuli consisted of brief
VEP waveforms and topography
The VEP waveforms elicited at selected electrode sites by stimuli in each of the four quadrants are shown in Fig. 2. The amplitudes, latencies, and topographical features of the major components are listed in Table 2.
The earliest component (here termed N75/P85) had a peak latency of 75–85 ms and inverted in polarity for upper vs. lower field stimuli. For upper field stimuli, the N75 was most prominent at occipitoparietal sites slightly ipsilateral to the midline (see Fig. 3 for scalp
Discussion
The present results provide strong support for the hypothesis that the first major component of the VEP elicited by a pattern reversal stimulus (N75/P85) arises from surface-negative activity in the primary visual cortex (area V1). The scalp topography of this component, its short onset latency, retinotopic polarity inversion, and dipole source localization in conjunction with structural and functional MRI all point to a neural generator in area V1 within the calcarine fissure. This conclusion
Acknowledgments
This research was supported by Italian grants from MIUR and IUSM to DS and FDR, and by NIMH (USA) grant MH-25594 to SAH.
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