Neuroscience Research, 10 ( 1991 ) 5 2 ¢~3 '~ 1991 Elsevier Scientific Publishers Ireland, Ltd. 0168-0102/91/$03.5()
Frontal negativity of pattern-reversal visual evoked potentials in humans Shizuka Kurita-Tashima, Shozo Tobimatsu and Motohiro Kato Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Kyushu University, Fukuoka (Japan) (Received 23 July 1990; Accepted 13 September 1990)
Key words: Pattern-reversal visual evoked potential; Frontal negativity; Independent generator; Prefrontal cortex; Extrageniculate system; Human
SUMMARY We investigated the nature of negative potential in the frontal region with an approximate latency of 100 ms ('frontal negativity') as a component of pattern-reversal visual evoked potential (PVEP) in healthy human subjects. It was recorded by stimulation of one-half of the visual field, with different reference electrodes and with experimental manipulations of the stimulating visual field ('central scotomata' and ' peripheral constriction'). A negative potential field was demonstrated to be localized in the frontal region, and its physiological properties detected by the visual field manipulations were shown to be different from those of the occipital positive (P100) and negative (N105) components of PVEP. We conclude, therefore, that frontal negativity of PVEP is an actual electrical event generated in the frontal region, independent of P100 and N105.
Pattern-reversal visual evoked potential (PVEP) has been used as the most reliable functional indicator of the visual system in humans. The most prominent and consistent component is a positive peak in the occipital region with an approximate latency of 100 ms (P100). It appears symmetrically when both sides of the visual field are stimulated (full-field stimulation), whereas its scalp distribution is asymmetrical when only one side of the visual field is stimulated (half-field stimulation), with the P100 appearing on the side ipsilateral to the stimulated visual field and with a negative peak of similar latency (N105) appearing on the contralateral side 6,7. The two components have been assumed to be generated by afferent impulses arising from the macular and paramacular areas of the retina and passing through the geniculostriate visual pathway s,9 Recently a negative potential of similar latency has been demonstrated in the frontal region ('frontal negativity' 11,16.28,29,33). However, its nature has not been fully elucidated and is still controversial. There are three possibilities as to the nature of frontal negativity: the first is that frontal negativity is a mere expression of an inverted polarity of positive potential at a reference electrode caused by an extension of the electrical field Correspondence: Dr. Shizuka Kurita-Tashima, Department of Clinical Neurophysiology, Neurological Institute, Faculty of Medicine, Kyushu University 60, Fukuoka 812, Japan.
53 of the P100 4,23; the second is that it is an expression of the opposite end of a single dipole generating the P100 2,13,22; and the third is that it is an expression of an independent generator localized in the frontal region 29. It would be of significant relevance if frontal negativity could be proven to be an independent electrical event generated in the frontal region in response to visual stimulation in humans, because such potentials have been demonstrated in animal experiments during visually guided task performances 24- 26 We therefore performed the following two studies on healthy human subjects. The first was to clarify whether or not frontal negativity was due to activation of a reference electrode by the positive electrical field of P100, and the second was to identify whether a frontal negative potential was due to the opposite end of a single horizontal dipole of P100 or due to an independent frontal generator, if such a negative potential did exist in the frontal region. We have found that frontal negative potential does exist in response to pattern-reversal visual stimulation, and it is independent of the dipole source for P100 or the negative field of N105.
SUBJECTS AND METHODS
Recording and analysis of PVEPs Our method for recording PVEP has been described in detail previously ~4. In brief, visual stimulation consisted of a black-and-white checkerboard pattern, which was back-projected on a translucent screen and reversed at a rate of 1 Hz. The pattern was set to subtend 16 degrees in radius of the visual field, with a check size of 50 minutes of arc. The subject gazed at a red point at the center of the screen during a recording session. Visual acuity was corrected to or above 2 0 / 2 0 in all subjects. N o subjects were on any kind of medication. Unilateral stimulation of the visual field on the left (half-field stimulation) was done in order to differentiate the ipsilateral P100 and contralateral N105 in the occipital region. Eight scalp electrodes were placed bilaterally in the occipitoparietal and frontal regions: 5 cm above the inion at the midline (Oz), 5 cm lateral from Oz on either side (O1 for the left, and 0 2 for the right), and 10 cm lateral from Oz (LT for the left and RT for the right), and Fz, F3 and F4 according to the 10-20 electrode system. Electrodes on the left ear lobe (A1), the right ear lobe (A2), linked ear lobes (A1A2), or at Fz served as a reference. Recordings were made with a bandpass between 1.6 and 120 Hz, averaging 64 responses with an analysis time of 300 ms. The recording session was repeated at least twice to ensure the stability of PVEPs. PVEPs were evaluated by assessing how often P100, N105 and frontal negativity appeared in the PVEPs recorded in any given experimental session ('incidence'), by observing scalp distribution of the three components, and by measuring their latencies and amplitudes. The definitions of the three components were as follows: P100 was the first major positivity maximal in the occipital region ipsilateral to the stimulated visual half-field (O1), N105 was the negativity maximal in the contralateral posterior region (02) with an approximate latency of 105 ms, and the frontal negativity was the first major negativity in the frontal region. The latencies of each component were measured from the moment of stimulation to the peaks of each component (Fig. la, b, Fig. 2b). The amplitudes of each component were measured between the peaks of P100 and of the preceding negativity for P100 (Fig. lb), between the peaks of N105 and of the preceding
54 positivity for N105 (Fig. 2b), and between the peaks of frontal negativity and the preceding positivity (or the baseline) for frontal negativity (Fig. la). The measures were analyzed statistically using a X2-test and a Mann-Whitney U-test.
Effects of ear reference on frontal negativity In order to study how ear lobe electrodes are activated by the occipital components of PVEP, and how their use as reference electrodes modifies frontal negativity, PVEPs were recorded simultaneously from the frontal and occipital regions using A1, A2 and A1A2 as a reference. An Fz reference was also used for recording PVEPs from the occipital region. PVEPs recorded by using the three different ear references make it possible to calculate potentials at AI(P1) and A2(P2) separately at the moment of peak of frontal negativity, and an amplitude of frontal negativity not affected by P1 or P2 ( A M P * ) , according to the following equations: A M P * = AMP(A1) + P1 = AMP(A2) + P2 = AMP(A1A2) + (P1 + P2) where AMP(A1), AMP(A2) and AMP(A1A2) are the measured amplitudes of frontal negativity recorded with reference electrodes at A1, A2 and A1A2, respectively. Thus: P1 = AMP(A2) - AMP(A1A2) P2 = AMP(A1) - AMP(A1A2) A M P * = AMP(A1) + AMP(A2) - AMP(A1A2) Nine healthy volunteers, 3 males and 6 females, ranging in age from 21 to 31 years (mean of 26 years) participated in the experiment.
Physiological properties of frontal negativity, PIO0 and N105 To identify whether frontal negativity was due to a single horizontal dipole of P100 or due to an anteriorly extended negative field of N105, or due to an independent generator localized in the frontal region, modifications of its physiological features were compared with those of P100 and N105 during experimental manipulations of the visual half-field. Two kinds of visual field manipulation were done: firstly, the central part of the screen was masked so as to produce a dark spot of variable sizes (2, 4 and 8 degrees) in order to eliminate stimulation to the central part of the retina ('central scotoma'), and secondly, the peripheral part of the screen was masked so as to eliminate stimulation to the peripheral part of the retina, leaving the central 2 degrees to be stimulated (' peripheral constriction'). The effects of these visual field manipulations on the incidence of occurrence, scalp topography, latency and amplitude of each component were evaluated as described above. A total of 31 healthy volunteers, 12 males and 19 females, with ages ranging between 19 and 31 years (mean 22), participated in the experiment. RESULTS
Negative field in the frontal region Effects of ear reference The amplitudes of frontal negativity were different depending on the reference sites at A1, A2 or A1A2 [AMP(A1), AMP(A2) and AMP(A1A2), respectively], with AMP(A1) being maximal, AMP(A2) minimal and AMP(A1A2) intermediate (Fig. la, Table I). The
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