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Spatial Frequency and Right Hemisphere: An Electrophysiological Investigation
36, 21–29 (1998) BR970957
BRAIN AND COGNITION ARTICLE NO.
Spatial Frequency and Right Hemisphere: An Electrophysiological Investigation Mohamed Rebaı¨, Christian Bernard, Jacques Lannou, and Franc¸ois Jouen Laboratoire de Neurophysiologie Sensorielle, Universite´ de Rouen, Mont-Saint-Aignan, France The influence of the spatial frequency of visual stimuli on hemispheric asymmetry has been studied with visual evoked potentials (VEP). Nineteen different sinusoidal gratings (19 SF from 1 to 10 cpd) were presented in an ON–OFF mode to five right-handed subjects. The amplitude of the VEPs and the latency of the first positive component (C1) were analyzed. The results show that in the low range of spatial frequencies, the latency and the amplitude of C1 are similar in both hemispheres. At medium to high spatial frequencies, the VEPs on the right hemisphere (RH) present shorter latencies and larger amplitudes than those on the left hemisphere (LH). These results, discussed in relation to the directional differences in the time of callosal interhemispheric transfer, strengthen the idea that the RH is relatively more sensitive than the LH to the spatial component of the visual stimuli. 1998 Academic Press
Previous studies with visual evoked potentials (VEPs) have shown that the two cerebral hemispheres do not operate similarly in the early processing of visual information (spatial and temporal frequencies, contrast, etc.) (Rebaı¨, Bagot, & Viggiano, 1993; Mecacci, 1993). These results stand in agreement with the idea that hemispheric asymmetry originates in the differential sensitivity of both hemispheres to the physical characteristics of the visual stimuli (Christman, 1989; Kitterle, Christman, & Hellige, 1990; see Hellige, 1993, 1996 for a review). In a previous study (Rebaı¨ et al., 1993) we showed that the amplitude of the VEP of the right hemisphere (RH), in response to sine wave gratings of luminance presented in ON–OFF mode, increased with spatial frequency (SF), while it remained almost constant in the left hemisphere (LH). These results, together with the psychophysical results of Fiorentini and Berardi
Address correspondence and reprint requests to Mohamed Rebaı¨, Laboratoire de Neurophysiologie Sensorielle, Universite´ de Rouen, 1, Rue Thomas-Becket, 76821 Mont-Saint-Aignan Cedex, France. 21 0278-2626/98 $25.00
Copyright 1998 by Academic Press All rights of reproduction in any form reserved.
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(1984), suggest that the RH is preferentially specialized in the processing of spatial frequencies. The present experiment was designed to strengthen this hypothesis by measuring the latencies of the early components of the VEP and more precisely the latency of the C1 (first positive component). It is well known that presenting sine wave gratings with different SFs affects the latency of C1, which increases with increasing SF beyond 2–4 cycles per degree (cpd) (cf. Vassiliev & Strashimirov, 1979). This increase seems to correspond to a decrease in sensitivity to spatial frequency (beyond 1 to 4 cpd), as estimated through contrast thresholds (Campbell & Robson, 1968). The hypothesis on which the present study lies is that latency of C1 would be affected by an increase in spatial frequency in a different way in each hemisphere, thus indicating the differential sensitivity of the two hemispheres in the processing of SF. The C1 latency of the VEP should increase less in the hemisphere which is more sensitive to SF processing, especially in the high range. This hypothesis predicts that the latency of C1 would increase more in the LH than in the RH with increasing SF. EXPERIMENTAL METHOD Vertical sine wave gratings, generated on a Tektronix 608 monitor (P31 phosphor), were displayed through a rectangular aperture (6.25° 3 5°). Their temporal frequency of ON–OFF presentation was 1 Hz. The mean luminance of the screen (60 cd/m 2 ) did not change with alternating background and gratings, the contrast of which was fixed at 60%. Nineteen different spatial frequencies were used: 1, 1.5, 2, 2.25, 2.5, 2.75, 3, 3.25, 3.5, 3.75, 4, 4.25, 4.5, 4.75, 5, 5.5, 6, 8, and 10 cpd. These 19 values were not randomly chosen, but were chosen because the literature mentions that it is necessary to test a large number of SFs to observe the effect of SF on the latency of C1 (Vassiliev & Stomonyakov, 1987) and because our previous results showed that the hemispheric asymmetries of the VEP are less evident for low SFs than for high SFs (Rebaı¨, Mecacci, Bagot, & Bonnet, 1989). We have chosen small steps in the low SF range (1–4 cpd) to explore the limits of the interhemispheric differences in this range. The present analysis was conducted only on the C1, the origin of which lies in the peristriate visual areas (Maier, Dagnelie, Spekreise, and Van Dijk, 1986), since it is known that C1 is very sensitive to spatial frequency variations which affect its latency as well as its amplitude (Kulikowski, 1977; Parker & Salzen, 1977). Active electrodes (impedance below 5 kΩ) were placed 2.5 cm above the inion and 5 cm bilaterally from the midline, locations where hemispheric asymmetries are prominent (Rebaı¨, Mecacci, Bagot, & Bonnet, 1986). The linked earlobes served as reference and a forehead electrode served as ground. Potentials were amplified (bandpass 1/2 amplitude: 0.3–100 Hz) and 50 accumulations were averaged with Tracor Northern 1710. Measurements of the latencies were obtained with a special software which makes it possible to determine numerically the peak of the amplitude of the C1 and to read its latency with an accuracy of 3.9 ms. For VEPs amplitude, only the ONSET phase of the ON–OFF stimulation was considered, since the ONSET phase is less dependent than the OFFSET phase on the contrast change (Kulikowski, 1977). This amplitude was measured according to the method proposed by Spekreijse, Dagnielie, Maier, and Regan (1985) as the mean of the two positive components (C1, C3) minus the maximum of the negative component (C2) (see Fig. 1). We did not analyze C2 and C3, which are known to exhibit a substantial degree of adaptation during a relatively long stimulation (Regan, 1989).
SPATIAL FREQUENCY AND HEMISPHERIC ASYMMETRY IN VEPs
23
FIG. 1. Example of visual evoked potentials (VEPs) recorded in one subject on the right/ left hemispheres at the onset phase of the presentation of sinusoidal gratings at different spatial frequencies ranging from 1 to 10 cpd. In the lower right corner, the way we measured the VEP amplitude is indicated (for further explanation see text). Note the difference in the latencies of the C1 peak on both hemispheres from medium to high spatial frequencies.
Subjects were comfortably seated in the darkened experimental room (the only light came from the monitor screen) and they fixated on a small black dot in the center of the screen. The 19 spatial frequencies were presented in a random order in successive trials. Each trial consisted of a single round of 50 temporal cycles, at the fixed temporal frequency of 1 Hz, during which the 50 accumulations were performed. A 2-min pause occurred between recordings for each spatial frequency. Five right-handed subjects with normal or corrected-to-normal vision (checked with the Titmus Vision Tester) participated in the experiment. Handedness was assessed with a short questionnaire (Oldfield, 1971); all of the subjects were right-handed, with a handedness coefficient above 60% (62%, 1 subject; 74%, 1 subject; 85%, 2 subjects; 93%, 1 subject).
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RESULTS AND DISCUSSION
Figure 1 shows the VEPs recorded in one subject for the 19 spatial frequencies. In each record obtained with the ONSET phase, three successive components are observed, C1, C2, and C3 (Fig. 1), corresponding to CI, CII, and CIII (Jeffreys, 1977). Only the C1 latencies were averaged and submitted to an analysis of variance [two-way ANOVA: factor electrode (2 levels); factor spatial frequency (19 levels)]. The amplitude has been submitted to the same analysis of variance. The increase in the latency of C1 with spatial frequency is significant [F(18, 72) 5 7.07; p , .0005]. Such an increase is more obvious for middle to high frequencies in both recording positions (Fig. 2a). Also significant is the effect of the electrode position [F(1, 4) 5 9.08; p , .05] and the interaction between the electrode and the spatial frequency [F(18, 72) 5 2.88; p , .001]. This interaction indicates that there is no difference between hemispheres at low SF but, in the range of medium to high SF, a larger increase of the C1 latencies on LH than on RH is shown. Such a difference is illustrated in Fig. 2a, which shows the mean C1 latencies as a function of spatial frequencies for the two recording positions in five subjects. Mecacci, Spinelli, and Viggiano (1990) did not observe such differences in the latencies of these components in both hemispheres, but the stimuli they used (checkerboards with a large spatial frequency spectrum) make comparisons with our own results difficult because the spatial frequency is an important factor in determining hemispheric prominence. Figure 2b displays the mean amplitude of C1 as a function of the spatial frequency of the grating for each hemisphere; in both hemispheres this amplitude reaches a maximum at 4.75 cpd. The amplitude of the VEPs is significantly larger in the RH than in the LH [F(1, 4) 5 8.31; p , .05], and the interaction hemisphere 3 SF, which is also significant [F(18, 72) 5 3.06; p , .001], indicates that the higher the SF, the larger the difference in favor of the RH. In a previous study (Rebaı¨ et al, 1989, 1993), we mentioned that this difference resulted from a relatively constant amplitude of the VEP within the full range of SFs in the LH while in the RH this amplitude varied in a curvilinear manner; Fig. 2b illustrates this point. A global quadratic analysis indicated no significant trend. The relative constancy of the amplitudes for the first five to six spatial frequencies and the limitation of the higher SFs to 10 cpd could explain this absence of significance. In previous study (Rebaı¨ et al., 1989) in which a wider range of SFs were employed (0.5 to 16 cpd) such a quadratic trend was demonstrated, indicating that the amplitude of the VEP first increases, up to 4 cpd, and then decreases with higher SF. Post hoc comparisons for latencies and amplitudes for every spatial frequency show that the interhemispheric differences were not significant from 1 to 2.5 cpd, but that in the range of 2.75–10 cpd the latency of C1 and the amplitude of the VEP were significantly different in the hemispheres,
SPATIAL FREQUENCY AND HEMISPHERIC ASYMMETRY IN VEPs
25
FIG. 2. (a) Averaged latencies of the C1 component of the VEPs as function of spatial frequency for the right and left hemispheres (RH/LH). Vertical bars represent standard errors. (b) VEPs spatial frequency tuning as a function of hemisphere. The amplitude of the VEPs of the RH is larger than those of the LH and increases from medium to high spatial frequencies. The amplitude of the VEP on the LH is relatively constant over the whole range of SFs.
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FIG. 3. Average C1 latencies as function of the averaged VEPs amplitude. The VEPs of the right and left hemispheres are characterized by large amplitudes and short latencies and small amplitudes and long latencies, respectively.
[F(13, 52) 5 3.46; p , .0007] and [F(13, 52 ) 5 4.03; p , .0002], respectively (Fig. 3). Concerning the latency of C1, its variation with SF is classically attributed to the behavior of the transient/sustained visual systems (Breitmeyer, 1984). The transient system would be preferentially responding to low SF where the C1 latency does not vary so much, and the sustained system would be sensitive to mean and high SF, for which the C1 latency varies significantly. Both systems would be involved in the processing of SF, but their relative involvement would depend on the spatiotemporal characteristics of the visual stimulation. In our previous study (Rebaı¨ et al., 1993), we suggested that the RH was relatively more sensitive to the outputs of the sustained system and consequently would be relatively more specialized than the LH in the processing of SF. In the present study, the large range of SF allowed us to observe that the latency and the amplitude of C1 were, in the range of low to medium SF, similar in both hemispheres, suggesting then that they are equally sensitive to the outputs of the transient system. Another possible interpretation comes from the results of Berardi and Fiorentini (1987) and Berardi, Bisti, and Maffei (1987), who have shown that if there were a specific transcallosal transfer of low SF informations, this transfer would equalize the response of both hemispheres in this range of SF, whereas if there were no transfer of high SF, then in this range both hemispheres would respond independently to the outputs of the sustained system.
SPATIAL FREQUENCY AND HEMISPHERIC ASYMMETRY IN VEPs
27
In the range of medium to high SFs, the performances of both hemispheres diverged and it appeared that the amplitude of C1 was larger in the RH than in the LH, while the latencies in the RH were smaller than in the LH. Thus, the RH would be more sensitive than the LH, in this range of SF, to the outputs of the sustained system. And not only would the RH be more sensitive to the outputs of this sustained system, but these outputs would reach this hemisphere earlier than the LH since the latency of C1 is always shorter in the RH than in the LH. The temporal lag observed between both hemispheres in our study could be correlated with the directional differences in the times of interhemispheric transfer (IHTT) through the corpus callosum. The literature (see Brown, Larson, & Jeeves, 1994) reports that the IHTT of visual information is shorter when it is RH to LH directed rather than the opposite. This difference is evidenced by the latencies of the P1 and N1 components (corresponding to our C1 and C2) of the hemisphere ipsilateral to the visual stimulation: when the LH is on the side of the stimulated visual hemiretina, one observes latencies shorter than those occurring when the RH is stimulated ipsilaterally. If the time of transmission is the same for both the hemifield and the contralateral hemisphere, then the gap between both hemispheres for ipsilateral visual stimulation must be due to the IHTT through the corpus callosum, which would be shorter in the direction RH to LH than in the opposite direction. This directional asymmetry is interpreted to be caused either by the involvement of different slow/fast channels selected by the types of information and determined by the degree of hemispheric specialization (see Brown et al., 1994) or by anatomical asymmetries within callosal projections with more fibers passing from the RH to the LH than in the opposite direction (Marzi, Bisiacchi, & Nicoletti, 1991). The present results do not allow us to decide which interpretation is correct but they may explain why the spatial information, which is processed more efficiently (amplitude of the VEP) and quickly (latency of C1) in the RH than in the LH, can be transferred more quickly through the corpus callosum from the RH to the LH. Whatever the case, our results must be integrated in the current models of hemispheric asymmetries such as the afferent model of laterality (Umilta`, Rizzolatti, Anzola, Luppino, & Porro, 1985; see Zaidel, 1983) or mixed models of differential hemispheric efficiencies and interhemispheric transfer (Moscovitch, 1986). The processing of visual spatial frequency information, in its broadest sense, would be organized in hierarchical stages requiring specialized modules located in one or both hemispheres. The RH, which is more efficient than the LH for the processing of SF, would transmit information for further stages of handling, such as association with other visual features, triggering of cognitive processes (memory, discrimination decision), or speech production, which would be localized in the left hemisphere. The present electrophysiological results stand in opposition with those of behavioral research indicating a left versus right superiority in the processing
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of high versus low spatial frequencies (cf. Sergent & Hellige, 1986). We have already discussed this discrepancy (Rebaı¨ et al., 1993; Rebaı¨, Lannou, Bernard, Bonnet, and Rocchetti, 1997), which is probably due to methodological differences in the types of stimulations as well as the modes of measures (behavioral versus electrophysiological) recorded from the subjects. Whatever the case, this discrepancy points to the question of the correlation of the various types, levels, and natures of hemispheric asymmetries demonstrated by different methods. As a final conclusion, the present results, combined with our previous results (Rebaı¨ et al., 1993), show clearly that, in right-handers, the early evoked activities in the RH are relatively more sensitive to SF than the LH. We interpret this by the hypothesis that the RH is more specialized in the processing of spatial information at a low level. Others results, obtained with different techniques, are also consistent with this view: Wendt, Risberg, Stenberg, Rose´n, and Ingvar (1994) have shown by the measure of regional cerebral blood flow (rCBF) that the RH was more activated than the LH by spatially patterned visual stimuli (checkerboard). REFERENCES Berardi, N., Bisti, S., & Maffei, L. 1987. The transfer of visual information across the corpus callosum: Spatial and temporal properties in the cat. Journal of Physiology, 384, 619–632. Berardi, N., & Fiorentini, A. 1987. Interhemispheric transfer of visual information in humans: Spatial characteristics. Journal of Physiology, 387, 633–647. Bradshaw, J. L., & Nettleton, N. C. 1981. The nature of hemispheric specialization in man. Behavioral and Brain Science, 4, 51–91. Breitmeyer, G. B. 1984. Visual masking: An integrative approach. New York: Oxford Univ. Press. Brown, S., Larson, E. B., & Jeeves, M. A. 1994. Directional asymmetries in interhemispheric transmission time: Evidence from visual evoked potentials. Neuropsychologia, 32, 439– 448. Campbell, F. W., & Robson, J. G. 1968. Application of Fourier analysis to the visibility of grating. Journal of Physiology, 197, 551–566. Christman, S. 1989. Perceptual characteristics of visual laterality research. Brain and Cognition, 11, 238–257. Fiorentini, A., & Berardi, N. 1984. Right hemisphere superiority in the discrimination of spatial phase. Perception, 13, 695–708. Hellige, J. B. 1993. Hemispheric asymmetry: What’s right and what’s left. Cambridge, MA: Harvard Univ. Press. Hellige, J. B. 1996. Hemispheric asymmetry for visual information processing. Acta Neurobiologiae Experimentalis, 56, 485–497. Jeffreys, D. A. 1977. The physiological significance of pattern visual evoked potentials. In J. E. Desmedt (Ed.), Visual evoked potentials in man: New developments, Oxford: Clarendon. Pp. 134–167. Kitterle, F. L., Christman, S., & Hellige, J. B. 1990. Hemispheric differences are found in the identification, but not the detection, of low versus high spatial frequencies. Perception & Psychophysics, 48, 297–308.
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Kulikowski, J. J. 1977. Separation of occipital potentials related to detection of pattern and movement. In J. E. Desmedt (Ed.), Visual evoked potentials in man: New developments, Oxford: Clarendon. Pp. 184–196. Maier, J., Dagnelie, G., Spekreise, H., & Van Dy¨k, B.W. 1986. Principal component analysis for source locations of VEPs in man. Vision Research, 27, 165–177. Marzi, C. A., Bisiacchi, P., & Nicoletti, R. 1991. Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis. Neuropsychologia, 29, 1163– 1177. Mecacci, L. 1993. On spatial frequencies and cerebral hemispheres: Some remarks from the electrophysiological and neuropsychological points of view. Brain and Cognition, 22, 199–212. Mecacci, L., Spinelli, D., & Viggiano, M. P. 1990. The effects of visual field size on hemispheric asymmetry of pattern reversal visual evoked potentials. International Journal of Neuroscience, 51, 141–151. Moscovitch, M. 1986. Afferent and efferent models of visual perceptual asymmetries: Theoretical and empirical implications. Neuropsychologia, 24, 91–114. Oldfield, R. C. 1971. The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97–113. Parker, D., & Salzen, E. A. 1977. The spatial selectivity of early and late waves within the human visual evoked responses. Perception, 6, 85–95. Rebaı¨, M., Bagot, J. D., & Viggiano, M. P. 1993. Hemispheric asymmetry in transient visual evoked potentials induced by the spatial factor of the stimulation. Brain and Cognition, 23, 263–278. Rebaı¨m M., Lannou, J., Bernard, C., Bonnet, C., & Rochetti, G. 1997. Hemispheric asymmetries of visual evoked potentials in relation to spatial frequency, handedness and familial left-handedness. International Journal of Psychophysiology, 25, 85–95. Rebaı¨, M., Mecacci, L., Bagot, J. D., & Bonnet, C. 1986. Hemispheric asymmetries in the visual evoked potentials to temporal frequency: Preliminary evidence. Perception, 15, 589–594. Rebaı¨, M., Mecacci, L., Bagot, J. D., & Bonnet, C. 1989. Influence of spatial frequency and handedness on hemispheric asymmetry in visually steady-state evoked potentials. Neuropsychologia, 27, 315–324. Regan, D. 1989. Human brain electrophysiology: Evoked potentials end evoked magnetic fields in science and medicine. New York: Am. Elsevier. Spekreijse, H., Dagnielie, G., Maier, J., & Regan, D. 1985. Flicker and movement constituents of the pattern reversal response. Vision Research, 25, 1297–1304. Umilta`, C., Rizzolatti, G., Anzola, G.P., Luppino, G., & Porro, C. 1985. Evidence of interhemispheric transmission in laterality effects. Neuropsychologia, 23, 203–213. Vassiliev, A., & Stomonyakov, V. 1987. The effect of grating spatial frequency on the early VEP-component CI. Vision Research, 27, 727–729. Vassiliev, A., & Strashimirov, D. 1979. On the latency of human visually evoked response to sinusoidal gratings. Vision Research, 19, 843–846. Wendt, P. E., Risberg, J., Stenberg, G., Rose´n, I., & Ingvar, D. H. 1994. Ethanol reduces asymmetry of visual rCBF responses. Journal of Cerebral Blood Flow and Metabolism, 14, 963–973. Zaidel, E. 1983. Disconnection syndrome as a model for lateral effects in the normal brain. In J. B. Hellige (Ed.) Cerebral hemisphere asymmetry: Method, theory and application. New York: Praeger.
BRAIN AND COGNITION ARTICLE NO.
Spatial Frequency and Right Hemisphere: An Electrophysiological Investigation Mohamed Rebaı¨, Christian Bernard, Jacques Lannou, and Franc¸ois Jouen Laboratoire de Neurophysiologie Sensorielle, Universite´ de Rouen, Mont-Saint-Aignan, France The influence of the spatial frequency of visual stimuli on hemispheric asymmetry has been studied with visual evoked potentials (VEP). Nineteen different sinusoidal gratings (19 SF from 1 to 10 cpd) were presented in an ON–OFF mode to five right-handed subjects. The amplitude of the VEPs and the latency of the first positive component (C1) were analyzed. The results show that in the low range of spatial frequencies, the latency and the amplitude of C1 are similar in both hemispheres. At medium to high spatial frequencies, the VEPs on the right hemisphere (RH) present shorter latencies and larger amplitudes than those on the left hemisphere (LH). These results, discussed in relation to the directional differences in the time of callosal interhemispheric transfer, strengthen the idea that the RH is relatively more sensitive than the LH to the spatial component of the visual stimuli. 1998 Academic Press
Previous studies with visual evoked potentials (VEPs) have shown that the two cerebral hemispheres do not operate similarly in the early processing of visual information (spatial and temporal frequencies, contrast, etc.) (Rebaı¨, Bagot, & Viggiano, 1993; Mecacci, 1993). These results stand in agreement with the idea that hemispheric asymmetry originates in the differential sensitivity of both hemispheres to the physical characteristics of the visual stimuli (Christman, 1989; Kitterle, Christman, & Hellige, 1990; see Hellige, 1993, 1996 for a review). In a previous study (Rebaı¨ et al., 1993) we showed that the amplitude of the VEP of the right hemisphere (RH), in response to sine wave gratings of luminance presented in ON–OFF mode, increased with spatial frequency (SF), while it remained almost constant in the left hemisphere (LH). These results, together with the psychophysical results of Fiorentini and Berardi
Address correspondence and reprint requests to Mohamed Rebaı¨, Laboratoire de Neurophysiologie Sensorielle, Universite´ de Rouen, 1, Rue Thomas-Becket, 76821 Mont-Saint-Aignan Cedex, France. 21 0278-2626/98 $25.00
Copyright 1998 by Academic Press All rights of reproduction in any form reserved.
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REBAI¨ ET AL.
(1984), suggest that the RH is preferentially specialized in the processing of spatial frequencies. The present experiment was designed to strengthen this hypothesis by measuring the latencies of the early components of the VEP and more precisely the latency of the C1 (first positive component). It is well known that presenting sine wave gratings with different SFs affects the latency of C1, which increases with increasing SF beyond 2–4 cycles per degree (cpd) (cf. Vassiliev & Strashimirov, 1979). This increase seems to correspond to a decrease in sensitivity to spatial frequency (beyond 1 to 4 cpd), as estimated through contrast thresholds (Campbell & Robson, 1968). The hypothesis on which the present study lies is that latency of C1 would be affected by an increase in spatial frequency in a different way in each hemisphere, thus indicating the differential sensitivity of the two hemispheres in the processing of SF. The C1 latency of the VEP should increase less in the hemisphere which is more sensitive to SF processing, especially in the high range. This hypothesis predicts that the latency of C1 would increase more in the LH than in the RH with increasing SF. EXPERIMENTAL METHOD Vertical sine wave gratings, generated on a Tektronix 608 monitor (P31 phosphor), were displayed through a rectangular aperture (6.25° 3 5°). Their temporal frequency of ON–OFF presentation was 1 Hz. The mean luminance of the screen (60 cd/m 2 ) did not change with alternating background and gratings, the contrast of which was fixed at 60%. Nineteen different spatial frequencies were used: 1, 1.5, 2, 2.25, 2.5, 2.75, 3, 3.25, 3.5, 3.75, 4, 4.25, 4.5, 4.75, 5, 5.5, 6, 8, and 10 cpd. These 19 values were not randomly chosen, but were chosen because the literature mentions that it is necessary to test a large number of SFs to observe the effect of SF on the latency of C1 (Vassiliev & Stomonyakov, 1987) and because our previous results showed that the hemispheric asymmetries of the VEP are less evident for low SFs than for high SFs (Rebaı¨, Mecacci, Bagot, & Bonnet, 1989). We have chosen small steps in the low SF range (1–4 cpd) to explore the limits of the interhemispheric differences in this range. The present analysis was conducted only on the C1, the origin of which lies in the peristriate visual areas (Maier, Dagnelie, Spekreise, and Van Dijk, 1986), since it is known that C1 is very sensitive to spatial frequency variations which affect its latency as well as its amplitude (Kulikowski, 1977; Parker & Salzen, 1977). Active electrodes (impedance below 5 kΩ) were placed 2.5 cm above the inion and 5 cm bilaterally from the midline, locations where hemispheric asymmetries are prominent (Rebaı¨, Mecacci, Bagot, & Bonnet, 1986). The linked earlobes served as reference and a forehead electrode served as ground. Potentials were amplified (bandpass 1/2 amplitude: 0.3–100 Hz) and 50 accumulations were averaged with Tracor Northern 1710. Measurements of the latencies were obtained with a special software which makes it possible to determine numerically the peak of the amplitude of the C1 and to read its latency with an accuracy of 3.9 ms. For VEPs amplitude, only the ONSET phase of the ON–OFF stimulation was considered, since the ONSET phase is less dependent than the OFFSET phase on the contrast change (Kulikowski, 1977). This amplitude was measured according to the method proposed by Spekreijse, Dagnielie, Maier, and Regan (1985) as the mean of the two positive components (C1, C3) minus the maximum of the negative component (C2) (see Fig. 1). We did not analyze C2 and C3, which are known to exhibit a substantial degree of adaptation during a relatively long stimulation (Regan, 1989).
SPATIAL FREQUENCY AND HEMISPHERIC ASYMMETRY IN VEPs
23
FIG. 1. Example of visual evoked potentials (VEPs) recorded in one subject on the right/ left hemispheres at the onset phase of the presentation of sinusoidal gratings at different spatial frequencies ranging from 1 to 10 cpd. In the lower right corner, the way we measured the VEP amplitude is indicated (for further explanation see text). Note the difference in the latencies of the C1 peak on both hemispheres from medium to high spatial frequencies.
Subjects were comfortably seated in the darkened experimental room (the only light came from the monitor screen) and they fixated on a small black dot in the center of the screen. The 19 spatial frequencies were presented in a random order in successive trials. Each trial consisted of a single round of 50 temporal cycles, at the fixed temporal frequency of 1 Hz, during which the 50 accumulations were performed. A 2-min pause occurred between recordings for each spatial frequency. Five right-handed subjects with normal or corrected-to-normal vision (checked with the Titmus Vision Tester) participated in the experiment. Handedness was assessed with a short questionnaire (Oldfield, 1971); all of the subjects were right-handed, with a handedness coefficient above 60% (62%, 1 subject; 74%, 1 subject; 85%, 2 subjects; 93%, 1 subject).
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RESULTS AND DISCUSSION
Figure 1 shows the VEPs recorded in one subject for the 19 spatial frequencies. In each record obtained with the ONSET phase, three successive components are observed, C1, C2, and C3 (Fig. 1), corresponding to CI, CII, and CIII (Jeffreys, 1977). Only the C1 latencies were averaged and submitted to an analysis of variance [two-way ANOVA: factor electrode (2 levels); factor spatial frequency (19 levels)]. The amplitude has been submitted to the same analysis of variance. The increase in the latency of C1 with spatial frequency is significant [F(18, 72) 5 7.07; p , .0005]. Such an increase is more obvious for middle to high frequencies in both recording positions (Fig. 2a). Also significant is the effect of the electrode position [F(1, 4) 5 9.08; p , .05] and the interaction between the electrode and the spatial frequency [F(18, 72) 5 2.88; p , .001]. This interaction indicates that there is no difference between hemispheres at low SF but, in the range of medium to high SF, a larger increase of the C1 latencies on LH than on RH is shown. Such a difference is illustrated in Fig. 2a, which shows the mean C1 latencies as a function of spatial frequencies for the two recording positions in five subjects. Mecacci, Spinelli, and Viggiano (1990) did not observe such differences in the latencies of these components in both hemispheres, but the stimuli they used (checkerboards with a large spatial frequency spectrum) make comparisons with our own results difficult because the spatial frequency is an important factor in determining hemispheric prominence. Figure 2b displays the mean amplitude of C1 as a function of the spatial frequency of the grating for each hemisphere; in both hemispheres this amplitude reaches a maximum at 4.75 cpd. The amplitude of the VEPs is significantly larger in the RH than in the LH [F(1, 4) 5 8.31; p , .05], and the interaction hemisphere 3 SF, which is also significant [F(18, 72) 5 3.06; p , .001], indicates that the higher the SF, the larger the difference in favor of the RH. In a previous study (Rebaı¨ et al, 1989, 1993), we mentioned that this difference resulted from a relatively constant amplitude of the VEP within the full range of SFs in the LH while in the RH this amplitude varied in a curvilinear manner; Fig. 2b illustrates this point. A global quadratic analysis indicated no significant trend. The relative constancy of the amplitudes for the first five to six spatial frequencies and the limitation of the higher SFs to 10 cpd could explain this absence of significance. In previous study (Rebaı¨ et al., 1989) in which a wider range of SFs were employed (0.5 to 16 cpd) such a quadratic trend was demonstrated, indicating that the amplitude of the VEP first increases, up to 4 cpd, and then decreases with higher SF. Post hoc comparisons for latencies and amplitudes for every spatial frequency show that the interhemispheric differences were not significant from 1 to 2.5 cpd, but that in the range of 2.75–10 cpd the latency of C1 and the amplitude of the VEP were significantly different in the hemispheres,
SPATIAL FREQUENCY AND HEMISPHERIC ASYMMETRY IN VEPs
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FIG. 2. (a) Averaged latencies of the C1 component of the VEPs as function of spatial frequency for the right and left hemispheres (RH/LH). Vertical bars represent standard errors. (b) VEPs spatial frequency tuning as a function of hemisphere. The amplitude of the VEPs of the RH is larger than those of the LH and increases from medium to high spatial frequencies. The amplitude of the VEP on the LH is relatively constant over the whole range of SFs.
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FIG. 3. Average C1 latencies as function of the averaged VEPs amplitude. The VEPs of the right and left hemispheres are characterized by large amplitudes and short latencies and small amplitudes and long latencies, respectively.
[F(13, 52) 5 3.46; p , .0007] and [F(13, 52 ) 5 4.03; p , .0002], respectively (Fig. 3). Concerning the latency of C1, its variation with SF is classically attributed to the behavior of the transient/sustained visual systems (Breitmeyer, 1984). The transient system would be preferentially responding to low SF where the C1 latency does not vary so much, and the sustained system would be sensitive to mean and high SF, for which the C1 latency varies significantly. Both systems would be involved in the processing of SF, but their relative involvement would depend on the spatiotemporal characteristics of the visual stimulation. In our previous study (Rebaı¨ et al., 1993), we suggested that the RH was relatively more sensitive to the outputs of the sustained system and consequently would be relatively more specialized than the LH in the processing of SF. In the present study, the large range of SF allowed us to observe that the latency and the amplitude of C1 were, in the range of low to medium SF, similar in both hemispheres, suggesting then that they are equally sensitive to the outputs of the transient system. Another possible interpretation comes from the results of Berardi and Fiorentini (1987) and Berardi, Bisti, and Maffei (1987), who have shown that if there were a specific transcallosal transfer of low SF informations, this transfer would equalize the response of both hemispheres in this range of SF, whereas if there were no transfer of high SF, then in this range both hemispheres would respond independently to the outputs of the sustained system.
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In the range of medium to high SFs, the performances of both hemispheres diverged and it appeared that the amplitude of C1 was larger in the RH than in the LH, while the latencies in the RH were smaller than in the LH. Thus, the RH would be more sensitive than the LH, in this range of SF, to the outputs of the sustained system. And not only would the RH be more sensitive to the outputs of this sustained system, but these outputs would reach this hemisphere earlier than the LH since the latency of C1 is always shorter in the RH than in the LH. The temporal lag observed between both hemispheres in our study could be correlated with the directional differences in the times of interhemispheric transfer (IHTT) through the corpus callosum. The literature (see Brown, Larson, & Jeeves, 1994) reports that the IHTT of visual information is shorter when it is RH to LH directed rather than the opposite. This difference is evidenced by the latencies of the P1 and N1 components (corresponding to our C1 and C2) of the hemisphere ipsilateral to the visual stimulation: when the LH is on the side of the stimulated visual hemiretina, one observes latencies shorter than those occurring when the RH is stimulated ipsilaterally. If the time of transmission is the same for both the hemifield and the contralateral hemisphere, then the gap between both hemispheres for ipsilateral visual stimulation must be due to the IHTT through the corpus callosum, which would be shorter in the direction RH to LH than in the opposite direction. This directional asymmetry is interpreted to be caused either by the involvement of different slow/fast channels selected by the types of information and determined by the degree of hemispheric specialization (see Brown et al., 1994) or by anatomical asymmetries within callosal projections with more fibers passing from the RH to the LH than in the opposite direction (Marzi, Bisiacchi, & Nicoletti, 1991). The present results do not allow us to decide which interpretation is correct but they may explain why the spatial information, which is processed more efficiently (amplitude of the VEP) and quickly (latency of C1) in the RH than in the LH, can be transferred more quickly through the corpus callosum from the RH to the LH. Whatever the case, our results must be integrated in the current models of hemispheric asymmetries such as the afferent model of laterality (Umilta`, Rizzolatti, Anzola, Luppino, & Porro, 1985; see Zaidel, 1983) or mixed models of differential hemispheric efficiencies and interhemispheric transfer (Moscovitch, 1986). The processing of visual spatial frequency information, in its broadest sense, would be organized in hierarchical stages requiring specialized modules located in one or both hemispheres. The RH, which is more efficient than the LH for the processing of SF, would transmit information for further stages of handling, such as association with other visual features, triggering of cognitive processes (memory, discrimination decision), or speech production, which would be localized in the left hemisphere. The present electrophysiological results stand in opposition with those of behavioral research indicating a left versus right superiority in the processing
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of high versus low spatial frequencies (cf. Sergent & Hellige, 1986). We have already discussed this discrepancy (Rebaı¨ et al., 1993; Rebaı¨, Lannou, Bernard, Bonnet, and Rocchetti, 1997), which is probably due to methodological differences in the types of stimulations as well as the modes of measures (behavioral versus electrophysiological) recorded from the subjects. Whatever the case, this discrepancy points to the question of the correlation of the various types, levels, and natures of hemispheric asymmetries demonstrated by different methods. As a final conclusion, the present results, combined with our previous results (Rebaı¨ et al., 1993), show clearly that, in right-handers, the early evoked activities in the RH are relatively more sensitive to SF than the LH. We interpret this by the hypothesis that the RH is more specialized in the processing of spatial information at a low level. Others results, obtained with different techniques, are also consistent with this view: Wendt, Risberg, Stenberg, Rose´n, and Ingvar (1994) have shown by the measure of regional cerebral blood flow (rCBF) that the RH was more activated than the LH by spatially patterned visual stimuli (checkerboard). REFERENCES Berardi, N., Bisti, S., & Maffei, L. 1987. The transfer of visual information across the corpus callosum: Spatial and temporal properties in the cat. Journal of Physiology, 384, 619–632. Berardi, N., & Fiorentini, A. 1987. Interhemispheric transfer of visual information in humans: Spatial characteristics. Journal of Physiology, 387, 633–647. Bradshaw, J. L., & Nettleton, N. C. 1981. The nature of hemispheric specialization in man. Behavioral and Brain Science, 4, 51–91. Breitmeyer, G. B. 1984. Visual masking: An integrative approach. New York: Oxford Univ. Press. Brown, S., Larson, E. B., & Jeeves, M. A. 1994. Directional asymmetries in interhemispheric transmission time: Evidence from visual evoked potentials. Neuropsychologia, 32, 439– 448. Campbell, F. W., & Robson, J. G. 1968. Application of Fourier analysis to the visibility of grating. Journal of Physiology, 197, 551–566. Christman, S. 1989. Perceptual characteristics of visual laterality research. Brain and Cognition, 11, 238–257. Fiorentini, A., & Berardi, N. 1984. Right hemisphere superiority in the discrimination of spatial phase. Perception, 13, 695–708. Hellige, J. B. 1993. Hemispheric asymmetry: What’s right and what’s left. Cambridge, MA: Harvard Univ. Press. Hellige, J. B. 1996. Hemispheric asymmetry for visual information processing. Acta Neurobiologiae Experimentalis, 56, 485–497. Jeffreys, D. A. 1977. The physiological significance of pattern visual evoked potentials. In J. E. Desmedt (Ed.), Visual evoked potentials in man: New developments, Oxford: Clarendon. Pp. 134–167. Kitterle, F. L., Christman, S., & Hellige, J. B. 1990. Hemispheric differences are found in the identification, but not the detection, of low versus high spatial frequencies. Perception & Psychophysics, 48, 297–308.
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