THE STEADY STATE VISUALLY EVOKED POTENTIAL TOPOGRAPHY AND VIGILANCE* Richard B. Silberstein,1,2 Joseph Ciorciari,1 Andrew Pipingas, 1 Mark A. Schier1 and Stephen R. Wood1 1 Centre For Applied Neurosciences, Swinburne Institute of Technology, John St. Hawthorn, 3122. Australia. NH & MRC. Schizophrenia Research Unit, Royal Park Hospital, Park Parkville 3052 Australia 2 We report data which demonstrates a correlation between the magnitude of the Steady State Visually Evoked Potential (SSVEP) and visual vigilance. The SSVEP was recorded from 64 scalp sites and elicited by a 13 Hz uniform visual flicker presented while subjects undertook a visual vigilance task. Fifteen right-handed males were required to view three times a 180 second series of geometrical shapes; a continuous sequence of 60 squares, 60 circles and finally 60 squares. Just prior to the final trial subjects were asked to identify a target circle. A comparison of the last two trials indicated that the appearance of the target circle was associated with a transient SSVEP attenuation in the occipito-parietal and right pre-frontal regions. The same comparison indicated a pronounced SSVEP attenuation in the centro-parietal region peaking after the appearance of the circles. The distribution of the attenuation at the pre-frontal, centro-parietal and occipito-parietal regions was lateralised with the right hemisphere showing pronounced and long lasting effects. Aspects of normal brain function and dysfunction can be further explored using this novel technique. Many studies have been undertaken to examine the effects of cognition and attention on measurable brain electrophysiological potentials. Libet, Gleason, Wright and Pearl (1983,1985) reported on the ReadinessPotential in relation to a conscious intention to act. Other authors have reported that Event-Related Potentials (ERP's) can be quite useful in qualifying the attentional process (Gevins & Cutillo, 1986). The P300 has also been shown to be associated with the decisions of particular task events (Gevins & Cutillo, 1986). Some studies have investigated changes to the Transient ERP (Regan, 1977) using discontinuous stimuli such as auditory tones and clicks, and tachistoscopic presentation of visual targets. (Johnson & Donchin, 1982; Ruchkin, Johnson, Canoune, Ritter & Hammer, 1990). Yet few have reported the effects of cognition on the evoked potentials associated with rapidly repetitive stimuli; especially visual stimuli. The evoked potentials associated with this form of technique are termed Steady State Visually Evoked Potentials (SSVEP). These potentials consist of sinusoidal components at the stimulus frequency or its multiples (Regan, 1977). Using Fourier techniques it is possible to estimate the magnitude of the SSVEP using as little as 10 seconds of recorded data. This would make it a very useful tool for the investigation of electrophysiological correlates of cognitive processes. In addition to this technique, the probe ERP paradigm (Papanicolaou & Johnstone, 1984) was used, wherein the stimulus generating the ERP is irrelevant to the task. Brain regions generating increased levels of activity would attenuate in response to the "probe" stimulus. In this study we examined the effects of a visual vigilance task and the associated topography of the SSVEP. It was hypothesised that cortical regions with increased neural activity associated with the task would demonstrate an attenuated SSVEP. METHOD Subjects: Fifteen right-handed males with normal uncorrected visual acuity served as subjects (mean age = 24.1 yrs., sd=6.3, range 18-42 yrs.). Informed consent was obtained from all subjects. Tasks: All subjects were seated comfortably and requested to fixate on the centre of a video screen, and observe a series of geometric shapes; 60 squares followed by 60 circles and finally followed by another 60 squares. Each shape appeared every second and remained displayed for half a second. A fixation cross appeared at the centre of the screen during the other half. Each series of 180 shapes constituted a trial. Subjects were asked to fixate on the centre of the screen and view the, series three lines, (trials 1 to 3 * Published in: Levick WR et al. (eds) (1991). Brain Impairment: advances in applied research, University of Newcastle, Newcastle Australia, ISBN 0-7259-0720-7. pp. 275–280. Preprint © Mark Schier Silberstein et al. Preprint SSVEP & Vigilance Page 2 of 6 respectively) (see Figure 1). During the third trial, subjects were asked to attend to a modified circle; the last of the circles sequence. Trial 1 was used to familiarise the subjects with the task, trial 2 was a passive viewing task while trial 3 was an active viewing task requiring vigilance. Figure 1. Illustration of Task Protocol: Each Trial Consisted of 60 Squares Followed by 60 Circles Then Another 60 Squares. All Three Trials Were Similar Except For the TARGET Appearing During the Circles Phase of Trial 3. Each Trial Was 180 Seconds in Duration. Stimulus: The stimulus used to evoke the SSVEP consisted of a superimposed 13 Hz sinusoidal flicker. Maximum and minimum illuminance was 3.2 and 1.2 candela per square metre (c/m2) respectively. A set of goggles which allowed the stimulus to be superimposed on the viewing field was used. The centre of the video screen subtended an angle of one degree vertically and horizontally when viewed by the subject sitting one metre away. The shapes had an illuminance of 13.0 c/m2 while screen background was 1.2 c/m2 Recording: Brain electrical activity was recorded from 64 scalp electrode sites, including all 10-20 International System electrode sites with additional midway locations. All electrodes were housed in an electrode helmet designed and constructed within the Centre for Applied Neurosciences (Ciorciari, Silberstein, Simpson, & Schier, 1987). All recordings were referenced to linked ear lobe with the forehead as the ground. Brain electrical activity was amplified 20,000 times with a band pass down 3dB at 0.1 Hz and 30 Hz. Data was then digitised to 12 bit accuracy at a rate of 200 Hz and stored on hard disk for subsequent off-line analysis. All stimulus control was performed using an AT compatible computer (Schier, Ciorciari, Silberstein, & Simpson, 1988). Signal processing: The magnitude of the 13 Hz component was determined by calculating the cosine and sine 13 Hz Fourier coefficients. These coefficients were then evaluated using a 20 second integration window. This process was repeated for the full 180 second segment for each of the 64 electrodes, and yielded an SSVEP magnitude versus time series for each site. Silberstein et al. Preprint SSVEP & Vigilance Page 3 of 6 Group data for each trial were represented by 64 magnitude time series formed from the across subject average of the Fourier coefficient time series. Normalisation was achieved by calculating the mean of the magnitude time series associated with trial 2. Normalisation occurred prior to across subject averaging. Topographic maps were produced by using a two dimensional interpolation technique similar to that described by Dubinsky and Barlow (1980). The 32000 interpolated values produced by this interpolation procedure were displayed using a 16 level grey scale. RESULTS All subjects were able to identify the target circle. Figure 2, illustrates the SSVEP magnitude time series recorded at a right parietal site from a subject during trial 1 and 2. The large fluctuations were present in all the recordings from all subjects. These fluctuations are very similar to the Auditory Steady State potential fluctuations reported by Galambos and Makeig (1988). Figure 2. SSVEP Magnitude Time Series a Single Electrode Site Located Midway Between P4 and C4 (International 10-20), of the Across Subject Averaged Data. The Vertical Lines Indicate the Beginning of the Squares, Circles and Squares Task Segments. The Broken Line Represents Activity During Trial 2 and The Solid Line Represents Activity During Trial 3 (Target). For discussion purposes, three phases during the task protocol will be examined, and comparisons will be made between trial 2 and trial 3 during which the subject was asked to detect a target circle. The three phases will be termed presentation, anticipation, and target detection. Presentation is the point in time when the first circle appeared, alerting the subject that the main task was beginning (trial 3). In the 60 seconds after the appearance of the first circle, it was assumed that the subject would be in a state of anticipation. This state did coincide with a prolonged reduction of the trial 3 SSVEP magnitude when compared to trial 2. This reduction was diffusely distributed over the occipital/parietal region and peaked approximately 15 seconds after the appearance of the first circle (see Figure 3). It subsequently decayed over the next 45 seconds, the topography of this attenuation was essentially unchanged with the maximum effect Silberstein et al. Preprint SSVEP & Vigilance Page 4 of 6 located in the right occipital/parietal and central/parietal regions. Figure 3 is a map of the differences of SSVEP magnitude between trail 2 and trial 3 (target). Figure 4 illustrates the topographic differences between trial 2 and 3 during the presentation phase of the experiment. Larger differences between trials occur in the temporal/parietal and right frontal/temporal regions. Figure 3. Trial 2/3. Difference Map at Anticipation Phase. The SSVEP Differences Are Characterised by a Pronounced and Diffuse Difference in the Occipital/Parietal Region. The Map Represents the Differences in Activity When Viewed From Above, the Upper Portion Being the Prefrontal Region While the Lower Part Represents the Occipital Region. Figure 4. Trial 2/3, Difference Map at Presentation Phase. Larger Differences Between the Trials Occur in the Temporal/Parietal and Right Frontal/Temporal Regions. Silberstein et al. Preprint SSVEP & Vigilance Page 5 of 6 Figure 5 illustrates the SSVEP magnitude differences between trial 2 and 3 during the target detection phase of the experiment; a normalised average for all subjects. Prominent SSVEP differences were seen in the right parietal/temporal, right prefrontal and left temporal/occipital regions (see Figure 5). Figure 5. Trial 2/3 Difference Map at Target Detection Phase. Prominent SSVEP Differences Were Seen in the Right Parietal/Temporal, Right Prefrontal and Left Temporal/Occipital Regions. DISCUSSION When comparing a target to a non-target situation; trial 3 to trial 2, the most dominant feature noted is an attenuation of the SSVEP magnitude at most of the 64 recording sites. In particular, the occipital/parietal parietal/temporal, and right frontal regions of the scalp. Using the Probe-ERP technique to interpret these attenuations, suggests higher regional brain activity during trial 3, when compared to trial two. One feature which was very apparent during all three phases of the circles, presentation, anticipation, and target detection, was a consistent occipital attenuation of the SSVEP. This suggests, increased occipital activity during the three phases of the vigilance task. This finding is consistent with reports of increased blood flow in the occipital/parietal regions, with heightened visual attention (Roland, 1984; Mazziotta & Phelps, 1984). The other interesting feature which appeared solely during presentation and target detection was the attenuation which occurred in the right frontal regional. This increased frontal activity is consistent with neurophysiological and neuropsychological evidence for this regions involvement for mediating attentional processes (Fuster, 1980; Fuster, Bauer, & Jervey, 1982; Milner & Petrides, 1984). The right frontal findings are also consistent with reports that the right hemisphere has a specialised role in directing attention for visuospatial material (Weintraub & Mesulam, 1987). During the anticipation phase, attenuation of the SSVEP was noted in the central/parietal and occipital/parietal regions. This attenuation continued for the first 15 seconds after the presentation of the first circle. This decay was not symmetric; the right hemisphere being more long lasting. Silberstein et al. Preprint SSVEP & Vigilance Page 6 of 6 In conclusion we have demonstrated that changes in the SSVEP topography are associated with particular phases of a visual vigilance task paradigm. It is suggested that this technique warrants further investigation as an indicator of regional brain activity associated with cognitive processes. REFERENCES Ciorciari, J., Silberstein R.B., Simpson, D.G., &- Schier, MA. (1987). The multichannel electrode helmet Proceedings Conference on Engineering and Physical Sciences in Medicine, Becon p.52. Dubinsky, J., & Barlow, J.S. (1980). A simple dot-density topogram for EEG. EEG and Clinical Neurophysiology, 48,473-47. Fuster, J.M. (1980). The Prefrontal Cortex. New York: Academic Press. Fuster, J.M., Bauer, R.H., & Jervey, J.P. (1982). Cellular discharge in the dorsolateral prefrontal cortex of the monkey cognitive tasks. Experimental Neurology, 77, 679-694. Galambos, R., & Makeig, S. (1988). Dynamic changes in steady-state responses. In E. Basar (Ed.). Springer Series in Brain Dynamics (Vol 1). Berlin: Springer-Verlag. Gevins, A.S., Cutillo, B.A. (1986). Signals of cognition. In F.H. Lopes da Silva, W. Storm van Leeuwen & A. Remond (Eds.), Clinical Applications of Computer Analysis of EEG and other Neurophysiological Signals (Handbook of Electroencephalography and Clinical Neurophysiology: New series Vol. 2), Amsterdam: Elsevier. Johnson, C.C., &- Donchin, E. (1982). P300 component of the event-related potential as an index of information processing. Biological Psychiatry, 14, 1-52. Libet, B., Gleason, C.A., Wright, E.W., & Pearl, D.K. (1983). Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). Brain, 106, 623-642. Libet B., (1985). Unconscious cerebral initiative and the role of conscious will in voluntary action. The Behavioural and Brain Sciences, 8, 529-566. Mazziotta, J.C., & Phelps, M.E. (1984). Human sensory stimulation and deprivation: Positron emission tomographic results and strategies. Annals of Neurology, 15, 50-60. Milner, B., & Petrides, M. (1984). Behavioural effects of frontal lobe lesions in man. Trends in Neurosciences, 7, 403-407. Papanicolaou, A.C., & Johnstone, J. (1984). Probe evoked potentials: Theory, method and applications. International Journal of Neuroscience, 24, 107-131. Regan, D. (1977). Steady-state evoked potentials. Journal of the Optical Society of America, 11, 1475-1489. Roland, P. E. (1984). Metabolic measurements of the working frontal cortex in man. Trends in Neurosciences, 7, 430-435. Ruchkin, D.S., Johnson, R., Canoune, H.L., Ritter, W., & Hammer, M. (1990). Multiple sources of P3b associated with different types of information. Psychophysiology, 27, 157-176. Schier, M.A., Ciorciari, J., Silberstein R.B., & Simpson, D.G. (1988). Requirements of a high spatial resolution brain electrical activity data acquisition system. Neuroscience Letters, 30 (Suppl.) S151. Weintraub, S., & Mesulam, M.M. (I 987). Right cerebral dominance in spatial neglect. Archives of Neurology, 44, 621-625.