International Journal of Psychophysiology, 6 (1988) 255-261 Elsevier 255 PSP 00207 Detection of cerebral lateralization of function using EEG alpha-contingent visual stimulation II David Goodman ’ and Thomas Mulholland * ’ Veterans Administration Medical Center and Division of Psychiatry, Boston University Medical School, Boston, MA 02130 (U.S.A.) and ’ Veterans Administration Medical Center Bedford, MA 01730 and Divisions of Neurology and Psychiatry, Boston Uniuersiiy Medical School, Boston, MA 02130 (U.S.A.) (Accepted 29 March 1988) Key words; Alpha-contingent stimulation; Control of EEG The replicative reliability of durations of alpha-blocking following visual stimulation over different cortical sites was assessed with the method of alpha-contingent stimulation. Fourteen right-handed undergraduates were tested in a randomized factorial design. Words or geometric designs of equal luminance were presented by computer to randomly selected visual half-fields contingent on the occurrence of alpha at one of 4 placements (left and right occipital and left and right temporal). The control (X/s) of alpha-blocking durations was significantly greater for contralateral visual half-field stimulation compared to ipsilateral visual half-field stimulation. This and other results were interpreted in terms of the concept of replicative reliability of retinal-cortical connections to occipital and temporal lobes and affirm the validity and sensitivity of the method. INTRODUCTION In previous publications (Goodman, 1978; Goodman et al., 1980) a feedback method for locating the most controlled EEG alpha-attenua- tion response to visual stimuli (MuIholland, 1979, 1977a,b) was used to investigate the cerebral later- ality of linguistic function and the anatomically based lateralization of cortical processing of hemiretinal stimulation. The method allows an estimate of the relative replicative reliability of different within-organism forward paths (e.g. peripheral sense organ --, cerebral cortex) by introducing an error-correcting negative feedback path from the dependent vari- able (EEG alpha duration) to the system input (visual stimulus presentation). The introduction of the external feedback path produced an increase in the control of the dependent EEG variable by Correspondence: T. Mulholland, Psychology Service, VA Medi- cal Center, 200 Springs Road, Bedford, MA 01730, U.S.A. the independent stimulus-related variable, mea- sured as the ratio of systematic trend (X, mean alpha duration) to unsystematic, noisy variation (s, standard deviation of alpha durations). The amount of increase in this control ratio (X/s) is related to the replicative reliability of the forward paths producing the greater increase in the control ratio. As expected, contingent feedback was associ- ated with a significantly higher alpha control ratio than sham feedback. Within contingent feedback data, the following variables were also associated with significantly higher alpha control ratios; Pathway (contralateral > ipsilateral), and Ap- propriateness of verbal and non-verbal stimuli (appropriate > inappropriate). The major source of these control ratio differences was shown to be in the standard deviation of alpha durations, which would be expected in terms of hypothesized dif- ferences and with regard to replicative reliability. This paper presents other results from that study with regard to the duration of alpha-block- ing termed ‘not-alpha’ duration (Atna). 0167-8760/88/$03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)
Transcript
International Journal of Psychophysiology, 6 (1988) 255-261
Elsevier 255
PSP 00207
Detection of cerebral lateralization of function using EEG alpha-contingent visual stimulation II
David Goodman ’ and Thomas Mulholland * ’ Veterans Administration Medical Center and Division of Psychiatry, Boston University Medical School, Boston, MA 02130 (U.S.A.) and
’ Veterans Administration Medical Center Bedford, MA 01730 and Divisions of Neurology and Psychiatry, Boston Uniuersiiy Medical
School, Boston, MA 02130 (U.S.A.)
(Accepted 29 March 1988)
Key words; Alpha-contingent stimulation; Control of EEG
The replicative reliability of durations of alpha-blocking following visual stimulation over different cortical sites was assessed with
the method of alpha-contingent stimulation. Fourteen right-handed undergraduates were tested in a randomized factorial design.
Words or geometric designs of equal luminance were presented by computer to randomly selected visual half-fields contingent on the
occurrence of alpha at one of 4 placements (left and right occipital and left and right temporal). The control (X/s) of alpha-blocking
durations was significantly greater for contralateral visual half-field stimulation compared to ipsilateral visual half-field stimulation.
This and other results were interpreted in terms of the concept of replicative reliability of retinal-cortical connections to occipital and
temporal lobes and affirm the validity and sensitivity of the method.
INTRODUCTION
In previous publications (Goodman, 1978; Goodman et al., 1980) a feedback method for locating the most controlled EEG alpha-attenua- tion response to visual stimuli (MuIholland, 1979, 1977a,b) was used to investigate the cerebral later- ality of linguistic function and the anatomically based lateralization of cortical processing of hemiretinal stimulation.
The method allows an estimate of the relative replicative reliability of different within-organism forward paths (e.g. peripheral sense organ --, cerebral cortex) by introducing an error-correcting negative feedback path from the dependent vari- able (EEG alpha duration) to the system input (visual stimulus presentation). The introduction of the external feedback path produced an increase in the control of the dependent EEG variable by
Correspondence: T. Mulholland, Psychology Service, VA Medi- cal Center, 200 Springs Road, Bedford, MA 01730, U.S.A.
the independent stimulus-related variable, mea- sured as the ratio of systematic trend (X, mean alpha duration) to unsystematic, noisy variation (s, standard deviation of alpha durations). The amount of increase in this control ratio (X/s) is related to the replicative reliability of the forward paths producing the greater increase in the control ratio.
As expected, contingent feedback was associ- ated with a significantly higher alpha control ratio than sham feedback. Within contingent feedback data, the following variables were also associated with significantly higher alpha control ratios; Pathway (contralateral > ipsilateral), and Ap- propriateness of verbal and non-verbal stimuli (appropriate > inappropriate). The major source of these control ratio differences was shown to be in the standard deviation of alpha durations, which would be expected in terms of hypothesized dif- ferences and with regard to replicative reliability.
This paper presents other results from that study with regard to the duration of alpha-block- ing termed ‘not-alpha’ duration (Atna).
This experiment was reviewed and approved by the Human Studies subcommittee of this Medical Center in accordance with V.A. circular 10-75-121. The method is safe and non-stressful.
Twenty-four right-handed (Edinburgh handed- ness inventory Oldfield, 1971) male undergraduate volunteers (ages 18-25 years) with normal vision (corrected, if necessary) participated in the experi- ment. Of these, 4 subjects were excluded for EMG or EKG artifacts or insufficient alpha (less than 50% time alpha during an eyes-closed resting in the dark baseline). Further data from 6 subjects were later found to be contaminated with 60 Hz artifacts. These data were discarded. The remain- ing artifact-free data from 14 subjects were analyzed.
Four monopolar EEG recordings were made using chlorided silver cup electrodes referenced to linked earlobes with the right mastoid grounded. Electrodes were placed on the occipital-parietal border in each hemisphere midway between 02 and P4, over Wemicke’s area in the left hemi- sphere, defined by Matsumiya et al. (1972) as the center of the triangle formed by locations P3, T3 and T5, and the homologous electrode placements over the right hemsiphere. Lateral EOG was re- corded (DC) from silver/silver-chloride electrodes at the outer canthi of both eyes using a polygraph and FM tape recorder.
Alpha activity was detected in each of the 4 EEG channels independently using identical bandpass filtering and amplitude-threshold detec- tion as described by Boudrot et al. (1978). The amplitude threshold for each channel was set at 25% of the maximum peak-to-peak alpha am- plitude of that channel observed while the subject was viewing a fixation cross. This procedure com- pensates for both interchannel and intersubject differences in the amplitude of alpha activity by standardizing the definition of alpha relative to each subject’s observed maximum. Thus, an alpha ‘burst’ is defined by the onset and offset of the detection circuitry.
A laboratory computer was used to randomize, generate, and display the visual stimuli and to collect, store and analyze the duration of alpha-
blocking data (Goodman, 1973). The computer generated and displayed the stimuli on an 18 x 23 cm CRT located 45 cm in front of the subject who viewed the stimuli monocularly using his right eye while positioned in a chin and forehead rest.
Stimuli were of two types, verbal and spatial, and were displayed to either the right or left hemiretina. The stimuli were intermixed across trials and ordering of both stimulus type and location was completely randomized.
Sixty frequently used three-letter words (Thorndike and Lorge, 1944) were chosen as verbal stimuli and displayed on the CRT using a 4 x 6 dot-matrix configuration for the component block letters (Buchsbaum and Fedio, 1969). The spatial stimuli were 60 geometric designs also composed of 3 dot-matrix (geometric) elements (analogous to letters in the verbal stimuli). They occupied the same area with the same total number of dots as the verbal stimuli, thus controlling for the size and average luminosity of the stimuli. Luminosity was not measured.
Each stimulus, subtending 2.55” of visual an- gle, was presented hemiretinally with the stimulus center laterally displaced 2.40” from a small central fixation cross. This displacement is com- parable to that used in other experiments which utilized hemiretinal stimulation (Buchsbaum and Fedio, 1970; Fedio and Buchsbaum, 1971).
The EOG was calibrated by having the subject alternately fixate on the cross and the outer border of the stimulus windows (3.67 ’ from center). Half this displacement (1.84” ) was established as a limit of eye angle for acceptance as experimental data.
Subjects were instructed to fixate on a small cross in the center of CRT and, without moving their eyes, to “pay attention” to the words and design which would flash on either side of the fixation cross. They were asked to silently dis- criminate between the words and designs and to read the words and to examine the shape and form of the design to prepare for a subsequent memory task.
The purpose of informing the subject at the outset of the experiment to expect a later memory test was to motivate him to pay attention to all the stimuli during the session.
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During the experiment the subjects were seated in a light- and soundproof, electrically shielded room equipped with an audio-communication sys- tem. Eye and head movements were reduced by pretraining subjects, by using a chin and forehead rest, by providing a patterned fixation stimulus (a cross), and by completely randomizing the field of presentation for each stimulation. Similar proce- dures have been similarly employed (Buchsbaum and Fedio, 1970; Fedio and Buchsbaum, 1971; Cavonius and Esteves-Uscanga, 1974).
Following the calibration of the alpha detection equipment, three baseline conditions were re-
corded, each lasting 1.5 min. They were (1) eyes closed, (2) eyes open in the dark, and (3) viewing the fixation cross. Three baseline conditions were repeated in reverse order at the end of the session. A practice condition was presented following the initial baselines and served to familarize the sub- ject with the experiment and to provide training for the reduction of eye movements. An additional practice condition was given if excessive eye movements occurred.
The experiment was divided into five lo-min blocks (not including rest periods): four using alpha-contingent visual stimulation, and one with random non-contingent visual stimulation. Each block included four 2.5min trials separated by a rest period of at least 30 s.
In each trial of alpha-contingent visual stimula- tion, a randomly selected stimulus was presented at the onset of an alpha burst and remained in view until the offset of alpha activity. Since only one EEG channel could control the visual display at any time, four blocks of alpha-contingent visual stimulation were necessary, one for each of the recording sites. The sequential order of these blocks was randomized across subjects. In the non-contingent, random visual stimulation trials, stimulus durations ranged between 0.02 and 0.68 s (mean = 0.35) with interstimulus intervals of 1.68 + 5.32 s (mean = 3.5 s). These values are typical of those generated with alpha-contingent visual stimulation (Mulholland, 1973). This block of non-contingent visual stimulation was employed to permit (1) a comparison of alpha control ratios for alpha-contingent vs random stimulation, and (2) an analysis of cortical evoked potentials (EPs)
to verbal and non-verbal visual stimuli presented hemiretinally. These EP data are reported elsewhere (Goodman, 1978).
The selection of a particular stimulus (1 out of 60 items of each type), and of the type (verbal or spatial) of stimulus, and visual field placement (left or right) was randomly controlled by the computer for each presentation. This randomiza- tion procedure was designed to discourage the subjects from establishing a cognitive processing mode independent of the stimulus type. This randomization also acted to reduce any tendency of the subject to bias fixation away from the center as he could not predict in which visual field the next stimulus would appear.
‘Catch’ or ‘blank’ unstimulated trials were ran- domly interspersed among the actual stimuli in all conditions. Catch trials were identical to other trials except that no stimuli were presented. The unstimulated trials provided random samples of unstimulated portions of the EEG throughout the experiment.
After the last baseline condition, the subject was disconnected from the polygraph and the electrodes were removed. A recall test was then administered to the subject to determine if he could recall any of the stimuli he had seen. All subjects recalled at least 10 stimuli of each type. At no time before or during the experiment was the subject informed or aware that his EEG was controlling the stimulus presentation.
Data analysis The duration of time of each separate occur-
rence of alpha and not-alpha was recorded by the computer in each of the four EEG channels to the nearest 0.02 s. For each of the four alpha-contin- gent conditions, only the alpha and not-alpha time durations from the one EEG channel controlling the stimulation were analyzed. For the random stimulation trials, all four EEG channels were independent of the stimulation process. Therefore, data during random stimulation trials were col- lected simultaneously from all four channels.
To facilitate the identification of those alpha and not-alpha episodes during the random stimu- lation trials which were present during the stimu- lations, the concept of an EEG ‘event pair’ was
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created. An event pair was defined as an alpha burst duration followed by a not-alpha duration. During alpha-contingent visual stimulation, an event pair represents a typical stimulation-induced alpha-blocking response in which the alpha-burst duration includes the latency of the blocking re- sponse and the not-alpha duration represents the temporal persistence of the blocking response. This operational definition of an alpha-blocking re- sponse (an EEG event pair) was then applied to the random stimulation trials such that the entire event pair (alpha duration followed by not-alpha duration) that contained a stimulation within it was identified as the EEG event pair associated with the stimulation.
Each event pair associated with a contingent or sham feedback stimulation was grouped according to the stimulus (1 of 5) that occurred during that alpha and not-alpha event pair. Three statistics were computed from the alpha and not-alpha time durations associated with each stimulus category: the mean (X), standard deviation (s), and the ratio of the mean to the standard deviation of the alpha and not-alpha durations (X/s) called the ‘control ratio’.
The ipsilateral pathway includes all the left visual field/left hemisphere data and right visual field/right hemisphere data. The contralateral Pathway includes all left visual field/right hemi- sphere data and also all right visual field/left hemisphere data. A significant main effect of Pathway indicated a hemiretinal stimulation-cere- bral lateralization effect.
Five independent variables in a completely fac- torial, randomized, repeated-measures within-sub- jects design, the variables being: visual Pathway (visual half-field to EEG hemisphere-contralateral [direct], ipsilateral [indirect]): appropriateness of stimuli (referred to EEG hemisphere-appropriate [verbal or non-verbal], inappropriate [verbal or non-verbal]); EEG Hemisphere (left, right); EEG Lobe (occipital, temporal Wemicke’s area); and Contingency of the feedback (true alpha-contin- gent feedback, or sham feedback non-contingent stimulation).
Each ANOVA was computed using the Mill- man and Glass (1967) algorithm (analogous to Winer’s (1971) technique) in which the mean
square of each fixed effect source of variance (within-subject effects) is tested against the mean- square error term of the interaction of that fixed error source of variance with random subjects (S) effect. Thus, Pathway (P) was tested against the Pathway x Subject interaction. A significance level of p = 0.05 was adopted for all statistical tests. Degrees of freedom for each F-test were 1 and 13.
RESULTS
Mean not-alpha durations were: longer for sham (2.80 s) than for alpha-contingent stimulation (1.47 s); longer for occipital EEG’s (2.38 s) than for temporal EEG’s (1.85 s); longer for a contralateral pathway (2.14 s) than for an ipsilateral (2.08 s). The difference between Pathways with regard to not-alpha durations was evident for occipital EEGs (ipsilateral 2.33 s; contralateral 2.43 s), but not for temporal EEG (ipsilateral 1.84 s; contralateral 1.85 s).
Variability (s) of not-alpha durations is greater for sham (k2.52 s) than for alpha contingent stimulation (+ 1.37 s).
Variability (s) of not-alpha durations is greater for occipital EEG’s ( f 2.22 s) than for temporal EEG’s (k 1.70 s).
The control (X/s) of not-alpha durations was greater for a contralateral pathway (1.25) than for an ipsilateral pathway (1.15).
The difference between sham and alpha-contin- gent stimulation, with regard to the variability of not-alpha durations, was greater for right-sided EEG’s than for left-sided EEG’s: contingent-right (+ 1.25 s) sham right ( f 1.14 s); contingent left (i 1.15 s), sham left (_t 1.18 s).
When data from alpha-contingent stimulation and sham conditions are analyzed separately, the control (X/s) of not-alpha durations is greater for contralateral pathways than for ipsilateral path- ways in both alpha-contingent and sham condi- tions. (Alpha-contingent stimulation: contra- lateral, 1.23; ipsilateral, 1.16; sham feedback stimulation: contralateral, 1.18; ipsilateral, 1.13. Control of not-alpha durations (X/s) is greatest for the alpha-contingent stimulation conditions, and contralateral pathways.
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For alpha-contingent stimulation, control of the right-sided EEG’s (1.24) is greater than for left- sided EEG’s (1.14).
The mean duration of not-alpha is greater for occipital EEG’s (1.6 s) compared to temporal EEG’s (1.34 s).
Catch trials Catch trials were unstimulated (blank) trials
interspersed within every condition among the ‘true’ stimuli. ANOVAs were performed on the catch trials using three factors: Contingency, Lobe and Hemisphere. The mean not-alpha duration of catch trials was greater in the sham conditions compared to stimulation conditions (F = 7.9, P =
0.015). Variability (s) of not-alpha durations in the
catch trials was greater for the sham conditions than for alpha contingent stimulation (F = 7.0,
P = 0.02).
Catch trials us stimulation trials l-Tests for correlated samples (Ferguson, 1971)
were made to compare EEG’s of catch events with stimuli events. Results are presented in Table I.
Stimulation trials, compared to catch trials (without visual stimuli), produced significantly greater control of alpha and not-alpha durations, and smaller percent time alpha.
TABLE I
t-tests comparing catch trials with stimulation trials
Dependent
variable
Alpha X/s Alpha X
Alpha S Not-alpha X/S Not-alpha s Not-alpha X Percent-time
alpha
Mean
catch
1.09 1.25 5.52 < 0.001
0.75 0.59 3.00 < 0.025
0.73 0.52 3.84 < 0.01 1.00 1.17 4.26 i 0.001
2.06 1.96 1.14 _
1.96 2.13 1.46 _
33.9
stimu- lation
26.9
Statistical tests
t (4 13) P (two-tail)
4.32 < 0.001
DISCUSSION
In this experiment, the method of alpha-contin- gent visual stimulation decreased the variability of the durations of not-alpha (alpha-blocking) com- pared to non-contingent (sham feedback condi- tions). This means that alpha-contingent stimula- tion is followed by alpha-blocking responses whose durations have a greater replicative reliability than those obtained with a non-contingent, sham feedback, schedule of stimulation. This result was also found for alpha durations (Goodman et al., 1980). Control of alpha durations with contingent stimulation is always greater than the control of alpha-blocking durations (Mulholland and Eber- lin, 1977; Mulholland and Goodman, 1982). Stat- istical comparisons of measurements from differ- ent experimental conditions should be improved under conditions of contingent stimulation, be- cause ‘noisy’ variations of the dependent variable relative to the Mean is reduced.
For contingent stimulation conditions, the durations of alpha blocking recorded from the derivations contralateral to the visual field of the stimulus were better controlled, i.e. the ratio x/s was greater than that from the ipsilateral field. This result and those reported previously for alpha durations (Goodman et al., 1980) show that the latency and duration of alpha suppression has a greater replicative reliability when the EEG is recorded from a lobe which is the more direct and shorter (fewer synapses) pathway from the hemiretina stimulated compared to EEG’s re- corded from lobes which are the terminus of path- ways from hemiretina which are not direct and longer (Carpenter, 1976).
This interpretation suggests that in EEGs re- corded from lobes which are connected indirectly to the hemiretina by even longer, less direct paths (more synaptic junctions?), the latency and dura- tion of alpha-blocking will have even lower repli- cative reliability. This is, perhaps, the reason for reduced control of latency and duration of alpha-blocking recorded from temporal deriva- tions compared to occipital ones in this study and from parieto-central derivations compared to oc- cipital ones in other experiments (Mulholland and Goodman, 1982).
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Also, in EEG derivations anterior to P-O de- rivations, alpha-blocking is less reliably associated with visual stimuli and oculomotor processes com- pared to other sensory stimuli and motor processes. This is interpreted in terms of other classes of alpha rhythms, e.g. the mu rhythms. The sup- pression of mu and other classes of alpha rhythms shows a functional specialization of temporal and central cortex compared to parietal and occipital cortex (Kuhlman, 1978).
In this study the right-sided EEG is better controlled by stimulation which is contingent with alpha from the right-sided EEG than are left-sided EEG’s when stimulation is contingent with alpha from left-sided EEG. Other experiments however, have shown no evidence for such a difference (Mulholland and Goodman, 1982).
The differences between left- and right-sided EEG’s with regard to control of alpha durations by verbal and non-verbal alpha-contingent visual stimulation, results which were noted in the previ- ous report of this experiment (Goodman et al., 1980) were not found for not-alpha durations. Perhaps the variabiliy of not-alpha durations was too great, even with alpha-contingent visual stimu- lation, to permit a statistically significant dif- ference of control to be observed.
The greater variability and less control (Z/s) of not-alpha durations compared to alpha durations can be discussed in terms of the qualitatively and quantitatively different processes which, during contingent stimulation, determine the specific magnitude of latency and duration of alpha-block- ing. For contingent stimulation, the duration of alpha depends on the time-lag between alpha in the EEG and the onset of stimulation (system ON delay) and the time-lag between the onset of the stimulus and alpha-suppression, i.e. the latency.
The processes which cause or initiate blocking of alpha rhythms, however, are not the same as those which cause a continuance or persistence of alpha-blocking. After alpha-block occurs, many other neurophysiological processes, which are spread out in time, may cascade one after the other or even ‘overlap’ each other, in time, so that alpha-blocking continues.
Among these many and varied processes, any of which can eventuate in alpha-blocking, the
process which arrives first at the cortical locations which are the source of the recorded EEG alpha rhythms, will initiate alpha-blocking and de- termine the latency which most often is near 200 ms.
Following after this initial ‘speediest’ process are other processes related for instance to integra- tive and oculomotor functions which can contrib- ute to alpha-blocking. Their ‘ time of arrival’, how- ever, cannot be detected in the interval of alpha- blocking, perhaps because no unique EEG signal is associated with them, i.e. they overlap in time within the alpha-block which has already started.
The likelihood is that only one or only a few kinds of processes cause an initiation of alpha- blocking; many more and different processes are involved in or cause alpha-blocking to continue. Because they are many, there are many more ways they can be combined or interact and this diver- sity is associated with a greater variability of the duration of alpha-blocking compared to the latency of alpha-blocking even under conditions of alpha-contingent visual stimulation. Thus with alpha-contingent visual stimulation, the lower rep- licative reliability and reduced control of the dura- tions of alpha-blocking compared to the durations of alpha (Goodman et al., 1980) may simply indi- cate that there are a greater number and more different kinds of processes involved in the con- tinuation of alpha-blocking compared to the num- ber and kinds of processes which determine the latency of alpha-blocking.
ACKNOWLEDGEMENTS
This research was supported by V.A. Medical Research Central Office, Washington DC.
REFERENCES
Boudrot, R., Goodman, D.M. and Mulholland, T.B. (1978) An EEG alpha detection feedback stimulation and data analy-
