303
Attention and the EEG Alpha Rhythm in Learning Disabled Children
Peter W. Fuller, PhD
Using several measures of attention, researchers are investigating the ability of LD children to attend to various information while performing different tasks. Technological advances in "reading" EEG (electroencephalogram) brain wave information have made it possible to measure reliably the difference between two persons' brain responses. In light of considerable research showing that the reduction in the percentage of so-called alpha waves relates to attention, this study examines LD children's EEGs for evidence of deficient attentional processes. — G.M.S. Parieto-occipital EEGs were recorded during resting baseline intervals, during an initial instruction period, and during active performance on mental arithmetic and immediate recall tasks to determine if 10 learning disabled boys would show less alpha attenuation than 11 normal controls. Fourier transform power spectral analysis was performed on FM magnetic tape recordings of the EEGs. The logs of the ratio of the average power in each task over the average power in the resting period were then computed. LD boys showed less alpha attenuation than the normal control boys. In addition, control boys responded correctly to more of the problems. Since EEG research has shown attenuation of the parieto-occipital alpha rhythm to be an electrophysiological con-
comitant of attention, these results support the implication that attention deficits play at least some part in learning disabilities.
C
hildren currently termed minimally brain damaged and learning disabled (MBD/ LD) are a heterogeneous population at large. Strother (1973) and others have pointed out the need to reclassify all those now included under this rubric into more specific, homogeneous categories. Even though they constitute a diverse group, MBD/LD children may be alike in certain underlying traits. Defective attention maybe one of those key traits. Certainly, it is almost always incorporated in official definitions of MBD/LD children, such as that of HEW (Clements 1966). Journal of Learning Disabilities
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304 William James (1890) defined attention as follows: Everyone knows what attention is. It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. Focalization, concentration of consciousness are its essence. It implies withdrawal from some things in order to deal effectively with others, and is a condition which is a real opposite in the confused, dazed, scatterbrained state which in French is called "distraction" (pp. 103-104).
alpha attenuation, or blocking, to be highly correlated with certain aspects of attention. The alpha rhythm originally described by Berger (1929, 1931) was recognized by him to decrease amplitude (attenuate) or obliterate (block) with the onset of alert attention. These well-known effects have been regularly described (Adrian and Mathews 1934, Mulholland 1969, Kooi 1971) and have been incorporated into the official definition of alpha rhythm of the International Federation for Electroencephalography and Clinical Neurophysiology. ... rhythm at 8-13Hz occurring during wakefulness over the posterior regions of the head, generally with higher voltage over the occipital areas. Amplitude is variable but mostly below 50/uv in the adult. Best seen with eyes closed or under conditions of physical relaxation and relative mental inactivity. Blocked or attenuated by attention, especially visual and mental effort (Chatrian, Bergamini, Dondey, Klass, LennoxBuchtal, & Petersen 1974, p. 538).
There is no current agreement over a formal definition of attention, and it may not be feasible or desirable to reach such consensus. Attention factors such as span and distractibility in LD children are normally deduced from subjective behavioral reports by teachers or from clinical observations (Hallahan & Cruickshank 1973). There have, however, been a few more systematic investigations of attention deficits and impulsivity. Luria (1959, 1961) used a task with LD children that required them to press a response key to a visual or auditory signal designated positive and not to press the key in response to a negative stimulus. The LD children became disorganized in their responses when the presentation rate was increased sufficiently. The children either did not respond at all or pressed the key impulsively. Dykman, Walls, Suzuki, Ackerman, and Peters (1970) and Dykman, Ackerman, Clements, and Peters (1971) used an impulsivity task that required LD children to depress a key to various arrangements of flashing lights. LD children made more errors and exhibited longer response latencies than control subjects. Dykman and colleagues treated attention as if it were a single trait consisting of four interrelated components: alertness, stimulus selection, focusing, and vigilance. Anderson, Halcomb, and Doyle (1973) also used a vigilance task on which LDs did more poorly than controls.
The subjects were 10 experimental boys, 10.1 to 12.6 years old (Mean = 11.3), and 11 normal control boys, 10.6 to 11.7 years old (Mean= 11.2), from the public school system. The experimental subjects were from special LD classes and the controls were from regular classrooms. A lower age limit of 10 years was decided on because by the tenth year the occipital alpha band is fairly well established at a mean value of 9.5cps, with a range of 8 to lOcps (Brazier 1968, Kooi 1971).
The present study used electrophysiological effect (alpha attenuation) to define objectively and operationally the degree of attending in groups of LD and control children performing tasks involving mental arithmetic and immediate recall. EEG research has consistently shown
The experimental boys were selected from the broad, controversial, and currently loosely defined category of children who exhibit learning disability and minimal brain dysfunction, or LD/MBD. Because of current confusion and disagreement over terminology, the
Thus, if there are attention deficits present in children with learning disabilities, there may be accompanying changes in ability to attenuate to alpha rhythms. The present study was undertaken to determine whether LD children show less alpha attenuation as compared with a matched group of normal control children.
METHOD AND MATERIAL
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305 following eligibility criteria were used to operationally define the term learning disability: (1) A WISC full scale IQ of 90 or above. (2) A minimum of two grade levels low in reading and one grade level low in arithmetic on the Wide Range Achievement Test (WRAT). (3) The presence of attention deficits, distractibility, hyperactivity, or other signs of marked inability to attend, as rated by the teacher and/or specialist on a 5-point rating scale (1 = minimal to 5 = extensive). A rating of 4 or 5 constituted eligibility on this item. (4) No specific visual, hearing, or motor handicaps (established from school records and the participating school specialist, and verified by parent). (5) No history of epilepsy (established from school records and the participating school specialist, and verified by parent). (6) No brain injury (established from school records and the participating school specialist, and verified by parent). The control subjects were matched with experimental subjects on all of the above criteria, except items 2 and 3. Controls performed at expected levels for age and grade on the Metropolitan Achievement Test (MAT) and showed no evidence of marked inability to attend. Adherence to the federal Family Education Rights and Privacy Act and local district policy prevented investigators from establishing means and standard deviations for individual scores. However, all of the above items appeared in the selection data form completed by school personnel and parents during the selection process. All EEG recordings were made in a shielded room with the child sitting in a chair. A Beckman Accutrace eight-channel electroencephalograph was used. Nine-millimeter tin disc electrodes (developed at the Mayo Clinic) filled with conducting jelly were placed on the scalp according to the International 10-20 system at Pi, P4, Oi, and 0 2 , and an electrode near Cz served as ground. The above electrode placements constituted two bipolar parieto-occipital
derivations for the left and right hemispheres, respectively. The EEGs were recorded at a sensitivity of 7.5/zv/mm with a frequency band of 0.5-50cps (-3dB) at a paper speed of 30mm/sec. The EEG was also recorded on a Hewlett-Packard FM instrumentation tape recorder. The experimenter explained to each child how the recording was done and each step in preparation, and the child was encouraged to talk about his expectations to minimize anxiety. Each child was also told that he would receive two dollars for participating in the experiment and doing the tasks, but he could decide not to participate at any time. After the child was seated and the electrodes were in place, each subject was instructed to sit quietly with his eyes closed while a five-minute baseline recording was made. The child was also requested twice, toward the end of this recording, to open his eyes and look directly ahead at a designated point on the wall for a few seconds and then to close his eyes. This was done to determine the degree of each subject's alpha attenuating ability. The research assistant explained to each subject that he would be following taped instructions and then gave one sample practice problem from each of three sets: (1) recall, (2) pure addition, and (3) arithmetic word problems. The following are examples: (1) pie — ice cream — cake — candy — cookies (in the order given) (2) 6 + 6 + 3 + 5 + 9 (3) If James has 25 cents and spends 15 cents on penny candy, how many cents are left? Cotton balls were taped over the subjects' eyes, and the programmed taped instructions and problems were begun as follows: Listen closely to the sound of my voice. You are going to be given some problems you will do in your head. There will be three groups of problems with a short rest in between. You will only hear the problem once. You must then answer as soon as you have the answer and then listen for the next problem. You cannot ask for the problem to be repeated or for the instruction to be stopped. If you do not have the answer when the next problem starts, go on to the next new problem. Journal of Learning Disabilities
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306
TABLE I. Mean log ratios of the average EEG power during each task to the average EEG power during the resting period, i.e., log (PT/PR) * for each group for each task.
Controls (normal children)
Experimentals (LD children)
-0.096 -0.089 -0.101
0.000 0.047 -0.024
Ti — Immediate recall T2 — Mental arithmetic T3 — Initial instructions
*PT = mean power of the alpha frequency during task work time PR = mean power of the alpha frequency during the resting time
Half of the subjects heard instruction tape A and the other half tape B. The order of the computational and reasoning requirements was reversed on the two tapes to balance them for any order effect. Problems were chosen that involved reasoning and pure addition to ensure that the tasks were relevant to language skills as well as arithmetic skills. The entire procedure, including practice and actual tasks, took just under an hour on the average. On completion, recordings were checked, and those that did not have the following characteristics were eliminated from the study: (1) a resting average alpha frequency between 8 and 13cps. (2) attenuation with the eyes open as opposed to closed during the baseline recording. Alpha attenuation was scored when there was a manually measured amplitude decrease of at least 75% when the eyes were opened for at least 0.2 seconds, a phenomenon termed blocking by Mulholland and Pepper (1971) and Mulholland (1972). Ten out of 13 experimental subjects and 11 out of 14 control subjects satisfactorily met the above criteria. The FM magnetic tape was then digitized at 200 samples per second. The digitized data were analyzed on a Raytheon 704 computer using the Radix 2 Fast Fourier Transform Program RFT 1
(Cooley & Tukey 1965). The EEG data from channels 1 and 2 were transformed in blocks of 256 samples (1.28 sec) to produce power spectra that were band-averaged separately for the theta, alpha, and beta bands for each of the two channels. Channel 3 was a marker channel. All EEG data recorded during problem working were analyzed, and all nonproblem EEG data were deleted. The computer output was checked for artifacts against the direct written polygraph records and disregarded in the final average, if any were present. The average (mean) power* was calculated for the immediate recall task (Ti), mental arithmetic (T2), the initial taped instruction period (T3), and the baseline resting interval for the alpha band of the left hemisphere (channel 2). The left side was used because language and arithmetic tasks have been shown to engage the left hemisphere primarily (Galin & Ornstein 1972, Doyle, Ornstein, & Galin 1974). To control for an observable, large, betweenindividual variability in EEG average power in all conditions, a more meaningful variable was used — the ratio of average power during the various tasks to the power during the resting condition. Use of the ratio is possible because •Power is the integral of the square of the amplitude, or voltage, divided by the resistance, P = E2/R; thus the greater the amplitude at a specified frequency, the greater the power.
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307 TABLE II. Ratios of average EEG power during each of three tasks to the average EEG power of the rest period for the experimental LD children and normal controls.
T,
Experimental
Control
T2
T,
Immediate recall
Mental arithmetic
Initial instructions
2 3 4 5 6 7 8 9 10
1.07 .95 .94 1.04 .96 1.13 .90 1.02 1.04 .97
1.02 1.11 .93 1.12 1.01 1.21 .89 1.08 1.16 .99
1.02 .87 .89 1.05 .96 .96 1.14 1.02 .93 .96
Mean
1.00
1.05
.98
1 2 3 4 5 6 7 8 9 10 11
.89 .96 .91 1.03 .93 .87 .91 .98 .83 .80 .92
.87 .97 .89 .96 .99 .89 .88 .89 .89 .87 .98
.93 .88 .89 .97 .78 1.00 .93 .86 .86 .90 .94
Mean
.91
.92
.91
1
power may be described as a ratio scale, that is, a scale with an absolute zero point. The ratios were transformed to better meet the assumption of multivariate normality (Morrison 1967), by taking the natural logarithm of the above ratios (see Table I). The Hotelling T 2 test was used to determine whether the two groups arose from populations with common means.
RESULTS The LD group selected for observed attention deficits showed less alpha attenuation than the normal control group. For tasks Ti and T2 and
the initial instruction period T3 combined, the difference between LD and control groups in EEG alpha attenuation was significant at the .001 level (T2=30.1; F=8.99; d/=3, 17). Directional differences in means between LD and control children were uniform over the three conditions. Table I shows the mean score for LD and normal control boys in each condition. Negative scores in this table signify alpha attenuation during the task condition. The control group, but not the LD group, showed alpha attenuation in the Ti and T2 conditions, and the control group showed greater alpha attenuation in the T3 condition than
48
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308 TABLE the
HI. Simultaneous
confidence
experimental population
intervals
mean as shown 95% Interval
1
for the control in
population mean
minus
Table L 90% Interval
75% Interval
Ti — Immediate recall
(-.198, +.006) width:.209 Includes 0 not significant
(-.185, -.007) width: .175 Excludes 0 significant
(-.166, -.026) width: .140 Excludes 0 significant
T : — Mental arithmetic
(-.246, -.026) width:.220 Excludes 0 significant
(-.232, -.040) width: .192 Excludes 0 significant
(-.212, -.060) width: .152 Excludes 0 significant
Tj — Initial instructions
(-.183, +.029) width:.212 Includes 0 not significant
(-.169, +.019) width: .188 Includes 0 not significant
(-.149, -.005) width: .144 Excludes 0 significant
did the LD group. Table II shows data for each individual, as well as the group means. Eight of the 10 experimental LD boys failed to show alpha attenuation in one or more of the three conditions, while 9 of the 11 normal control boys showed alpha attenuation in all three conditions. Using Fisher's exact test for a Z-by-Z contingency table, this difference is statistically significant at the .01 level (Beyer 1968). To determine the statistical significance of the group differences in the three conditions separately, simultaneous confidence intervals were computed (Morrison 1967). This statistical method takes into account the nonindependence of scores for each subject across the three conditions. Table III shows that the alpha attenuation difference between LD and normal control boys was significantly different at the .05 level for the mental arithmetic (T2) condition. The immediate recall (Ti) condition had a p < .10 but did not reach the .05 significance level. For the initial instruction condition (T3), the difference was not significant at the .05 level. Tables IV, V, and VI show the considerable overlap and separation of scores of the two groups in the three conditions.
In addition to greater alpha attenuation, the normal control children responded correctly to more problems than did the LD children. On the average the control group correctly answered 12 of the 16 problems; the LD boys averaged 7 correct responses.
DISCUSSION This research shows that the EEG alpha activity of normal boys a t t e n u a t e d more during experimental tasks in this study than did the alpha activity of the experimental group. Table II shows that this difference occurred in all conditions studied. Tables IV, V, and VI show that, although the group means differed in the expected direction in all three conditions, there was considerable overlap in the individual scores in conditions Ti and T 3 . Only on T2 (mental arithmetic) were the groups consistently different, with only two LD boys having scores that overlapped with the scores of control group boys (Table V). That the greatest group differences were found during the mental arithmetic test is not surprising, because it is safe to say that the mental arithmetic demanded the
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309 TABLE IV. Ratios of average EEG power during immediate recall task to average EEG power during rest period showing individual subjects in order from least to most alpha attenuation. Subject number
E6 E1 E4 E9 C4 E8 C8 E10 E5 C2 E2 E3 C5 C11 C3 07
E7 C1 C6 C9 C10
Rank
t
2 3.5 3.5 5 6 7 8 9.5 9.5 11 12 13 14 15.5 15.5 17 18 19 20 21
most mental effort, and thus the most potential alpha attenuation as a physiological response to the mental effort. Thus, the potential for differences would be maximized between those subjects who had attended well and those who did not on the arithmetic task. These differences were statistically significant for the three conditions combined, and for T2 separately, but not for Ti or T3 considered separately. Since the groups contained only 10 and 11 subjects, additional data from further experimentation are needed to determine whether the observed trends would be confirmed if the number of subjects were larger. It should also be pointed out that all the LD children studied had marked attentional defects as measured by behavioral criteria. Thus, the results might not hold in a larger more heterogeneous group of LD
Experimental group
Score
\
Control group
1.13 1.07 1.04 1.04 1.03 1.02 .98 .97 .96 .96 .95 .94 .93 .92 .91 .91 .90 .89 .87 .83 .80
children. On the other hand, regarding attentional and perceptional cognitive function in the LD population additionally defined as MBD, Wender (1971) has said: "The most striking and constant perceptional-cognitive abnormality of the MBD child is shortness of attention span and poor concentration ability." EEG research has shown that alpha attenuation is a concomitant of attention and mental effort (Glass 1959,1960,1964); therefore, the results of this experiment are consistent with the possibility of attention deficits in these LD children. Such deficits could result from a number of causes. It is possible that (1) specific neurological dysfunction in LD children interferes with the focusing- of attention and therefore leads to less alpha attenuation; (2) some LD children may be slow to mature in Journal of Learning Disabilities
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310 I
TABLE V. Ratios of average EEG power during mental arithmetic task to the average EEG power during rest period showing individual subjects in order from least to most alpha attenuation.
I
Subject number
Rank
E6 E9 E4 E2 E8 E1 E5 E10 C5 C11 C2 C4 E3 E7 C3 C6 C8 C9 C7 C1 C10
1 2 3 4 5 6 7 8 8 10 11 12 13 14.5 14.5 14.5 14.5 14.5 19 20.5 20.5
CNS function, their maturational lag accounting for both an attention deficit and less alpha attenuation; (3) the observed differences are of psychological rather than neurological origin; or (4) some combination of the above three possibilities may pertain. Further research is needed to determine the relative importance of these possibilities; more precise understanding of cognitive functioning will help us to understand these relationships. Research in this area has been hampered by the use of inconsistent criteria in diagnosing learning disabilities. In LD children brain damage or trauma is often not observable, a clearly defined medical syndrome has not been established, and almost all definitions have relied totally on behavioral criteria. Furthermore, traditional approaches to EEG research may not
Experimental group
Score
Control group
1.21 1.16 1.12 1.11 1.08 1.02 1.01 .99 .99 .98 .97 .96 .93 .89 .89 .89 .89 .89 .88 .87 .87
be particularly rewarding with LD children. Findings in this area vary (Daveau 1959, Satterfield, Cantwell, Lesser, & Podosin 1972, Capute, Neidermeyer, & Richardson 1968). Previous studies of the relationship between mental abilities and EEG "have been hampered by a rigid adherence to traditional methodological approaches" (Vogel, Broverman, & Klaiber 1968, p. 166), and similar criticisms have been stated by Vogel and Broverman (1964,1966) and Mundy-Castle (1957). Vogel and Broverman (1964) argued that EEG measurements taken during an active intellectual effort would most probably show the greatest relationship to cognitive measurements. Furthermore, Brazier has stated that: ... the development from the concept of the electroencephalogram as primarily an aid in
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311 I TABLE VI. Ratios of average EEG power during the initial instruction period to the average EEG power during the rest period showing the subjects in order from least to most alpha attenuation. Subject number
Rank
E7 E4 E1 E8 C6 C4 E5 E6 E10 C11 E9 C1 C7 C10 E3 C3 C2 C9 E2 C8 C5
1 2 3.5 3.5 5 6 7.5 7.5 7.5 10 11.5 11.5 11.5 14 15.5 15.5 17.5 17.5 19 20 21
assessing the normality of the resting "inactive" brain to a dynamic formulation of it as an indicator of the brain in action, has, with its emphasis on function rather than on morphology, suggested a wider application of the EEG to the study of behavior. (1968, p. 302) Thus, it is relevant and feasible to explore disturbances of attention in LD children in relation to EEG parameters while the children are actively attending to stimuli analogous to those that are difficult in the school learning environment. A search for anomalous responses to stimuli might be expected to yield better results than the search for abnormal characteristics in the resting EEG. Therefore, the purpose of this study was to begin exploration of an objective physiological concomitant of attention in LD and control children. It should, however, be noted that EEG analysis by computer power spectral analysis is
Score
Experimental group
|
Control group
1.14 1.05 1.02 1.02 1.00 .97 .96 .96 .96 .94 .93 .93 .93 .90 .89 .89 .88 .88 .87 .86 .78
prohibitively expensive and thus impractical for routine clinical use. I look forward, though, to one day in the near future when microprocessors will be built into electroencephalographs and give immediate, inexpensive readouts. ABOUT THE
AUTHOR
Peter W. Fuller, research assistant professor at the Child Development and Mental Retardation Center, University of Washington, received his doctorate in clinical psychology from the Wright Institute, Berkeley, California. He is currently a postdoctoral intern at the Parent/Child Learning Clinic, Department of Psychiatry and Behavioral Sciences, University of Washington. Dr. Fuller has also been a research fellow in the Division of Neuropathology, University of Washington School of Medicine. ACKNOWLEDGMENT Special thanks are extended to Dr. Charles R. Strother, Professor Emeritus, Psychology and Psychiatry, University of Washington, for his advisory role in the design of this study, which was submitted to the Wright Institute in Berkeley in
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312 partial fulfillment of the requirements for a doctoral degree, and for his repeated critical reviews during the development of the present manuscript.
REFERENCES Adrian, E.D., Mathews, B.H.C.: The Berger rhythm: Potential changes from the occipital lobe in man. Brain, 1934, 57, 355-385. Anderson, R.P., Halcomb, C.G., Doyle, R.B.: The measurement of attentional deficits. Exceptional Child, 1973, 39, 534-539. Berger, //.. Ueber des Elektrenkephelogramm des Menchen. Archiv fur Psychiatrie und Nervenkrankheiten, 1929, 87, 527-570. Berger, H.. Ueber des Elektrenkephelogramm des Menchen. Archiv fur Psychiatrie und Nervenkrankheiten, 1931, 94, 16-60. Beyer, W. (Ed.): Handbook of Tables for Probability and Statistics. 2nd ed. New York: The Chemical Rubber Co., 1968, Table III, Sec. 11. Brazier, M.A.B.: The Electrical Activity of the Nervous System. 3rd ed. Baltimore: Williams 6- Wilkins, 1968. Capute, A.J., Neidermeyer, E.F.L., Richardson, F.: The electroencephalogram in children with minimal cerebral dysfunction. Pediatrics, 1968, 6, 1104-1114. Chatrian, G.E., Bergamini, L., Dondey, M., Klass, D.W., Ijennox-Buchthal, M., Petersen, I.: A glossary of terms most commonly used by clinical electroencephalographers. Electroencephalography and Clinical Neurophysiology, 1974, 37, 538-548. Clements, S.D.: Minimal brain dysfunction in children: Terminology and identification. NINDS Monograph No. 3, U.S. Public Health Service Publication No. 1415. Washington, DC: U.S. Government Printing Office, 1966. Cooley, J.W., Tukey, J.W.: An algorithm for the machine calculation of complex Fourier series. Mathematics of Computation, 1965, 19, 297-301. Daveau, M.: The EEG of 150 children with behavior disorders. Electroencephalography and Clinical Neurophysiology, 1959,10,198. Doyle, J.C., Ornstein, R., Galin, D.: Lateral specialization of cognitive mode: EEG frequency analysis. Psychophysiology, 1974, 2, 567-587. Dykman, R., Walls, R., Suzuki, T., Ackerman, P., Peters, J.E.: Children with learning disabilities: Conditioning differentiation, and the effect of distraction. American Journal of Orthopsychiatry, 1970, 40, 766-781. Dykman, R.A., Ackerman, P.T., Clements, S.D., Peters, J.E.: Specific learning disabilities: An attentional deficit syndrome. In H.R. Myklebust (Ed.): Progress in learning Disabilities, Vol. 2. New York: Grune 6- Stratton, 1971, pp. 56-93.
Galin, D., Ornstein, R.: Lateral specialization of cognitive mode: an EEG study. Psychophysiology, 1972,9,412-418. Glass, A.: Blocking of the occipital alpha rhythm and problemsolving efficiency. Electroencephalography and Clinical Neurophysiology, 1959, 11, 605. Glass, A.: Motivation and the intensity of blocking to problemsolving. Electroencephalography and Clinical Neurophysiology, 1960,12, 262. Glass, A.: Mental arithmetic and blocking of the alpha rhythm. Electroencephalography and Clinical Neurophysiology, 1964,16, 595-603. Hallahan, D.P., Cruickshank, W.M.: Psychoeducational Foundations of Learning Disabilities. Englewood Cliffs, N.J.: Prentice-Hall, 1973. James, W.: The Principles of Psychology. NewYork: Holt, 1980. Kooi, K.A.: Fundamentals of Electroencephalography. New York: Harper and Row, 1971. Luria, A.R.: Experimental study of the higher nervous activity of the abnormal child. Journal of Mental Deficiency Research, 1959, 3,1-22. Luria, A.R.: The Role of Speech in the Regulation of Normal and Abnormal Behavior. New York: Liveright, 1961. Morrison, D.F.: Multivariate Statistical Methods. New York: McGraw-Hill, 1967. Mulholland, T.B.: The concept of attention and the electroencephalographic alpha rhythm. In C.R. Evans and T.B. Mulholland (Eds.): Attention in Neurophysiology. London: Butterworth 6 Co., 1969. Mulholland, T.B.: Occipital alpha revised. Psychological Bulletin, 1972, 78,178-182. Mulholland, T.B., Peper, E.: Occipital alpha and accommodative vergence, pursuit-tracking and fast eye movements. In J. Stoyua (Ed.): Biofeedback and Self Control. New York: Aldine-Atherton, 1971. Mundy-Castle, A.C.: The electroencephalogram and mental activity. Electroencephalography and Clinical Neurophysiology, 1957, 9, 643-655. Satterfield, J.H., Cantwell, DP., Lesser, L.I., Podosin, R.L.: Physiological studies of the hyperkinetic child. American Journal of Psychiatry, 1972, 128, 1418-1424. Strother, C.R.: Minimal cerebral dysfunction: A historical overview. Minimal Brain Dysfunction. Annals of the New York Academy of Sciences, 1973, 205, 6-17. Vogel, W., Broverman, D.M.: Relationship between EEG and test intelligence: A critical review. Psychological Bulletin, 1964, 62,132-144. Vogel, W., Broverman, D.M.: A reply to "relationship between EEG and test intelligence: A commentary." Psychological Bulletin, 1966, 65, 99-109. Vogel, W., Broverman, DM., Klaiber, E.L.: EEG and mental abilities. Electroencephalography and Clinical Neurophysiology, 1968, 24, 166-175. Wender, P.H.: Minimal Brain Dysfunction in Children. New York: John Wiley 6 Sons, 1971.
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Attention and the EEG Alpha Rhythm in Learning Disabled Children
Peter W. Fuller, PhD
Using several measures of attention, researchers are investigating the ability of LD children to attend to various information while performing different tasks. Technological advances in "reading" EEG (electroencephalogram) brain wave information have made it possible to measure reliably the difference between two persons' brain responses. In light of considerable research showing that the reduction in the percentage of so-called alpha waves relates to attention, this study examines LD children's EEGs for evidence of deficient attentional processes. — G.M.S. Parieto-occipital EEGs were recorded during resting baseline intervals, during an initial instruction period, and during active performance on mental arithmetic and immediate recall tasks to determine if 10 learning disabled boys would show less alpha attenuation than 11 normal controls. Fourier transform power spectral analysis was performed on FM magnetic tape recordings of the EEGs. The logs of the ratio of the average power in each task over the average power in the resting period were then computed. LD boys showed less alpha attenuation than the normal control boys. In addition, control boys responded correctly to more of the problems. Since EEG research has shown attenuation of the parieto-occipital alpha rhythm to be an electrophysiological con-
comitant of attention, these results support the implication that attention deficits play at least some part in learning disabilities.
C
hildren currently termed minimally brain damaged and learning disabled (MBD/ LD) are a heterogeneous population at large. Strother (1973) and others have pointed out the need to reclassify all those now included under this rubric into more specific, homogeneous categories. Even though they constitute a diverse group, MBD/LD children may be alike in certain underlying traits. Defective attention maybe one of those key traits. Certainly, it is almost always incorporated in official definitions of MBD/LD children, such as that of HEW (Clements 1966). Journal of Learning Disabilities
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304 William James (1890) defined attention as follows: Everyone knows what attention is. It is the taking possession by the mind, in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. Focalization, concentration of consciousness are its essence. It implies withdrawal from some things in order to deal effectively with others, and is a condition which is a real opposite in the confused, dazed, scatterbrained state which in French is called "distraction" (pp. 103-104).
alpha attenuation, or blocking, to be highly correlated with certain aspects of attention. The alpha rhythm originally described by Berger (1929, 1931) was recognized by him to decrease amplitude (attenuate) or obliterate (block) with the onset of alert attention. These well-known effects have been regularly described (Adrian and Mathews 1934, Mulholland 1969, Kooi 1971) and have been incorporated into the official definition of alpha rhythm of the International Federation for Electroencephalography and Clinical Neurophysiology. ... rhythm at 8-13Hz occurring during wakefulness over the posterior regions of the head, generally with higher voltage over the occipital areas. Amplitude is variable but mostly below 50/uv in the adult. Best seen with eyes closed or under conditions of physical relaxation and relative mental inactivity. Blocked or attenuated by attention, especially visual and mental effort (Chatrian, Bergamini, Dondey, Klass, LennoxBuchtal, & Petersen 1974, p. 538).
There is no current agreement over a formal definition of attention, and it may not be feasible or desirable to reach such consensus. Attention factors such as span and distractibility in LD children are normally deduced from subjective behavioral reports by teachers or from clinical observations (Hallahan & Cruickshank 1973). There have, however, been a few more systematic investigations of attention deficits and impulsivity. Luria (1959, 1961) used a task with LD children that required them to press a response key to a visual or auditory signal designated positive and not to press the key in response to a negative stimulus. The LD children became disorganized in their responses when the presentation rate was increased sufficiently. The children either did not respond at all or pressed the key impulsively. Dykman, Walls, Suzuki, Ackerman, and Peters (1970) and Dykman, Ackerman, Clements, and Peters (1971) used an impulsivity task that required LD children to depress a key to various arrangements of flashing lights. LD children made more errors and exhibited longer response latencies than control subjects. Dykman and colleagues treated attention as if it were a single trait consisting of four interrelated components: alertness, stimulus selection, focusing, and vigilance. Anderson, Halcomb, and Doyle (1973) also used a vigilance task on which LDs did more poorly than controls.
The subjects were 10 experimental boys, 10.1 to 12.6 years old (Mean = 11.3), and 11 normal control boys, 10.6 to 11.7 years old (Mean= 11.2), from the public school system. The experimental subjects were from special LD classes and the controls were from regular classrooms. A lower age limit of 10 years was decided on because by the tenth year the occipital alpha band is fairly well established at a mean value of 9.5cps, with a range of 8 to lOcps (Brazier 1968, Kooi 1971).
The present study used electrophysiological effect (alpha attenuation) to define objectively and operationally the degree of attending in groups of LD and control children performing tasks involving mental arithmetic and immediate recall. EEG research has consistently shown
The experimental boys were selected from the broad, controversial, and currently loosely defined category of children who exhibit learning disability and minimal brain dysfunction, or LD/MBD. Because of current confusion and disagreement over terminology, the
Thus, if there are attention deficits present in children with learning disabilities, there may be accompanying changes in ability to attenuate to alpha rhythms. The present study was undertaken to determine whether LD children show less alpha attenuation as compared with a matched group of normal control children.
METHOD AND MATERIAL
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305 following eligibility criteria were used to operationally define the term learning disability: (1) A WISC full scale IQ of 90 or above. (2) A minimum of two grade levels low in reading and one grade level low in arithmetic on the Wide Range Achievement Test (WRAT). (3) The presence of attention deficits, distractibility, hyperactivity, or other signs of marked inability to attend, as rated by the teacher and/or specialist on a 5-point rating scale (1 = minimal to 5 = extensive). A rating of 4 or 5 constituted eligibility on this item. (4) No specific visual, hearing, or motor handicaps (established from school records and the participating school specialist, and verified by parent). (5) No history of epilepsy (established from school records and the participating school specialist, and verified by parent). (6) No brain injury (established from school records and the participating school specialist, and verified by parent). The control subjects were matched with experimental subjects on all of the above criteria, except items 2 and 3. Controls performed at expected levels for age and grade on the Metropolitan Achievement Test (MAT) and showed no evidence of marked inability to attend. Adherence to the federal Family Education Rights and Privacy Act and local district policy prevented investigators from establishing means and standard deviations for individual scores. However, all of the above items appeared in the selection data form completed by school personnel and parents during the selection process. All EEG recordings were made in a shielded room with the child sitting in a chair. A Beckman Accutrace eight-channel electroencephalograph was used. Nine-millimeter tin disc electrodes (developed at the Mayo Clinic) filled with conducting jelly were placed on the scalp according to the International 10-20 system at Pi, P4, Oi, and 0 2 , and an electrode near Cz served as ground. The above electrode placements constituted two bipolar parieto-occipital
derivations for the left and right hemispheres, respectively. The EEGs were recorded at a sensitivity of 7.5/zv/mm with a frequency band of 0.5-50cps (-3dB) at a paper speed of 30mm/sec. The EEG was also recorded on a Hewlett-Packard FM instrumentation tape recorder. The experimenter explained to each child how the recording was done and each step in preparation, and the child was encouraged to talk about his expectations to minimize anxiety. Each child was also told that he would receive two dollars for participating in the experiment and doing the tasks, but he could decide not to participate at any time. After the child was seated and the electrodes were in place, each subject was instructed to sit quietly with his eyes closed while a five-minute baseline recording was made. The child was also requested twice, toward the end of this recording, to open his eyes and look directly ahead at a designated point on the wall for a few seconds and then to close his eyes. This was done to determine the degree of each subject's alpha attenuating ability. The research assistant explained to each subject that he would be following taped instructions and then gave one sample practice problem from each of three sets: (1) recall, (2) pure addition, and (3) arithmetic word problems. The following are examples: (1) pie — ice cream — cake — candy — cookies (in the order given) (2) 6 + 6 + 3 + 5 + 9 (3) If James has 25 cents and spends 15 cents on penny candy, how many cents are left? Cotton balls were taped over the subjects' eyes, and the programmed taped instructions and problems were begun as follows: Listen closely to the sound of my voice. You are going to be given some problems you will do in your head. There will be three groups of problems with a short rest in between. You will only hear the problem once. You must then answer as soon as you have the answer and then listen for the next problem. You cannot ask for the problem to be repeated or for the instruction to be stopped. If you do not have the answer when the next problem starts, go on to the next new problem. Journal of Learning Disabilities
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306
TABLE I. Mean log ratios of the average EEG power during each task to the average EEG power during the resting period, i.e., log (PT/PR) * for each group for each task.
Controls (normal children)
Experimentals (LD children)
-0.096 -0.089 -0.101
0.000 0.047 -0.024
Ti — Immediate recall T2 — Mental arithmetic T3 — Initial instructions
*PT = mean power of the alpha frequency during task work time PR = mean power of the alpha frequency during the resting time
Half of the subjects heard instruction tape A and the other half tape B. The order of the computational and reasoning requirements was reversed on the two tapes to balance them for any order effect. Problems were chosen that involved reasoning and pure addition to ensure that the tasks were relevant to language skills as well as arithmetic skills. The entire procedure, including practice and actual tasks, took just under an hour on the average. On completion, recordings were checked, and those that did not have the following characteristics were eliminated from the study: (1) a resting average alpha frequency between 8 and 13cps. (2) attenuation with the eyes open as opposed to closed during the baseline recording. Alpha attenuation was scored when there was a manually measured amplitude decrease of at least 75% when the eyes were opened for at least 0.2 seconds, a phenomenon termed blocking by Mulholland and Pepper (1971) and Mulholland (1972). Ten out of 13 experimental subjects and 11 out of 14 control subjects satisfactorily met the above criteria. The FM magnetic tape was then digitized at 200 samples per second. The digitized data were analyzed on a Raytheon 704 computer using the Radix 2 Fast Fourier Transform Program RFT 1
(Cooley & Tukey 1965). The EEG data from channels 1 and 2 were transformed in blocks of 256 samples (1.28 sec) to produce power spectra that were band-averaged separately for the theta, alpha, and beta bands for each of the two channels. Channel 3 was a marker channel. All EEG data recorded during problem working were analyzed, and all nonproblem EEG data were deleted. The computer output was checked for artifacts against the direct written polygraph records and disregarded in the final average, if any were present. The average (mean) power* was calculated for the immediate recall task (Ti), mental arithmetic (T2), the initial taped instruction period (T3), and the baseline resting interval for the alpha band of the left hemisphere (channel 2). The left side was used because language and arithmetic tasks have been shown to engage the left hemisphere primarily (Galin & Ornstein 1972, Doyle, Ornstein, & Galin 1974). To control for an observable, large, betweenindividual variability in EEG average power in all conditions, a more meaningful variable was used — the ratio of average power during the various tasks to the power during the resting condition. Use of the ratio is possible because •Power is the integral of the square of the amplitude, or voltage, divided by the resistance, P = E2/R; thus the greater the amplitude at a specified frequency, the greater the power.
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307 TABLE II. Ratios of average EEG power during each of three tasks to the average EEG power of the rest period for the experimental LD children and normal controls.
T,
Experimental
Control
T2
T,
Immediate recall
Mental arithmetic
Initial instructions
2 3 4 5 6 7 8 9 10
1.07 .95 .94 1.04 .96 1.13 .90 1.02 1.04 .97
1.02 1.11 .93 1.12 1.01 1.21 .89 1.08 1.16 .99
1.02 .87 .89 1.05 .96 .96 1.14 1.02 .93 .96
Mean
1.00
1.05
.98
1 2 3 4 5 6 7 8 9 10 11
.89 .96 .91 1.03 .93 .87 .91 .98 .83 .80 .92
.87 .97 .89 .96 .99 .89 .88 .89 .89 .87 .98
.93 .88 .89 .97 .78 1.00 .93 .86 .86 .90 .94
Mean
.91
.92
.91
1
power may be described as a ratio scale, that is, a scale with an absolute zero point. The ratios were transformed to better meet the assumption of multivariate normality (Morrison 1967), by taking the natural logarithm of the above ratios (see Table I). The Hotelling T 2 test was used to determine whether the two groups arose from populations with common means.
RESULTS The LD group selected for observed attention deficits showed less alpha attenuation than the normal control group. For tasks Ti and T2 and
the initial instruction period T3 combined, the difference between LD and control groups in EEG alpha attenuation was significant at the .001 level (T2=30.1; F=8.99; d/=3, 17). Directional differences in means between LD and control children were uniform over the three conditions. Table I shows the mean score for LD and normal control boys in each condition. Negative scores in this table signify alpha attenuation during the task condition. The control group, but not the LD group, showed alpha attenuation in the Ti and T2 conditions, and the control group showed greater alpha attenuation in the T3 condition than
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308 TABLE the
HI. Simultaneous
confidence
experimental population
intervals
mean as shown 95% Interval
1
for the control in
population mean
minus
Table L 90% Interval
75% Interval
Ti — Immediate recall
(-.198, +.006) width:.209 Includes 0 not significant
(-.185, -.007) width: .175 Excludes 0 significant
(-.166, -.026) width: .140 Excludes 0 significant
T : — Mental arithmetic
(-.246, -.026) width:.220 Excludes 0 significant
(-.232, -.040) width: .192 Excludes 0 significant
(-.212, -.060) width: .152 Excludes 0 significant
Tj — Initial instructions
(-.183, +.029) width:.212 Includes 0 not significant
(-.169, +.019) width: .188 Includes 0 not significant
(-.149, -.005) width: .144 Excludes 0 significant
did the LD group. Table II shows data for each individual, as well as the group means. Eight of the 10 experimental LD boys failed to show alpha attenuation in one or more of the three conditions, while 9 of the 11 normal control boys showed alpha attenuation in all three conditions. Using Fisher's exact test for a Z-by-Z contingency table, this difference is statistically significant at the .01 level (Beyer 1968). To determine the statistical significance of the group differences in the three conditions separately, simultaneous confidence intervals were computed (Morrison 1967). This statistical method takes into account the nonindependence of scores for each subject across the three conditions. Table III shows that the alpha attenuation difference between LD and normal control boys was significantly different at the .05 level for the mental arithmetic (T2) condition. The immediate recall (Ti) condition had a p < .10 but did not reach the .05 significance level. For the initial instruction condition (T3), the difference was not significant at the .05 level. Tables IV, V, and VI show the considerable overlap and separation of scores of the two groups in the three conditions.
In addition to greater alpha attenuation, the normal control children responded correctly to more problems than did the LD children. On the average the control group correctly answered 12 of the 16 problems; the LD boys averaged 7 correct responses.
DISCUSSION This research shows that the EEG alpha activity of normal boys a t t e n u a t e d more during experimental tasks in this study than did the alpha activity of the experimental group. Table II shows that this difference occurred in all conditions studied. Tables IV, V, and VI show that, although the group means differed in the expected direction in all three conditions, there was considerable overlap in the individual scores in conditions Ti and T 3 . Only on T2 (mental arithmetic) were the groups consistently different, with only two LD boys having scores that overlapped with the scores of control group boys (Table V). That the greatest group differences were found during the mental arithmetic test is not surprising, because it is safe to say that the mental arithmetic demanded the
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309 TABLE IV. Ratios of average EEG power during immediate recall task to average EEG power during rest period showing individual subjects in order from least to most alpha attenuation. Subject number
E6 E1 E4 E9 C4 E8 C8 E10 E5 C2 E2 E3 C5 C11 C3 07
E7 C1 C6 C9 C10
Rank
t
2 3.5 3.5 5 6 7 8 9.5 9.5 11 12 13 14 15.5 15.5 17 18 19 20 21
most mental effort, and thus the most potential alpha attenuation as a physiological response to the mental effort. Thus, the potential for differences would be maximized between those subjects who had attended well and those who did not on the arithmetic task. These differences were statistically significant for the three conditions combined, and for T2 separately, but not for Ti or T3 considered separately. Since the groups contained only 10 and 11 subjects, additional data from further experimentation are needed to determine whether the observed trends would be confirmed if the number of subjects were larger. It should also be pointed out that all the LD children studied had marked attentional defects as measured by behavioral criteria. Thus, the results might not hold in a larger more heterogeneous group of LD
Experimental group
Score
\
Control group
1.13 1.07 1.04 1.04 1.03 1.02 .98 .97 .96 .96 .95 .94 .93 .92 .91 .91 .90 .89 .87 .83 .80
children. On the other hand, regarding attentional and perceptional cognitive function in the LD population additionally defined as MBD, Wender (1971) has said: "The most striking and constant perceptional-cognitive abnormality of the MBD child is shortness of attention span and poor concentration ability." EEG research has shown that alpha attenuation is a concomitant of attention and mental effort (Glass 1959,1960,1964); therefore, the results of this experiment are consistent with the possibility of attention deficits in these LD children. Such deficits could result from a number of causes. It is possible that (1) specific neurological dysfunction in LD children interferes with the focusing- of attention and therefore leads to less alpha attenuation; (2) some LD children may be slow to mature in Journal of Learning Disabilities
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310 I
TABLE V. Ratios of average EEG power during mental arithmetic task to the average EEG power during rest period showing individual subjects in order from least to most alpha attenuation.
I
Subject number
Rank
E6 E9 E4 E2 E8 E1 E5 E10 C5 C11 C2 C4 E3 E7 C3 C6 C8 C9 C7 C1 C10
1 2 3 4 5 6 7 8 8 10 11 12 13 14.5 14.5 14.5 14.5 14.5 19 20.5 20.5
CNS function, their maturational lag accounting for both an attention deficit and less alpha attenuation; (3) the observed differences are of psychological rather than neurological origin; or (4) some combination of the above three possibilities may pertain. Further research is needed to determine the relative importance of these possibilities; more precise understanding of cognitive functioning will help us to understand these relationships. Research in this area has been hampered by the use of inconsistent criteria in diagnosing learning disabilities. In LD children brain damage or trauma is often not observable, a clearly defined medical syndrome has not been established, and almost all definitions have relied totally on behavioral criteria. Furthermore, traditional approaches to EEG research may not
Experimental group
Score
Control group
1.21 1.16 1.12 1.11 1.08 1.02 1.01 .99 .99 .98 .97 .96 .93 .89 .89 .89 .89 .89 .88 .87 .87
be particularly rewarding with LD children. Findings in this area vary (Daveau 1959, Satterfield, Cantwell, Lesser, & Podosin 1972, Capute, Neidermeyer, & Richardson 1968). Previous studies of the relationship between mental abilities and EEG "have been hampered by a rigid adherence to traditional methodological approaches" (Vogel, Broverman, & Klaiber 1968, p. 166), and similar criticisms have been stated by Vogel and Broverman (1964,1966) and Mundy-Castle (1957). Vogel and Broverman (1964) argued that EEG measurements taken during an active intellectual effort would most probably show the greatest relationship to cognitive measurements. Furthermore, Brazier has stated that: ... the development from the concept of the electroencephalogram as primarily an aid in
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311 I TABLE VI. Ratios of average EEG power during the initial instruction period to the average EEG power during the rest period showing the subjects in order from least to most alpha attenuation. Subject number
Rank
E7 E4 E1 E8 C6 C4 E5 E6 E10 C11 E9 C1 C7 C10 E3 C3 C2 C9 E2 C8 C5
1 2 3.5 3.5 5 6 7.5 7.5 7.5 10 11.5 11.5 11.5 14 15.5 15.5 17.5 17.5 19 20 21
assessing the normality of the resting "inactive" brain to a dynamic formulation of it as an indicator of the brain in action, has, with its emphasis on function rather than on morphology, suggested a wider application of the EEG to the study of behavior. (1968, p. 302) Thus, it is relevant and feasible to explore disturbances of attention in LD children in relation to EEG parameters while the children are actively attending to stimuli analogous to those that are difficult in the school learning environment. A search for anomalous responses to stimuli might be expected to yield better results than the search for abnormal characteristics in the resting EEG. Therefore, the purpose of this study was to begin exploration of an objective physiological concomitant of attention in LD and control children. It should, however, be noted that EEG analysis by computer power spectral analysis is
Score
Experimental group
|
Control group
1.14 1.05 1.02 1.02 1.00 .97 .96 .96 .96 .94 .93 .93 .93 .90 .89 .89 .88 .88 .87 .86 .78
prohibitively expensive and thus impractical for routine clinical use. I look forward, though, to one day in the near future when microprocessors will be built into electroencephalographs and give immediate, inexpensive readouts. ABOUT THE
AUTHOR
Peter W. Fuller, research assistant professor at the Child Development and Mental Retardation Center, University of Washington, received his doctorate in clinical psychology from the Wright Institute, Berkeley, California. He is currently a postdoctoral intern at the Parent/Child Learning Clinic, Department of Psychiatry and Behavioral Sciences, University of Washington. Dr. Fuller has also been a research fellow in the Division of Neuropathology, University of Washington School of Medicine. ACKNOWLEDGMENT Special thanks are extended to Dr. Charles R. Strother, Professor Emeritus, Psychology and Psychiatry, University of Washington, for his advisory role in the design of this study, which was submitted to the Wright Institute in Berkeley in
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312 partial fulfillment of the requirements for a doctoral degree, and for his repeated critical reviews during the development of the present manuscript.
REFERENCES Adrian, E.D., Mathews, B.H.C.: The Berger rhythm: Potential changes from the occipital lobe in man. Brain, 1934, 57, 355-385. Anderson, R.P., Halcomb, C.G., Doyle, R.B.: The measurement of attentional deficits. Exceptional Child, 1973, 39, 534-539. Berger, //.. Ueber des Elektrenkephelogramm des Menchen. Archiv fur Psychiatrie und Nervenkrankheiten, 1929, 87, 527-570. Berger, H.. Ueber des Elektrenkephelogramm des Menchen. Archiv fur Psychiatrie und Nervenkrankheiten, 1931, 94, 16-60. Beyer, W. (Ed.): Handbook of Tables for Probability and Statistics. 2nd ed. New York: The Chemical Rubber Co., 1968, Table III, Sec. 11. Brazier, M.A.B.: The Electrical Activity of the Nervous System. 3rd ed. Baltimore: Williams 6- Wilkins, 1968. Capute, A.J., Neidermeyer, E.F.L., Richardson, F.: The electroencephalogram in children with minimal cerebral dysfunction. Pediatrics, 1968, 6, 1104-1114. Chatrian, G.E., Bergamini, L., Dondey, M., Klass, D.W., Ijennox-Buchthal, M., Petersen, I.: A glossary of terms most commonly used by clinical electroencephalographers. Electroencephalography and Clinical Neurophysiology, 1974, 37, 538-548. Clements, S.D.: Minimal brain dysfunction in children: Terminology and identification. NINDS Monograph No. 3, U.S. Public Health Service Publication No. 1415. Washington, DC: U.S. Government Printing Office, 1966. Cooley, J.W., Tukey, J.W.: An algorithm for the machine calculation of complex Fourier series. Mathematics of Computation, 1965, 19, 297-301. Daveau, M.: The EEG of 150 children with behavior disorders. Electroencephalography and Clinical Neurophysiology, 1959,10,198. Doyle, J.C., Ornstein, R., Galin, D.: Lateral specialization of cognitive mode: EEG frequency analysis. Psychophysiology, 1974, 2, 567-587. Dykman, R., Walls, R., Suzuki, T., Ackerman, P., Peters, J.E.: Children with learning disabilities: Conditioning differentiation, and the effect of distraction. American Journal of Orthopsychiatry, 1970, 40, 766-781. Dykman, R.A., Ackerman, P.T., Clements, S.D., Peters, J.E.: Specific learning disabilities: An attentional deficit syndrome. In H.R. Myklebust (Ed.): Progress in learning Disabilities, Vol. 2. New York: Grune 6- Stratton, 1971, pp. 56-93.
Galin, D., Ornstein, R.: Lateral specialization of cognitive mode: an EEG study. Psychophysiology, 1972,9,412-418. Glass, A.: Blocking of the occipital alpha rhythm and problemsolving efficiency. Electroencephalography and Clinical Neurophysiology, 1959, 11, 605. Glass, A.: Motivation and the intensity of blocking to problemsolving. Electroencephalography and Clinical Neurophysiology, 1960,12, 262. Glass, A.: Mental arithmetic and blocking of the alpha rhythm. Electroencephalography and Clinical Neurophysiology, 1964,16, 595-603. Hallahan, D.P., Cruickshank, W.M.: Psychoeducational Foundations of Learning Disabilities. Englewood Cliffs, N.J.: Prentice-Hall, 1973. James, W.: The Principles of Psychology. NewYork: Holt, 1980. Kooi, K.A.: Fundamentals of Electroencephalography. New York: Harper and Row, 1971. Luria, A.R.: Experimental study of the higher nervous activity of the abnormal child. Journal of Mental Deficiency Research, 1959, 3,1-22. Luria, A.R.: The Role of Speech in the Regulation of Normal and Abnormal Behavior. New York: Liveright, 1961. Morrison, D.F.: Multivariate Statistical Methods. New York: McGraw-Hill, 1967. Mulholland, T.B.: The concept of attention and the electroencephalographic alpha rhythm. In C.R. Evans and T.B. Mulholland (Eds.): Attention in Neurophysiology. London: Butterworth 6 Co., 1969. Mulholland, T.B.: Occipital alpha revised. Psychological Bulletin, 1972, 78,178-182. Mulholland, T.B., Peper, E.: Occipital alpha and accommodative vergence, pursuit-tracking and fast eye movements. In J. Stoyua (Ed.): Biofeedback and Self Control. New York: Aldine-Atherton, 1971. Mundy-Castle, A.C.: The electroencephalogram and mental activity. Electroencephalography and Clinical Neurophysiology, 1957, 9, 643-655. Satterfield, J.H., Cantwell, DP., Lesser, L.I., Podosin, R.L.: Physiological studies of the hyperkinetic child. American Journal of Psychiatry, 1972, 128, 1418-1424. Strother, C.R.: Minimal cerebral dysfunction: A historical overview. Minimal Brain Dysfunction. Annals of the New York Academy of Sciences, 1973, 205, 6-17. Vogel, W., Broverman, D.M.: Relationship between EEG and test intelligence: A critical review. Psychological Bulletin, 1964, 62,132-144. Vogel, W., Broverman, D.M.: A reply to "relationship between EEG and test intelligence: A commentary." Psychological Bulletin, 1966, 65, 99-109. Vogel, W., Broverman, DM., Klaiber, E.L.: EEG and mental abilities. Electroencephalography and Clinical Neurophysiology, 1968, 24, 166-175. Wender, P.H.: Minimal Brain Dysfunction in Children. New York: John Wiley 6 Sons, 1971.
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