Visual information processing and alpha blocking in schizophrenics and normals

J. jnychial. Res. Vol. 16, No. 2, pp. 95-102, Printed in Great Britain.

1981

0022-3956/81/020095~38302.00/0 0 1981 Pergamon Press Ltd.

VISUAL INFORMATION PROCESSING AND ALPHA BLOCKING IN SCHIZOPHRENICS AND NORMALS JOHN R. DAVIS, ALAN G. GLAROS and GLENN S. DAVIDSON* Wayne State University (Received 18 January 1980; revised 20 October 1980)

A COMMON strategy used to investigate attention has involved the monitoring of electroencephalographic records. In particular, the blocking of the occipital alpha rhythm has often been taken as an indication of a state of visual attention.lP2 The examination of alpha blocking differences in schizophrenics and normals has typically involved the presentation of photic stimulation. Such research has frequently found less blocking of the alpha rhythm (i.e. a greater number of waves during a stimulus period) in schizophrenics than in normals.3-7 In none of these studies, however, was the amount of visual information presented to the subjects varied, a factor that may have significantly influenced attentional processes.as 9 NEALE, for example, has demonstrated that the attentional deficit seen in schizophrenics, as compared to normals, varies as a function of the amount of visual information presented to the subjects.9 More recently, DAVIDSON and NEALE varied the similarity of noise letters presented tachistoscopically with a target letter. These researchers found that schizophrenics were influenced by target-noise similarity in the same manner as normals, although schizophrenics performed less well than normals for all display types. DAVIDSON and NEALE suggested that the schizophrenic deficit was due to slowness of information processing. lo The formulations of MLJLHOLLAND* and NEISSER” suggest a bridge between the EEG/ alpha blocking latency and information processing methods used to investigate attentional deficits in schizophrenia. A series of studies reported by MULHOLLAND and PEPER” in which the relationship of alpha activity and oculomotor efferents was examined under feedback and non-feedback conditions indicated that alpha blocking is not due to visual attention per se, but, rather, to the visual processes of fixation, lens accommodation, and pursuit tracking. MLJLHOLLAND suggests that alpha blocking occurs when a person adjusts his eyes in such a way as to optimize vision and that alpha is present when vision-optimizing ocular adjustments are absent.* NEISSER has further suggested that these optimizing eye movements may be associated with the initial stage of information processing-pre-attentive processing. Specifically, NEISSER~~hypothesized that pre-attentive processing is guiding by information extracted Address reprint requests to: Alan G. Glares, Ph.D., Department of Psychology, Wayne State University, Detroit, Michigan 48202, U.S.A. *Glenn S. Davidson is now at Ball State University. 95

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GLENN S. DAVIDSON

from the stimuli presented to the subject and that this processing also controls shifts of attention involving eye movements. Thus, shifts of attention associated with pre-attentive processing of visual information can be estimated by measuring alpha-blocking latency when a stimulus is presented during the occurrence of alpha activity. The findings 3-7that schizophrenics block alpha more slowly than normals are, therefore, consistent with the findings presented by DAVIDSON and NEALE”that schizophrenics process information more slowly. This paper reports the findings of a preliminary study of the relationship between alpha blocking latency and information processing in schizophrenics and normals. The task used is a forced-choice letter recognition task similar to that employed by NEALE.~ To control for the possible effect of changes in illumination on alpha blocking latency, a blank stimulus field was also employed. Thus, subjects were instructed to respond “blank”, “T”, of “F” to the stimulus presentation. This study also incorporates a significant methodological innovation. Prior research has typically relied on subjective determination of the presence of alpha, variable latency of stimulus presentation within alpha bursts, and subjective determinations of alpha blocking. In contrast, the present study employed solid-state technology in the determination of the presence and absence of alpha and in the presentation of stimuli within alpha bursts. The device used to define alpha allowed for wave-by-wave examination of the EEGi3 and for stimulus presentation contingent upon a criterion period of alpha activity. It was hypothesized that schizophrenics would show an information processing deficit relative to normals,’ particularly for high amounts of information (i.e. the four- and eight-letter stimuli), that schizophrenics would show longer alpha blocking latencies than normals for all stimulus conditions, that both schizophrenics and normals would show decreasing alpha blocking latencies with increasing display sizes, and that schizophrenics would show significantly longer alpha blocking latencies than normals with increasing amounts of visual information. It was also predicted that verbal reaction times would be longer for schizophrenics than for normals. METHOD Subjects

Two groups of 12 male subjects each were selected. One group was comprised of college students whose mean age was 22.67 yr (S.D. = 2.93). The other group was comprised of hospitalized schizophrenics with a mean age of 27.83 yr (S.D. = 3.88). Nine of the patients were diagnosed chronic undifferentiated schizophrenic, and three were diagnosed paranoid schizophrenic. The diagnoses were made by staff psychiatrists and no disagreement in diagnosis was recorded. None of the patients had any history of brain damage, epilepsy, mental retardation, or alcoholism. Nine of the patients were single, one divorced, and two separated. The average number of previous hospitalizations was four, with average length of time since first hospitalization 6.29 yr. All but one of the schizophrenic subjects were on a regimen of neuroleptic medication; the average dose was equivalent to 455 mg of Thorazine. All subjects had normal or corrected to normal vision (20122 Snellen equivalent) as measured by a Keystone Visual Survey Telebinocular.

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Apparatus

Four visual stimulus conditions were presented to each subject by means of a threechannel N-1000 Scientific Prototype tachistoscope. A white fixation field with a centered red dot was continuously present except during a stimulus exposure. The luminance of the fixation field as measured by a spot photometer was 38.37 cd/m2 (11.2 footlamberts). Visual stimuli were presented for a duration of 120 msec and had a luminance of 24.26 cd/m* (7.08 footlamberts). One visual stimulus condition was the presentation of a blank card (zero-letter condition). The other three types of visual stimuli were constructed as described in NEALE~ and consisted of a letter T or F surrounded by zero, three, or seven random consonants (the one-, four-, and eight-letter conditions, respectively). For each stimulus condition, sixteen stimulus cards were constructed, half with the target letter T, and half with a target letter F. The stimulus letters were randomly assigned to the sixteen cells of an imaginary 4 letter by 4 letter matrix. The letter matrix was centered on the stimulus card and subtended 2.938” of visual angle horizontally and 3.438” of visual angle vertically. Letters were typed with an IBM Orator typing element. Horizontal and vertical spacing between letters subtended 45.272 min of visual angle. The letters themselves subtended 7.545 min of visual angle horizontally and 15.091 min of visual angle vertically. Sixteen randomly selected cards, four from the blank and two from each other condition, were used for practice trials. The remaining 48 cards were randomized, and presented during the experimental trials. Card order was identical for all subjects. Silver-chloride electrodes were placed at locations 0, and 0214,and a ground was placed on the ear lobe. EEG information was differentially amplified (Coulborn Hi Gain Bioamplifier/Coupler; Gain = 50 K; filters set at 1 and 40 Hz, rolloff = 12 dB/octave) and converted from analog to digital form with a Schmitt trigger. A digital frequency discriminator’3 determined when the criteria for alpha were met. Alpha was defined as 8-13 Hz activity exceeding 4.8 pV. Operation of the tachistoscope for stimulus presentation was contingent upon the presence of a given duration of alpha activity (criterion time in alpha) which was constant at 87 msec for all subjects during the practice trials. During experimental trials, the criterion time in alpha was set to a value determined during the baseline recording period (see below). The time from the onset of the stimulus to the disappearance (i.e. failure to meet criteria) of alpha (alpha blocking latency) was collected on a Med Associates DIG 800 counter. Verbal reaction time was defined as the period of time between presentation of the stimulus and the subject’s verbal identification of the stimulus.* Procedure

Subjects were introduced to the assistant and the procedure was described. After consent was obtained, their vision was assessed with the telebinocular. The subjects were then seated in front of the tachistoscope and electrodes were applied. Instructions requested that subjects continue to look into the tachistoscope at all times. The types of stimuli to *A description

author.

of the method

and operation

of equipment

in State Set Notation

is available

from the

second

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be presented were described and subjects were asked simply to report whether a card was “blank”, “T”, or “F”. Following the instructions, the experimenter dimmed the lights in the subject room and went to the equipment room. Sixteen practice trials were then presented. During the practice trials, a criterion timer was set so that stimulus presentation was contingent upon 87 msec of alpha activity. After each stimulus presentation, response latency and time to block alpha were recorded. An assistant changed the stimulus cards and recorded the subject’s verbal responses. Following the practice trials, the subject was told to sit quietly for the next few minutes while the equipment was adjusted. The subject was instructed to keep his eyes open and to keep looking at the fixation field. During this period, which typically lasted about 5 min, baseline measures were taken on two variables, and no stimuli were presented. Forty occurrences of continuous alpha wave activity were sampled and their durations measured. From the 40 samples of alpha activity, the subject’s median duration of alpha activity (median alpha time) was calculated. In addition, alpha density was measured by taking 1-min samples, every other minute, of the number of seconds in each minute sampled in which alpha occurred. At the end of the baseline recording, the criterion timer was set to the value of the median alpha time (MAT). The subject was then informed that the experimental trials would begin. The experiment then continued in the same manner as during the practice trials. RESULTS

A summary of the data is presented in Table 1. Data were analyzed by a Groups by Display mixed design multivariate analysis of covariance with repeated measures on the second factor.‘5**6 The dependent variables in the analysis were alpha blocking latency (ABL), verbal reaction time (RT) and percent correct identifications of the stimulus (PC). Covariates were median alpha time (MAT), alpha density (AD), and AGE. A test for skewness” performed on ABL and RT indicated that the distributions for these variables were positively skewed. Logarithmic transformations were therefore used to normalize the distributions.‘* TABLE 1. RESPONSES OF NORMALSAND SCHIZOPHRENICSBY IXSPLAY TYPE AND DEPENDENT VARIABLE Display type (number I

0

of letters) 4

8

M

S.D.

M

S.D.

M

S.D.

M

S.D.

99 85

1.7 30.6

96 76

6.2 17.2

85 64

1.4 18.8

75 62

12.2 17.9

RT (set) Normal Schizophrenic

1.30 2.33

0.30 1.55

1.25 1.80

0.36 0.92

1.46 2.02

0.36 0.88

1.84 2.49

0.45 1.27

ABL (msec) Normal Schizophrenic

84 83

57.1 71.2

101 82

61.1 60.4

104 89

68.4 56.0

92 65

54.4 42.9

Dependent variable Percentage correct Normal Schizophrenic

Note: For both normal

and schizophrenic

groups,

N = 12.

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The univariate test for PC indicated significant Display effects, F (3, 63) = 16.064, 0.001, and Groups effects, F (1, 19) = 16.411, p < 0.001. The Groups x Display interaction, however, was not significant, F (3, 63) = 0.597, p < 0.62. The schizophrenic group performed consistently less well at correctly identifying the stimulus than did the normal group. For both groups, the percentage of correct identifications decreased as the number of letters in the stimulus display increased. The univariate test for RT showed a significant effect for Display, F (3, 63) = 9.131, p < 0.001. The Groups and the Groups x Display effects were not significant, F (1, 19) = 1.959, p < 0.178, and F (3, 63) = 0.362, p < 0.780, respectively. Except for the blank condition, reaction times for both groups increased with increasing numbers of nontarget letters in the display. The univariate test for ABL indicated a significant Groups effect, F (1, 19) = 4.235, p < 0.05. The Display and Groups x Display effects were not significant, F (3, 63) = 1.191, p < 0.32, and F (3, 63) = 0.437, p < 0.72, respectively. The schizophrenic group blocked alpha more quickly than the normal group for all display conditions. The mean MAT was 168 msec for normals and 139 msec for schizophrenics, a nonsignificant difference, t (22) = 1.46, p < 0.16. The mean AD was 19.2 set for normals and 12.4 set for schizophrenics, also not significant, t (22) = 1.55, p < 0.14.

p <

DISCUSSION

It is clear from the results (Table 1) that increasing the number of letters in the display effectively increased the difficulty of the task. It may be concluded, then, that the attempt to manipulate the amount of information to be processed from the stimuli was successful. As predicted, increasing the amount of information resulted in performance decrements as measured by the percentage correct. In addition, the schizophrenic subjects performed as expected by showing consistently poorer performance than normal subjects, and slower reaction times.‘9*20These findings replicate those from other studies of span of apprehension in schizophrenia,” and, taken with the reaction time data in the present study, support the hypothesis that schizophrenics are slower than normal subjects in executing information processing operations.” A number of factors need to be taken into account in explaining what makes a schizophrenic slow in processing information. First, the results demonstrate a schizophrenic performance deficit. This deficit may result from slowness or from a quite different process. That is, schizophrenics may be generally slow or may instead carry out some micro-operations very rapidly or with great variability. The overall behavioral deficit, then, is not easily related to a specific underlying process. The alpha blocking latency is a second factor to be considered. While it was predicted that schizophrenics would block more slowly than normals, they in fact blocked more rapidly. The sole exception occurred in the “blank” stimulus condition, where schizophrenics and normals were essentially identical. It was also in this condition that the schizophrenics reached their highest levels of performance as measured by percent correct responses. Finally, alpha blocking rates for schizophrenics were fairly consistent across the stimulus conditions. This replicates the results of CROMWELL and HELD” who found

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schizophrenics to block alpha more quickly than normals, and is consistent with the hypothesis that schizophrenics are in a state of high arousal or hyperalertness.23V24 Although speculative, the data might be interpreted as follows: While there is general agreement that alpha blocking is associated with information processing and attention (perhaps at NEISSER’S pre-attentive stage)“, the relationship between alpha blocking latency and accurate information processing may not be linear. In other words, rapid alpha blocking may be associated with effective processing up to some point, but beyond this point, rapid blocking may be debilitating. To understand how excessively rapid blocking can be detrimental, the processes presumed to occur on a feature analysis task need to be examined. The stage of pre-attention (or feature extraction) is an active process that is guided by schemata,25 expectation26 and other active control processes. Efficient processing then requires rapid adjustment of the visual system (reflected in alpha blocking latency) along with a coordinated control system. Should these two operations become desynchronized, further processing would break down, or become fragmented. The schizophrenic subjects in the present study were observed to respond very quickly to the visual stimuli, as shown by their rapid blocking of alpha, and thus were prepared to begin the initial information processing operations very soon after stimulus presentation. This rapid response may be effective when the information load is reduced, as in the Blank condition in the present study, and the condition without visual distracters in NEALE’S work.’ However, as the information load increases, the control and extraction processes may desynchronize, resulting in an only partially processed input. If this result is then used for response execution, then the variability and performance deficits which are seen in the everyday behavior of the schizophrenic, as well as in the laboratory setting, might occur. The present study was an attempt to more clearly identify the variables underlying the characteristic information processing deficit in schizophrenic performance. The results add support to the hypothesis of a quantitative, rather than qualitative, difference between schizophrenics and normals. In addition, they suggest ways in which the present methodology might be further utilized in other research. For example, the effects of other stimulus manipulations on alpha blocking can be more closely examined. Measures of the time to recover alpha could also be employed to study the relationships between physiological variables and cognitive functions in schizophrenia. Finally, the method can be further refined to examine bilateral processing and alpha blocking to determine hemispheric differences, and possible interhemispheric transfer difficulties.27-29 Further understanding of schizophrenic processing problems depends on continuing refinement of our measurement techniques, as well as on a more detailed analysis of the inter-relationships among measures. SUMMARY

A multivariate study was conducted which brought together two separate paradigms which have been used to investigate attentional deficits in schizophrenia, namely, physiologically oriented studies of brain activity and information processing studies. Alpha blocking latency was used as a physiological index of early stages of visual information

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processing. The application of an innovative and highly reliable methodology for measuring alpha activity was described. Results from the experiment extended the findings that have been made in both the physiological and information processing fields, and’ suggest that investigation of the relationships between EEG variables and cognitive processes in schizophrenia merits continued inquiry. The results indicated that attentional deficits in schizophrenia do not arise because of slowness during the initial stages of processing. Directions for further research were described. Acknowledgements-This article is based on a master’s thesis done by the first author. We thank RUE L. CROMWELL,ROBERTFREEDMAN,GERALDRGSENBAUM and R. DOUGLASWHITMANfor their helpful comments. We also thank SCOTTGROVES,PAT HULSE,ED HUTCHINSON, YVONNEKRISELand LEONSTRICKLAND for their assistance as experimenters. We gratefully acknowledge the cooperation of ABDEL-SATTAR IBRAHIM,JOHN Mom and the staff of Northville State Hospital. REFERENCES 1. ADRIAN,E. D. and MATTHEWS,B. H. C. The Berger rhythm: potential changes from the occipital lobes in man. Brain 51,356, 1934. 2. LINDSLEY,D. B. Attention, consciousness, sleep and wakefulness. In: Handbook ofPhysiotogy (Section I). FIELD, J., MA~~uN, H. W. and HALL, V. E. (Editors), American Physiological Society, Washington, D.C., 1960. 3. BLUM,R. H. Photic stimulation, imagery and alpha rhythm. J. ment. Sci. 48,160,1956. 4. BLUM,R. H. Alpha rhythm responsiveness in normal, schizophrenic and brain-damaged persons. Science 126,749, 1957. 5. LIBERSGN,W. T. Functional electroencephalography in mental disorders. Dis. nerv. Syst. 5, 134, 1944. 6. SALM~ON,I. and POST,J. Alpha blocking and schizophrenia. Archsgen. Psychiat. 13,367, 1965. 7. WILSON,N. J. and Wnso~, W. P. The duration of human electroencephalographic arousal responses elicited by photic stimulation. Eiectroenceph. clin. Neurophysiol. 11,85, 1959. 8. MULHOLLAND, T. B. Objective EEG methods for studying covert shifts of visual attention. In: The Psychophysiology of Thinking. MCGUIGAN,E. J. and SCHOONOVER, R. A. (Editors). Academic Press, New York, 1973. 9. NEAL.E,J. M. Perceptual span in schizophrenia. J. abnorm. Psychol. 77,196, 1971. 10. DAVIDSON,G. S. and NEALE,J. M. The effects of signal-noise similarity on visual information processing of schizophrenics. J. abnorm. Psychol. 83,683, 1974. 11. NEISSER,U. Cognitive Psychology. Appleton-Century-Crofts, New York, 1967. 12. MULHOLLAND, T. B. and PEPER, E. Occipital alpha and accommodative vergence, pursuit tracking and fast eye movements. Psychophysiology 8,556,1971. 13. GLAROS,A. Cl., MARTIN, J. M. and CHIODO, L. A. A digitial frequency discriminator for biofeedback research. Behav. Res. Meth. Instrum. 10,663, 1978. 14. JASPER, H. H. Report of the committee on methods of clinical examination in electroencephalography. Electroenceph. clin. Neurophysiol. 10,371, 1958. 15. MANOVA-Miami Multivariate Analysis of Variance or Covariance. Wayne State University Computer Services Manual, Detroit, 1975. 16. CLYDE,D. J.; CRAMER, E. M. and SHERIN, R. J. Multivariate Statistical Programs. University of Miami Press, Coral Gables, FL, 1966. 17. SNEDECOR,G. W. and COCHRAN,W. G. Statistical Methods (6th edn.), p. 80. Iowa State University Press, Ames, IA, 1967. 18. WINER,B. J. Statistical Principles in ExperimentatDesign(2nd edn.), p. 400. McGraw-Hill, New York, 1971. 19. HUSTON,P. E., SHAKOW, D. and RIGGS, L. A. Studies in motor function in schizophrenia-II. Reaction time. J. gen. Psychol. 16,39, 1937. 20. RODNICK,E. H. and SHAKOW,D. Set in schizophrenia as measured by a composite reaction time index. Am. J. Psychiat. 97,214, 1940. 21. SACCU~~O,D. P. and MILLER,S. Critical interstimulus interval in delusional schizophrenics and normals. J. abnorm. Psychot. 86,261, 1977. 22. CROM\KELL,R. L. and HELD, J. M. Alpha blocking latency and reaction time in schizophrenics and normals. Percept. mot. Skills 29, 195, 1969.

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23. GOLDSTEIN,L. and SUGARMAN,A. A. EEG correlates of psychopathology. In: Neurobiological Aspects of Psychopathology. ZUBIN,J. and SHAGASS, C. (Editors). Grune and Stratton, New York, 1969. 24. VENAELES,P. H. Input dysfunction in schizophrenia. In: Progress in Experimental Personality Research (Vol. 1). MAHER,B. A. (Editor). Academic Press, New York, 1964. 25. NEISSER,U. Cognition andReality. W. H. Freeman, San Francisco, 1976. 26. LINDSAY,P. H. and NORMAN,D. A. Human Information Processing: An Introduction to Psychology (2nd edn.). Academic Press, New York, 1977. 27. GREEN, P. Defective interhemispheric transfer in schizophrenia. J. abnorm. Psycho/. 87,472, 1978. 28. HINK, R. F. and HILLYARD,S. A. Electrophysiological measures of attentional processes in man as related to the study of schizophrenia. J. psychiat. Res. 14, 155, 1978. 29. VAUGHAN,H. G., JR. Toward a neurophysiology of schizophrenia, J. psychiat. Res. 14,129, 1978.