IMPAIRED RECOGNITION MEMORY AFTER HEAD INJURyl H.

J.

Hannay, H. S. Levin and R. G. Grossman

(Department of Psychology, Auburn University, Auburn, Alabama, and the Division of Neurosurgery, University of Texas Medical Branch, Galveston, Texas)

Studies which provide quantitative analyses of memory function after CHI have been recently reviewed (Schacter and Crovitz, 1977). Defective performance by CHI patients on memory tasks presumably implicates reduced efficiency in at least one of the stages of memory, i.e., encoding, storage, and retrieval. However, conventional methods of testing memory do not permit exclusion of a shift in decision strategy or response criterion (e.g., greater caution in designating a stimulus as having been perceived before) as the basis for the change in performance. With the introduction of the theory of signal detection (Green and Swets, 1966), it was possible to obtain a measure of sensitivity or memory efficiency (d') theoretically independent of the subject's criterion for responding. Performance on continuous memory tasks is amenable to such a twochoice signal detection analysis. A series of stimuli is presented successively which essentially consists of two types of stimuli. Either a stimulus is appearing for the first time in the series and is designated as "new" or a stimulus is reappearing and is referred to as "old." Two responses to each stimulus are possible; the subject can call each stimulus old or new. A response would be correct if an old stimulus is called old or if a new stimulus is called new, hits and correct rejections respectively. Two types of errors can occur, a false alarm, calling a new stimulus old, or a miss, calling an old stimulus new. From proportions of hits and false alarms various signal detection measures can be determined. Of course more traditional measures of performance, such as the number of correct responses, can be examined also. Brooks (1972) employed a continuous memory task and found that corrected scores, scores obtained by subtracting false alarms from the number I This investigation was supported by DREW 5P50 NS 07377-08 Center for the Study of Nervous System Injury.

Cortex (1979) 15, 269-283.

270

H. ]. Hannay, H. S. Levil1 and R. G. Grossman

of correct responses, were significantly lower for CHI patients than for controls matched for age and education and bore a significant negative relation to severity of injury as indicated by duration of posttraumatic amnesia (PTA). Patients were tested at different times after injury but this variable was not related to performance. PTA duration was significantly related to performance of CHI patients 30 years or older but not to the performance of younger patients. This was interpreted as indicating a possible loss of plasticity of brain function with age. Employing the same task, Brooks (1974a) found that the rate of false alarms for CHI and controls did not vary significantly though the rate of misses was significantly higher for CHI patients. The rate of false alarms but not of misses was positively related to PTA duration. Since the rate of misses differed between CHI patients and controls, the lack of a correlation with PTA suggested that a higher rate of misses might be a general effect of cerebral trauma. Brooks (197 4b) reanalyzed these data in terms of signal detection theory finding a significantly lower d' in CHI patients which led him to infer a reduction in memory efficiency. The author also reported a significantly higher response criterion (~) value which was interpreted as evidence for CHI patients being more cautious about identifying a stimulus as having been presented previously. Memory capacity, as indexed by d', was inversely related to dura.tion of PTA, whereas no reliable correlation was obtained between ~ and duration of PTA. This dissociation suggested that memory efficiency decreases with greater severity of diffuse brain injury while a shift in response criterion may be a general, nonspecific effect. In contrast, the presence of focal neurological signs was not significantly related to either d', ~ or corrected scores, though only a small number of patients had focal neurological dificits. While Brooks (197 4b) has contributed to the study of recognition memory in CHI patients by making a distinction between deficits arising from changes in sensitivity as opposed to response criterion, his use of ~ as a measure of response criterion is indeed questionable. Basically, the theory of signal detection assumes that a subject is continuously receiving sensory input. On some trials this sensory input is generated by noise, in the present context, by a new item. On the other trials the sensory input is generated by signal plus noise, by an old item. The distributions of sensory input arising from both noise and from signal plus noise are assumed to be normal and often to have a variance of 1. The mean of the noise distribution is zero and the mean of the signal plus noise distribution is designated as d'. Sensitivity to a particular signal is determined by the degree to which the mean of the signal plus noise distribution deviates from the mean of the noise distribution and thus is d' for a subject. To the extent that the

Recognition memory after bead injury

271

distributions of sensory input produced by noise and signal plus noise overlap the stimulus situation is ambiguous for the subject; that is, the subject will not be certain whether the sensory input derived from the presente of noise or a signal. In this situation it is assumed that the subject sets a response criterion, c, a level of sensory input above which he always says a signal was present and below which he says the signal was absent. With respect to the noise distribution, the subject responds to sensory input above c as if it were a signal and makes false alarms. Since noise is assumed to be a normal variable with a variance of 1, it is possible to obtain a measure of c based on the probability of false alarms. Thus c equals - Z [P(S/n)] where P(S/n) is the probability of false alarms. With respect to the signal plus noise distribution, the subject responds that sensory input greater than c indicates a signal and makes hits. The distribution of signal plus noise is also a normal variable with variance of 1. The measure of sensitivity d' can be determined from the probability of hits and false alarms. Thus d' = Z[P(S/s)] + c or d' = Z[P(S/s)] - Z [P (Sin)] where P (Sis) is the probability of hits. Since the measure c is based soley on the probability of false alarms, it has a particularly desirable quality. If two subjects place their response criterion at the same level of sensory input even though the signal is more distinguishable from noise for one subject than for the other then c should be the same for both subjects but d' will be larger for the former subject. This is not so if ~ is used as a measure of response criterion. ~ is defined as the ratio of the ordinate of the signal plus noise distribution to the ordinate of the noise distribution at c; that is, ~ = fsn(c)/fn(c). ~ is thus dependent on the rate of hits as well as the rate of false alarms. If two subjects choose the same level of sensory input as their response criterion, ~ will not be the same for the subjects if they differ in sensitivity. The subject with the larger d' will have the smaller ~. ~ is more appropriately interpreted as a measure of whether the subject is behaving optimally; that is, setting his response criterion so as to maximize the number of correct responses. A subject would be behaving in this way if his response criterion were set at ~ = P(N)/P(S), the likelihood ratio, where P(N) and P(S) are the a priori probabilities of noise and signal plus noise trials respectively. To the extent that the obtained ~ differs from this value the subject is not behaving optimally. Although this interpretation of ~ might provide useful information in the present context, its use is still not warranted because it presupposes (Richardson, 1978) that the subject remembers the values of sensory input produced by almost all of the stimulus events, and furthermore has received feedback concerning the correctness of responses so that he can select the optimal response criterion. The continuous recognition memory task involves relatively few

272

H.

J.

Hannay, H. S. Levin and R. G. Grossman

trials and no feedback so it is unlikely that these assumptions will be met. Of course, criticism can be made of the use of the other signal detection theory parameters, d' and c, since other underlying assumptions may be violated. The alternative is to develop measures of sensitivity and response criterion which are independent of particular theories though this has proved difficult to do (Richardson, 1972). One alternative is simply to examine the hit and false alarm rates of the subjects (Richardson, 1978). If one subject obtains a much higher hit rate than another while maintaining the stlme false alarm rate, one may conclude that the first subject has a higher sensitivity. Similarly if subjects differ in false alarm rates they may be assumed to have different criteria for responding. A re-examination (Richardson, 1978) of the data reported by Brooks (1974a, 1974b) using appropriate signal detection measures of sensitivity (d') and response criterion (c) leads to a sligthly different interpretation of the deficits displayed by CHI patients. Their sensitivity is markedly lower but they do not differ from controls in terms of response criterion. The same statement can be made about an analysis of their hit and false alarm rates. The present study was undertaken to evaluate further the performance on continuous recognition memory of CHI patients using parametric and non-parametric measures of sensitivity and response criterion as well as a more traditional measure of performance in relation to neurologic indices and demographic characteristics of the patients. Our task differed from that employed by Brooks (1972; 1974a, 1974b) in that it consisted of line drawings of living things and was briefer. We attempted to develop a task which would be relatively insensitive to extended formal education and age, at least within the range represented by this study.

11ATERIALS AND 11ETHOD

Subjects

Forty-seven CHI patients, including eight women, participated in the study. The term CHI indicates that the mechanism of injury at the time of impact was one of blunt trauma, rather than a penetrating injury. Only patients less than 50 years were included to avoid confounding the effects of CHI with normal degenerative cerebral changes. None of the patients had a history of alcoholism, or other neuropsychiatric disorders. Handedness was disregarded since the injuries were diffuse. Following our previous procedure (Levin, Grossman, and Kelly, 1976) the CHI patients were classified with respect to severity of acute injury as having Grade I, Grade II, or Grade III injuries on the basis of duration of coma and the presence of neurological impairment. Coma was defined as the failure of the patient to exhibit verbal responses or to carryon purposeful motor activity after verbal or somatic stimulation by

Recognition memory after head in;ury

273

the examiner. Stupor was defined as an uncommunicative state of the patient from which he could be aroused to vocalization or purposeful motor activity. Transient loss of consciousness immediately after impact was not considered in assigning a grade because it was not always possible to have independent verification of brief loss of consciousness in accident victims. Grade I patients were conscious on admission and throughout the period of hospitalization, neurological deficits being absent. Grade I patients essentially formed a control group for severe acute injury as they presumably had premorbid characteristics similar to the Grade II and Grade III patients. Grade II patients were comatose for no more than 24 hours (median duration = .9 days, range = 0-1), though they may have been stuporous for a longer period and may have exhibited an acute neurological deficit (Table I). Grade III patients were comatose for more than 24 hours (median duration = 14 days, range = 1.3-23) and may have exhibited neurological deficits. The Glasgow Coma Scale (Teasdale and .Tennet, 1974) was completed retrospectively to quantify the severity of neurologic impairment at the time of admission. The total Coma Scale score, which can range between 0 (no verbal or motor response and no eye opening) and 15 (normal responsiveness), was computed on the basis of medical chart notes. The median (and range) for the total Coma score in Grade II patients was 8 (4-15); Grade III patients had a median Coma score of 5 (4-9). Electroencephalograms, computed tomography (CT) scans and skull films were obtained for many patients. The classification of patients with regard to the outcome of these procedures appears in Table 1. Nineteen patients, including six women, with diverse somatic complaints but without evidence or history of cerebral disease or injury served as a control group.

Stimuli The task consisted of 6 blocks of 20 stimuli, black line drawings presented individually on 5 X 8 inch white index cards. The stimuli in the first block were all different and thus "new" drawings. Eight of these drawings reappeared once each in all of the following five blocks and thus were "old" drawings every time they reappeared. One of these eight drawings was taken from each of the categories: flowers, birds, snails, moths, mushrooms, insects, fish, and rodents. The other twelve stimuli in these blocks were entirely "new," never reappearing in the task. However, eight of the "new" drawings in each of the last five blocks belonged to the eight categories of "old" drawings, one from each category. These "new" stimuli were perceptually very similar in many cases to the corresponding "old" drawing since theoretically the "new" stimuli are noise and sometimes should be indistinguishable for the patient from the "old" stimuli which are signals. The other four "new" stimuli in each block belonged to other categories. An example of an "old" stimulus or signal and the five "new" stimuli quite similar to that "old" stimulus is given in Figure 1. No "old" stimuli were presented in the first block, so the data analysis was completed on the last five blocks which together contained 40 "old" and 60 "new" stimuli. Procedure

The drawings were presented successively by the examiner so that they were easily seen. The patient was told to look at each drawing carefully and to tell

H.

274

J.

Hannay, H. S. Levin and R. G. Grossman TABLE I

Neurologic Indices of Severity of Initial I n;ury

(N EEG Focal slow Diffuse slow WNL Not performed

I

= 19) 6 1 4 8

Grade of injury II (N = 13)


30 days

3 2 1

6* 1*

1 8

2 6

1 10 5

3 4

19

10

8 7

19

5 8

8 7

HemIparesis

Present Absent

3

Aphasia

Present Absent Operated hematoma

Subdural Epidural Intracerebral No hematoma

1 1 2 17

10

15

2

1 4

2 2

2

3

6

8

13

3 12

Skull fracture

Linear Basilar Depressed Linear-basilar Depressed-basilar None

3 1 2 11

Oculovestibular deficit Present Absent

19

" Cortical atrophy also present.

Recognition memory after bead injury

275

a.

Fig. 1 -

An old stimulus (a) and its corresponding five new stimuli.

whether each drawing was an old drawing, exactly like one which he has seen before in the series, or a new drawing, one that he was seeing for the first time. The patient was told that each drawing would be presented for only 3 seconds so that he must tell the examiner if the drawing is old or new right away. The test required 15 minutes to administer. Testing of CHI patients was deferred until orientation for time (Benton, Van Allen and Fogel, 1962) and surroundings recovered to a normal level or reached a plateau without signs of further improvement. This precaution was observed in order to study memory function in patients after they emerged from PTA (Schacter and Crovitz, 1977).

RESULTS

Non-parametric statistics were used throughout because of heterogeneity of variance in the test scores for the various patient groups. Since many comparisons were made in the data analysis a level of .01 was used to test significance. Median scores and ranges for age, education, interval from injury to test, and the dependent measures are given in Table II. Pairwise comparison of the four patient groups on all of the variables was made using the Mann-Whitney U test. The z-values for these comparisons and their significance are given in Table III. CHI patients differing in grade of injury did not vary reliably in either age or education. Grade I patients were significantly younger than controls while Grade III patients were significantly less educated than controls. However, age and education were not related to any of the dependent measures considering all patients together, for CHI patients considered alone, for CHI patients under 30 years of age, or for CHI patients 30 and older (Table IV).

19

47

19

13

15

Controls

CHI

Grade I

Grade II

Grade III

N

TABLE II

11

16 to 43

R

3 to 13

11

21

M

11 6 to 14

21

R

14 to 49

8 to 14

14 to 50

M

R

11

20

R

M

3 to 14

21

14 to 50

M

11 to 945

434

10 to 499

48

3 to 525

50 to 96

80

61 to 92

83

78 to 100

93

15

14 7 to 40 2 to 38

37

o to

3

o to

2

o to

o to 14

1

6 22

1

o to 38

8

o to

o to

o to 16

1

33

18

15

33

4

Misses

6

False alarms

22 to 40 6 to 38

38

25 to 40

39

39 7 to 40

86 50 to 100

40

3 to 975

48

to

36

84 to 99

9 to 17

19 to 57

R

39

92

12

30

M

Hits

Education (years)

Age (years)

Correct responses

Injury-test interval (days)

3.00

1.11

-0.34 to 1.84

0.73 2.30 0.46 to 3.73

-0.34 to 1.28

0.73

0.34 to 3.00

1.28

- 0.34 to 3.00

0.53 to 4.11

2.12

2.31 to 6.00

3.35

0.46 to 6.00

0.62 to 3.00

1.28 2.94 2.37 to 4.96

c

d'

Median Scores (M) and Range (R) for Age, Education, Iniury-Test Interval and the Dependent Measures

N

""

~ ;:,

....CJ ...,...,0

CJ

~

"";:,\:l...

":::l.;:,

t-

Impaired recognition memory after head injury.

IMPAIRED RECOGNITION MEMORY AFTER HEAD INJURyl H. J. Hannay, H. S. Levin and R. G. Grossman (Department of Psychology, Auburn University, Auburn, A...
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