RECOVERY OF MEMORY AND LEARNING FUNCTIONS FOLL OWIN G TRAUMATIC BRAIN INJURY 1
Muriel D. Lezak (V. A. Hospital and University of Oregon Health Sciences Center, Portland, Oregon)
Both clinical observations and research studies of traumatically braininjured patients suggest that the rate and extent of recovery of any given intellectual function may differ from the recovery course of other functions, even seemingly quite similar ones (Mandleberg and Brook, 1975; Newcombe, Marshall, Carriwick and Hiorns, 1975). The course of recovery generally has been related to the side of the injury (Diller, Ben-Yi shay, Gerstmann, Goodkin, Gordo n and Weinberg, 1974; Warrington, James and Kinsbourne, 1966 ), the severity of the injury (Jennet, Teasdale and KnillJanes, 1975; Russell, 1932), and the age of the patient (Russell, 1932; A. Smith, 1960; Teuber, 1975). Complexity of the activity being examined also may contribute to differing recovery curves. Moreover, time elapsed since injury has been related to the quality of a patient's posttra umatic intellectual performance (Gronwall and Sampson, 1974; Ruesch and Moore, 1943; Russell and Smith, 1961). Little is known, however, of the relative impact of these variables on the course of recovery, or of the relative resiliency of different intellectual functions. As part of a longitudinal study, undertaken to gain a systematic insight into these questions, newly brain-injured patients have been given repeated neuropsychological examinations covering a wide range of intellec tual functions. This paper reports the data on verbal memory and learning tests taken within the first three years post injury.
MATERIALS AND METHOD
Subjects All of the 24 traumatically brain-injured white male patient volunte ers had closed head injuries. Eight of them had predominantly left hemisp here damage 1
This study was supported in part by VA Medical Research Service Grant N. 648-5243.
Cortex (1979) 15, 63-72.
64
M.D. Lezak
(1), eight had predominantly right hemisphere damage (R), and the damage
sustained by eight was bilateral or diffuse (B/D); in each subgroup, two patients had skull fractures. In most instances, site of lesion was identified by a neurologist or neurosurgeon in an accident report, report of examination on initial admission, discharge report of initial admission, or surgical report. When the physician did not specifically implicate a critical site, determination of site was based on medical reports of hemiplegia, EEG foci, etc. All patients had entered this study prior to CT scan availability. At the time of their accidents, the overall age range of this group was from 19 to 41 (mean = 26.4, S.D. = 5.6). Thirteen patients were 24 years old or younger. Procedure
Each subject had been injured less than a year when first examined. Most were examined within four to six weeks after return of consciousness but six of them did not have the initial examination until the latter half of the first year post injury. Twenty-three of the 24 subjects were examined within the second six months of the first year; all 24 were reexamined during the second year post injury and again during the third post trauma year. Verbal memory and learning were measured by Digits Forward (DF) and Digits Backward (DB) following Wechsler's instructions (1955); and by four trials of Rey's Auditory-Verbal Learning Test (AVLT) (Lezak, 1976; Rey, 1964). This latter test presents the subject the task of learning 15 common words in a series of five immediate recall trials. Following the 5-trial learning presentation, a second 15-word list is presented for immediate recall after which the subject is asked to recall as much as he can remember of the first list. Thus trial I tests immediate memory under a stimulus overload condition (i.e., unlike Digit Span, more material is presented for immediate memory than can be grasped in a single trial); trial V measures the amount of material retained after five immediately successive repetitions (i.e., simple learning); trial B, involving the second word list, tests immediate memory under stimulus overload conditions complicated by the possibility of proactive inhibition, and serves as an interference trial; and trial VI tests retention following the interference trial that typically takes three to five minutes from introduction through completion. Data analysis
Each AVLT and Digit Span score was classified as falling either within normal limits (i.e., within or above the average range of scores for that measure) or not within normal limits (i.e., below the average range of scores for that measure. Within normal limits (wnl) for each of the measures was defined as follows: DF = 6; DB= 5; AVLT-I = 6, AVLT-V = 12; AVLT-B = 6; AVLTVI 10 (see Lezak, 1976, for AVLT normative data). Using the dichotomized scores, the following questions were examined by means of a 2 X 2 contingency table (Finney, Latscha, Bennett and Hsu, 1963 ):
=
(1) How do the different functions (e.g., immediate memory, retention, immediate memory under stimulus overload conditions) change over time relative to one another? To answer this question, each possible pairing of the four AVLT measures and DF and DB were compared at each time frame for the proportion of wnl scores (see Table I).
65
Recovery of me1nory and learning functions
(2) Is site of injury related to change over time? To answer this question, comparisons were made of each of the six measures between each pairing of the three localization groups, L, R., and B/D, at each time frame for the proportion of wnl scores (see Table II.) (3) Is severity of injury related to change over time? To answer this question, the subjects were classified into one of two groups, unconscious less than two weeks and unconscious two weeks or more. Comparisons were made between these two groups for each of the six measures at each time frame for the proportion of wnl scores (see Table III).
(4) Is age at time of injury related to change over time? To answer this question, the subjects were classified into one of two groups, under 25 (U) or over 25 (0). Comparisons were made between the two age groups for each of the six measures at each time frame for the proportion of wnl scores.
RESULTS
The following profile of memory and learning functions of this sample of traumatically brain-injured patients emerged: (1) Only DF and AVLT-1, the simplest measures of immediate memory, registered systematic improvement over time (see Table I). Consistent imTABLE I
Percent of Subjects Performing Within Normal Limits on Each of Six Measures of Verbal Memory and Learning at Each Time Frame
Months since injury
Measure
0-6
7-12
13-24
25-36
AVLT I B
39 28
VI
6
6
48 30 22 13
48 48 17 30
58 17 29 25
Digit Span Forward Backward
47 41
65 52
70 56
83 39
v
Differences between measures reaching significance at each time frame: I·V,I·VI I·V,B·V Level of significance :~i I·VI
l
I·V,I·VI I·V,DF·DB
provement on DF produced a significant (p < .05) increase in the number of wnl performances on the fourth (within the third year) examination over the first (within six months) examination. On the AVLT measures, all of which measure aspects of memory or
66
M.D. Lezak
learning more complex than DF, fewer than half the subjects achieved wnl scores with the single exception of the third year trial of the least complex and demanding of these measures (AVLT-I). At best, only 30% of the sample achieved wnl scores on the two learning measures (AVLT-V and VI); and for the most part, the percentage of wnl scores on these two measures remained in the lowest quartile and not statistically distinguishable from one time frame to another. Moreover, when each measure was compared with scores obtained on the other measures at each time interval, a consistent and significant increase in the proportion of wnl performances was registered only by the two simplest measures of immediate memory, AVLT-I and DF. In sharp contrast, few gains were made on the two more complex immediate memory tasks, AVLT-B or DB, or on either measure of learning. In fact, of these latter four measures, all scores but those for AVLT-V, the simplest learning task, followed a similar pattern of gain from the earliest testing through the second year with a loss in the third year which, in the case of AVLT-B, was of significant (p < .05) dimensions. (2) By and large, site of injury made little difference in the proportion of wnl performances. On AVLT-I, R patients performed better than L patients at each time interval, but the difference between them reached statistical significance only in the fourth examination (see Table II). On every measure, L patients performed least well immediately post trauma and while their course differed from measure to measure, they tended to show least improvement. Only on DB did both L and B/D patient groups outstrip those whose injuries were predominantly right-sided, and then only after the first year post trauma. (3) On every measure, the more severely injured subjects (unconscious two or more weeks) performed more poorly at initial testing than those less severely injured (see Table III). On two of the measures, AVLT-I and AVLT-B, this difference reached significance. Further, on all of the measures at every testing the less severely injured subjects maintained their performance superiority. However, although the severely injured subjects displayed a considerable improvement trend from the first to the fourth examination on DF, no statistically significant gains were made by either severity group. (4) On none of the six measures at any of the four time frames did a significant difference occur on the basis of age.
DISCUSSION
The extent to which traumatically brain-injured men recover verbal memory and learning appears to vary with the nature of the function, task,
TABLE II
~easure
~easure
~easure
40 43 60
0 43 40
17 43 60 AVLT-B
AVLT-I 37 57 50
13-24
37 57 50 Digits Forward 62 75 57 62 75 71
25 43 25
25 71 50
7-12
* Difference between subgroups at .05 level of significance ** Difference between subgroups at .01 level of significance
Left Right Bi/Dif
Left Right Bi/Dif
Subgroup Left Right Bi/Dif
0-6
87 75 86
12 12 25
L·R* 1'
37 87 50
25-36
~onths
40 43 40
0 0 20
0 0 20
0-6
sipce injury
12 29 12
R·BjD*
AVLT-VI
AVLT-V
13-24
25 12 0 57 12 12 Digit Backwards 38 50 71 38 50 86
12 43 12
7-12
38 25 57
25 25 25
25 37 25
25-36
Percent of Each Localization Group Performing Within Normal Limits on Each of Six Measures of Verbal Memory and Learning at Each Time Frame
~
...,~
~ ~
":::-.a
0
~·
~
-
"'"'....
~
"';:,...
-
~
~
"'~ a
-
?;l
"'"a '"'...." ""'a
2 weeks 2 weeks
~
~ ~
Measure
Measure
Measure
64 17
45* 0
64* 0
0-6
AVLT-B
AVLT-I 67 27
13-24
67 27 9 Digits Forward 77 75 60 54
50*
75* 18
7-12
* Difference between subgroup pairs at .05 level of significance ** Difference between subgroup pairs at .01 level of significance
weeks 2 weeks
Muriel D. Lezak (V. A. Hospital and University of Oregon Health Sciences Center, Portland, Oregon)
Both clinical observations and research studies of traumatically braininjured patients suggest that the rate and extent of recovery of any given intellectual function may differ from the recovery course of other functions, even seemingly quite similar ones (Mandleberg and Brook, 1975; Newcombe, Marshall, Carriwick and Hiorns, 1975). The course of recovery generally has been related to the side of the injury (Diller, Ben-Yi shay, Gerstmann, Goodkin, Gordo n and Weinberg, 1974; Warrington, James and Kinsbourne, 1966 ), the severity of the injury (Jennet, Teasdale and KnillJanes, 1975; Russell, 1932), and the age of the patient (Russell, 1932; A. Smith, 1960; Teuber, 1975). Complexity of the activity being examined also may contribute to differing recovery curves. Moreover, time elapsed since injury has been related to the quality of a patient's posttra umatic intellectual performance (Gronwall and Sampson, 1974; Ruesch and Moore, 1943; Russell and Smith, 1961). Little is known, however, of the relative impact of these variables on the course of recovery, or of the relative resiliency of different intellectual functions. As part of a longitudinal study, undertaken to gain a systematic insight into these questions, newly brain-injured patients have been given repeated neuropsychological examinations covering a wide range of intellec tual functions. This paper reports the data on verbal memory and learning tests taken within the first three years post injury.
MATERIALS AND METHOD
Subjects All of the 24 traumatically brain-injured white male patient volunte ers had closed head injuries. Eight of them had predominantly left hemisp here damage 1
This study was supported in part by VA Medical Research Service Grant N. 648-5243.
Cortex (1979) 15, 63-72.
64
M.D. Lezak
(1), eight had predominantly right hemisphere damage (R), and the damage
sustained by eight was bilateral or diffuse (B/D); in each subgroup, two patients had skull fractures. In most instances, site of lesion was identified by a neurologist or neurosurgeon in an accident report, report of examination on initial admission, discharge report of initial admission, or surgical report. When the physician did not specifically implicate a critical site, determination of site was based on medical reports of hemiplegia, EEG foci, etc. All patients had entered this study prior to CT scan availability. At the time of their accidents, the overall age range of this group was from 19 to 41 (mean = 26.4, S.D. = 5.6). Thirteen patients were 24 years old or younger. Procedure
Each subject had been injured less than a year when first examined. Most were examined within four to six weeks after return of consciousness but six of them did not have the initial examination until the latter half of the first year post injury. Twenty-three of the 24 subjects were examined within the second six months of the first year; all 24 were reexamined during the second year post injury and again during the third post trauma year. Verbal memory and learning were measured by Digits Forward (DF) and Digits Backward (DB) following Wechsler's instructions (1955); and by four trials of Rey's Auditory-Verbal Learning Test (AVLT) (Lezak, 1976; Rey, 1964). This latter test presents the subject the task of learning 15 common words in a series of five immediate recall trials. Following the 5-trial learning presentation, a second 15-word list is presented for immediate recall after which the subject is asked to recall as much as he can remember of the first list. Thus trial I tests immediate memory under a stimulus overload condition (i.e., unlike Digit Span, more material is presented for immediate memory than can be grasped in a single trial); trial V measures the amount of material retained after five immediately successive repetitions (i.e., simple learning); trial B, involving the second word list, tests immediate memory under stimulus overload conditions complicated by the possibility of proactive inhibition, and serves as an interference trial; and trial VI tests retention following the interference trial that typically takes three to five minutes from introduction through completion. Data analysis
Each AVLT and Digit Span score was classified as falling either within normal limits (i.e., within or above the average range of scores for that measure) or not within normal limits (i.e., below the average range of scores for that measure. Within normal limits (wnl) for each of the measures was defined as follows: DF = 6; DB= 5; AVLT-I = 6, AVLT-V = 12; AVLT-B = 6; AVLTVI 10 (see Lezak, 1976, for AVLT normative data). Using the dichotomized scores, the following questions were examined by means of a 2 X 2 contingency table (Finney, Latscha, Bennett and Hsu, 1963 ):
=
(1) How do the different functions (e.g., immediate memory, retention, immediate memory under stimulus overload conditions) change over time relative to one another? To answer this question, each possible pairing of the four AVLT measures and DF and DB were compared at each time frame for the proportion of wnl scores (see Table I).
65
Recovery of me1nory and learning functions
(2) Is site of injury related to change over time? To answer this question, comparisons were made of each of the six measures between each pairing of the three localization groups, L, R., and B/D, at each time frame for the proportion of wnl scores (see Table II.) (3) Is severity of injury related to change over time? To answer this question, the subjects were classified into one of two groups, unconscious less than two weeks and unconscious two weeks or more. Comparisons were made between these two groups for each of the six measures at each time frame for the proportion of wnl scores (see Table III).
(4) Is age at time of injury related to change over time? To answer this question, the subjects were classified into one of two groups, under 25 (U) or over 25 (0). Comparisons were made between the two age groups for each of the six measures at each time frame for the proportion of wnl scores.
RESULTS
The following profile of memory and learning functions of this sample of traumatically brain-injured patients emerged: (1) Only DF and AVLT-1, the simplest measures of immediate memory, registered systematic improvement over time (see Table I). Consistent imTABLE I
Percent of Subjects Performing Within Normal Limits on Each of Six Measures of Verbal Memory and Learning at Each Time Frame
Months since injury
Measure
0-6
7-12
13-24
25-36
AVLT I B
39 28
VI
6
6
48 30 22 13
48 48 17 30
58 17 29 25
Digit Span Forward Backward
47 41
65 52
70 56
83 39
v
Differences between measures reaching significance at each time frame: I·V,I·VI I·V,B·V Level of significance :~i I·VI
l
I·V,I·VI I·V,DF·DB
provement on DF produced a significant (p < .05) increase in the number of wnl performances on the fourth (within the third year) examination over the first (within six months) examination. On the AVLT measures, all of which measure aspects of memory or
66
M.D. Lezak
learning more complex than DF, fewer than half the subjects achieved wnl scores with the single exception of the third year trial of the least complex and demanding of these measures (AVLT-I). At best, only 30% of the sample achieved wnl scores on the two learning measures (AVLT-V and VI); and for the most part, the percentage of wnl scores on these two measures remained in the lowest quartile and not statistically distinguishable from one time frame to another. Moreover, when each measure was compared with scores obtained on the other measures at each time interval, a consistent and significant increase in the proportion of wnl performances was registered only by the two simplest measures of immediate memory, AVLT-I and DF. In sharp contrast, few gains were made on the two more complex immediate memory tasks, AVLT-B or DB, or on either measure of learning. In fact, of these latter four measures, all scores but those for AVLT-V, the simplest learning task, followed a similar pattern of gain from the earliest testing through the second year with a loss in the third year which, in the case of AVLT-B, was of significant (p < .05) dimensions. (2) By and large, site of injury made little difference in the proportion of wnl performances. On AVLT-I, R patients performed better than L patients at each time interval, but the difference between them reached statistical significance only in the fourth examination (see Table II). On every measure, L patients performed least well immediately post trauma and while their course differed from measure to measure, they tended to show least improvement. Only on DB did both L and B/D patient groups outstrip those whose injuries were predominantly right-sided, and then only after the first year post trauma. (3) On every measure, the more severely injured subjects (unconscious two or more weeks) performed more poorly at initial testing than those less severely injured (see Table III). On two of the measures, AVLT-I and AVLT-B, this difference reached significance. Further, on all of the measures at every testing the less severely injured subjects maintained their performance superiority. However, although the severely injured subjects displayed a considerable improvement trend from the first to the fourth examination on DF, no statistically significant gains were made by either severity group. (4) On none of the six measures at any of the four time frames did a significant difference occur on the basis of age.
DISCUSSION
The extent to which traumatically brain-injured men recover verbal memory and learning appears to vary with the nature of the function, task,
TABLE II
~easure
~easure
~easure
40 43 60
0 43 40
17 43 60 AVLT-B
AVLT-I 37 57 50
13-24
37 57 50 Digits Forward 62 75 57 62 75 71
25 43 25
25 71 50
7-12
* Difference between subgroups at .05 level of significance ** Difference between subgroups at .01 level of significance
Left Right Bi/Dif
Left Right Bi/Dif
Subgroup Left Right Bi/Dif
0-6
87 75 86
12 12 25
L·R* 1'
37 87 50
25-36
~onths
40 43 40
0 0 20
0 0 20
0-6
sipce injury
12 29 12
R·BjD*
AVLT-VI
AVLT-V
13-24
25 12 0 57 12 12 Digit Backwards 38 50 71 38 50 86
12 43 12
7-12
38 25 57
25 25 25
25 37 25
25-36
Percent of Each Localization Group Performing Within Normal Limits on Each of Six Measures of Verbal Memory and Learning at Each Time Frame
~
...,~
~ ~
":::-.a
0
~·
~
-
"'"'....
~
"';:,...
-
~
~
"'~ a
-
?;l
"'"a '"'...." ""'a
2 weeks 2 weeks
~
~ ~
Measure
Measure
Measure
64 17
45* 0
64* 0
0-6
AVLT-B
AVLT-I 67 27
13-24
67 27 9 Digits Forward 77 75 60 54
50*
75* 18
7-12
* Difference between subgroup pairs at .05 level of significance ** Difference between subgroup pairs at .01 level of significance
weeks 2 weeks
