Journal of Consulting and Clinical Psychology 1977, Vol. 45, No. 4, 684-688
Assessment of Long-Term Memory in Brain-Damaged Patients Harvey S. Levin, Robert G. Grossman, and Patrick J. Kelly Division of Neurosurgery, University of Texas Medical Branch, Galveston A standardized questionnaire that tested the ability to recognize the names of television programs broadcast for a single year was found to provide an efficient method of examining long-term memory in patients with brain damage of diverse common etiologies. Contrary to the widely accepted view that remote memory is relatively invulnerable to disruption caused by cerebral disease, recognition memory was least efficient for titles of older programs in both brain-damaged and control groups. The relative degree of deficit in patients with brain lesions proved to be minimal for the most recently aired programs as compared with more remote information. These findings are discussed with respect to studies of markedly amnesic patients. Methodological problems involved in the assessment of remote memory are also considered. Clinical assessment of long-term memory (LTM) has been complicated by the practical problems inherent in an extended learningretention interval. Consequently, clinicians have generally relied on anecdotal observations and interview material (e.g., birthplace, personal history) to evaluate LTM. In contrast to novel material presented to the patient when testing short-term memory (e.g., paragraphs, geometric designs), the uncontrolled approach to evaluating LTM. is generally confined to information that has been well rehearsed and that can be difficult to verify. Experiments on animals (Orbach & Fantz, 1958) and human neuropsychological studies (Benton, Levin, & Van Allen, 1974) have established that overlearned material is relatively invulnerable to disruption by subsequent brain lesions. Attempts to quantify and better control the assessment of LTM have largely consisted of recall and recognition tests for previous public events and photographs of faces of public This study was supported by National Institutes of Health Grant DHEW 2PO1 NS 07377-06. We are indebted to Larry Squire of the University of California School of Medicine, San Diego, for providing us with his television program questionnaire and to Valerie Buege, Paula Grosse, and Maury Kleiman for their assistance in testing patients. Requests for reprints should be sent to Robert G. Grossman, Division of Neurosurgery, University of Texas Medical 15ranch, Galveston, Texas 77550.
figures who were prominent in past decades (Marslen-Wilson & Teuber, 1975; Sanders & Warrington, 1971; Seltzer & Benson, 1974; Squire, 1974). Utilizing this procedure, gerontological studies (Sanders & Warrington, 1971; Squire, 1974) have yielded findings opposite to the dictum (Ribot, 1882) that the extent of memory loss for any past event is inversely related to the time since its occurrence. These studies have found that LTM in middle-aged and elderly normal adults is least efficient for the oldest or most remote events. Comparison of performance across age groups revealed a significant decline in LTM in elderly persons that was relatively constant in magnitude across varying levels of remoteness (Sanders & Warrington, 1971; Squire, 1974). Quantitative investigation of LTM in relation to cerebral pathology has been limited to testing patients with severe anterograde amnesia (impaired learning and retention of new information) secondary to Korsakoff's syndrome or bilateral temporal lobectomy on protocols concerning past events or photographs of public figures. Sanders and Warrington (1971) found that LTM in amnesic patients was impaired for information spanning a 50year period without evidence of less severe disruption of more remote items. In contrast, recent studies have shown that the degree of LTM deficit in amnesic patients is inversely related to the remoteness of the memoranda
684
LONG-TERM MEMORY
(Marslen-Wilson & Teuber, 1975; Seltzer & Benson, 1974). In the former study, LTM for events preceding the onset of brain damage was remarkably preserved. Similar procedures were recently used by Squire, Slater, and Chace (1975) to uncover disruption of LTM following electroconvulsive therapy in depressed psychiatric patients. Although it is clear that cerebral pathology may impair LTM, potential application of tests based on public events poses methodological problems. The assumption that acquisition of information about an event is temporally contiguous with its occurrence is tenuous; recently acquired historical information may account for recall of well-known past events. Equating the level of difficulty across time periods and cultural variation in following the news have also complicated attempts to use public events in evaluating LTM. Recently, Squire and Slater (1975) have attempted to circumvent these methodological problems by assessing LTM in terms of recognition of the names of television shows. Selection of television shows aired for a single season assumes that information tested on the questionnaire is acquired close to the time the events occurred. This assumption was supported by Squire's finding that students had inferior scores on items concerning programs aired when they were very young and that adults had low scores on questions concerning programs that were aired while they were living outside of the United States. Preliminary investigation by Squire and Slater (1975) supported the assumption that exposure of American audiences to programs from different years was approximately constant. The present study was undertaken to evaluate LTM in patients with brain damage of common etiologies, since previous studies of LTM in patients with brain lesions have been confined to patients with KorsakofFs syndrome or bilateral temporal lobectomy who comprise a small proportion of the population referred for neuropsychological assessment in most clinical settings. The findings yielded an estimate of the extent of LTM deficit in brain-damaged patients and provided a test of Ribot's (1882) postulation concerning the relative invulnerability of remote memories.
685 Method
Subjects Twenty-eight adult patients with evidence of brain damage who were treated by the Neurology and Neurosurgery Services, University of Texas Medical Branch at Galveston, were tested. The presence of a brain lesion was inferred from unequivocal neurologic deficits and the results of ncurodiagnostic procedures (e.g., electroencephalogram, brain scan). Surgical findings were also available for six of the brain-damaged patients. Patients were excluded from the study if they had a history of alcoholism or were unable to cooperate with the testing procedure. Table 1 shows the biographic data and indicates that head injury and neoplasm were the most frequent etiologies of brain damage in this sample. Although several patients had lateralized cerebral disease, no attempt was made to select cases with focal cerebral pathology. Patients admitted on the general medical service without evidence or history of cerebral disease or injury and normal subjects comprised the group. Analysis indicated that the medical patients did not differ in performance on the experimental task from other adults of comparable age and educational level. Participants in the control group were individually matched to brain-damaged patients on the basis of age and years of education. The age of patients with brain lesions (M = 32.14, SD = 13.35) did not significantly differ from that of the control group (M = 31.86, SD = 12.90) according to the I test. i'Mucational level in brain-damaged patients (M = 11.59, SD = 2.06) was also comparable to that of the control group (M = 11.86, 5W = 1.76). There were 19 men and 9 women in each group.
Procedure ' Long-term recognition memory was assessed by a multiple-choice test wherein the subject was asked to select television programs that were broadcast nationally for a single season. The instrument used was a modified version of the questionnaire constructed by Squire and Slater (1975), which was confined to weekly evening programs. The protocol consisted of 32 questions that were equally divided among four levels of remoteness: 1966-1967, 1968-1969, 1970-1971, and 1972-1973. Questions representing each level of remoteness were randomly interspersed. ICach question asked: "Which of the following was a TV show?" Three incorrect choices (fictitious programs) were presented with each show. The target programs were verified by their listings in issues of local newspapers printed in the relevant years and by consulting a television network affiliate in Houston. Details concerning development of the questionnaire have been published (Squire & Slater, 1975). Subjects were tested individually and were not given feedback regarding the correctness of their choices. No time limit was used; subjects were encouraged to guess rather than omit questions.
686
H. LEVIN, R. GROSSMAN, AND P. KELLY
Table 1
Biographic Data, Test Score, and Diagnosis for Brain-Damaged Patients Patient 1 2
3 4
5 6 7 8 9 10 11 12 13 14 15 16
Age
Education
30 35 20 19 32 20 28 19 19
12.0 12.0 12.0 12.0 12.0 11.0 13.0
17
11.0
16 26
9.0
20
51 43 23 51
17 18
36 35 37 30 53 43 61 35 58 17 26
19 20 21 22
23 24 25 26 27 28
10.0 11.0
13.0 12.0 7.0
11.5 13.5 7.0 12.0 16.0 16.0 12.0
12.0 12.0 12.0 11.0 10.0 9.0 13.5
Sex
Score
Diagnosis
Male Male Male Male Male Male Male Male Male
24 19 24 18 6 9
Female Male Male Female Female Female Female Male Male Male Female Female Male Female Female Male Male Male Male
17 12 16
CHI with right orbital fracture CHI with multiple skull fractures CHI with left temporal fracture CHI with right fron to-temporal fracture CHI with frontal and basilar fracture CHI with right frontal intracerebral hematoma CHI CHI with frontal and basilar fractures CHI with right fronto-parietal epidural hematoma CHI with brain stem injury CHI CHI Left temporal gunshot wound Right parieto-occipital meningioma Right occipital astrocytoma Fourth ventricle tumor Left temporo-parietal glioblastoma Bilateral frontal glioblastoma Subarachnoid hemorrhage Right parietal CVA Right frontal aneurysm Parkinson's disease Huntington's chorea Alzheimer's disease Encephalopathy-heavy metal toxicity Encephalopathy-drug toxicity Bacterial meningitis Seizure disorder —grand mal
28 16 18
26 12 21
26 9 16 15 19 16 14
18 6 11 11 12 12
Note. CHI = closed head i n j u r y ; CVA = cerebrovascular accident; a perfect test score = 32.
Results Means and standard deviations for the number of correct responses at each level of Table 2 Recognition Memory Scores for Programs Broadcast During Various Time Periods Time
Control
Brain damaged
5.21 1.40
3.71 1.51
6.71 1.24
4.82 2.02
5.61
3.50
1.55
1.86
5.25 2.03
4.11 2.13
1966-1967
M SD 1968-1969 M SD 1970-1971 M SD 1972-1973
M SD
Note, n = 28 for each group.
remoteness are given for the brain-damaged and control groups in Table 2; test scores of individual brain-damaged patients appear in Table 1. Figure 1 depicts the corresponding percentage of correct responses and shows that the performance of brain-damaged patients was consistently below that of the control group. The functions given in Figure 1 are nearly parallel and also do not suggest relative preservation of older memoranda. However, peak retention in both groups was obtained for programs in 1968-1969. A 2 X 2 analysis of variance of the test scores was undertaken because the hypothesis of homogeneity of variance could not be rejected (Table 2). This procedure yielded a highly significant main effect for groups, F(l, 54) = 28.33, p < .001; for year of program, F(3, 162) = 15.47, p < .001, and for Groups X Years, F(3, 162) = 17.19, p < .001. Pairwise contrasts disclosed significantly higher scores in the control group for programs aired in 1966-
LONG-TERM MEMORY
1967 (t = 4.86, p < .0001), 1968-1969 (t = 6.12, p < .0001), 1970-1971 (t = 6.83, p < .0001), and 1972-1973 (t = 3.69, p < .001). Inspection of Figure 1 for sources of the interaction suggests that the magnitude of the difference in scores between the braindamaged and control groups was attenuated for the most recent programs (1972-1973) as compared with more remote information. Comparison of the group differences for programs in 1972-1973 with the differences obtained for other years yielded a significant effect only in relation to 1968-1969 (t = 2.43, p < .02) and 1970-1971 (/ = 3.12, p < .01). Pairwise contrasts did not disclose any other sources of interaction. Figure 1 depicts a nonmonotonic relationship between memory score and time period of programs; there is no consistent trend toward greater preservation of the most remote information. Recognition of programs aired in 1968-1969 was superior to the scores obtained for other years in both the brain-damaged (p < .01) and control (p < .01) groups. Further analysis did not demonstrate any other significant differences between time periods within either group. Scores for programs aired in 1966-1967 were compared to those aired in 1972-1973 in an attempt to uncover impressive instances of preservation of old memories. Within the control group, the greatest intraindividual decline in scores between 1966-1967 and 19721973 was from 7 to 1 (86% loss). By comparison, the brain-damaged patient manifesting the greatest decline had scores of 5 and 1 in 1966-1967 and 1972-1973, respectively (a reduction of 80%). Supplementary analysis was undertaken to compare the performance of patients with acute onset (post-1973) of brain damage with that of patients whose brain disease was slow in developing and presumably caused disruption of storage of information about the recent programs in short-term memory or disruption of transfer to LTM. Of the patients described in Table 1, the 13 cases of head injury were selected as the acute onset (Mdn duration of injury-test interval = 30 days) subgroup. The slow-onset (Mdn duration of illness = 270 days) subgroup consisted of the five patients with neoplasm and the three patients with Parkinson's disease, Huntington's chorea, or
687
,
, Control (n = 2Q)
X
x Braindamaged (n=28)
t 60e> o
«
50-
V
1966-1967
1968-1969
1970-1971
1972-1973
TIME PERIOD OF PROGRAM
Figure 1. Percent correct recognition memory as a function of the time period of the television program.
Alzheimer's disease. Reasonably accurate estimation of the onset of illness was not possible in the remaining cases. Preliminary comparison revealed that patients in the slow-onset group (M age = 45.13, SD = 11.74) were significantly older than recently injured patients (M age = 23.15, SD = 6.24; t = 4.89, p < .002), and educational level was comparable in the two subgroups. Although there was a trend suggesting higher total scores in the head-injured group (M = 17.92, SD = 6.50) than in the slow-onset patients (M = 15.25, SD = 6.48), the difference was not significant (t = .92). Separate comparisons of these groups for programs within each time period yielded no significant findings. Discussion The present study used a convenient instrument to evaluate recognition memory following an extended retention interval. Previous findings of an LTM deficit in brain-damaged patients with severe anterograde amnesia (Marslen-Wilson & Teuber, 1975; Sanders & Warrington, 1971; Seltzer & Benson, 1974) were extended to a sample of patients with brain lesions of diverse etiologies. No patient in this series was known to have a marked amnesic syndrome, though deficits in memory
688
H. LEVIN, R. GROSSMAN, AND P. KELLY
were suspected. The results indicate that examination. By comparison with tests based memory deficit in patients with cerebral on public events, questionnaires concerning disease or injury is not confined to short-term network programs aired for a single year are memory or to transfer of information to long- probably less affected by cultural variation, term storage. Although impairment of initial since 97% of American households had a storage of information about the recent television set in 1972 (Squire & Slater, 1975). programs and transfer to LTM may have Moreover, Squire has argued cogently that contributed to the difficulty encountered by this approach facilitates test construction patients with slow onset of illness, their per- wherein items sampled from different time formance did not differ impressively from that periods are comparable in difficulty. Although of patients with recent head injuries. This application of this technique is limited to iinding should be interpreted with caution television viewers, it should be noted that inasmuch as duration of illness was confounded occasional viewing provides an opportunity for by age in these patients. Extending the incidental learning as numerous programs are series of head-injured patients studied in our advertised. Extensive use of a television laboratory may clarify the relative contribu- questionnaire would require separate normations of short-term memory impairment versus tive data for subjects of varying ages (Sanders retrieval from LTM. & Warrington, 1971; Squire, 1974). Moreover, Contrary to Ribot's (1882) postulation annual updating of the instrument is necessary of the invulnerability of remote memory in to maintain a constant retention interval. patients with cerebral disease, LTM in patients It would also be imperative to verify locally with brain lesions was relatively preserved that the programs were televised during the for the most recently aired programs. Our designated time periods. results corroborate previous findings in normal adults (Sanders & Warrington, 1971; Squire, References 1974; Squire & Slater, 1975), which indicate that LTM is least efficient for remote memo- Benton, A. L., Levin, H. S., & Van Allen, M. W. Geographic orientation in patients with cerebral randa. Although two investigations (Marslendisease. Neuropsychohgia, 1974, 12, 183-191. Wilson & Teuber, 1975; Seltzer & Benson, Marslen-Wilson, W. U., & Teuber, H. L. Memory 1974) have reported relative preservation for remote events in anterograde amnesia: Recogniof remote memory in amnesic patients, neither tion of public figures from newsphotographs. Neuropsychologia, 1975, 13, 353-364. study could document that opportunity for exposure to the memoranda was restricted to Orbach, J., & Fantz, R. L. Differential effects of temporal neocortical resections -on overtrained and the nominal time period. In contrast, Squire non-trained visual habits in monkeys. Journal of and Slater (1975) found that normal subjects Comparative and Physiological Psychology, 1958, failed to recognize programs that were broad57, 126-129. cast while they were overseas or younger Ribot, T. Diseases of memory. New York: Appleton, 1882. than 9 years old. Functions relating accuracy Sanders, H. I., & Warrington, E. K. Memory for of LTM to year of program were nonmonotonic remote events in amnesic patients. Brain, 1971, 94, in both groups, with peak performance at an 661-668. intermediate level of remoteness. Consistent Seltzer, B., & Benson, D. F. The temporal pattern of retrograde amnesia in Korsakoff's disease. Neurology, with this finding, Squire et al. (1975) found 1974, 24, 527-530. that optimal performance in patients under- Squire, L. R., Remote memory as affected by aging, going electroconvulsive treatment was achieved Neuropsychologia, 1974, 12, 429-435. for programs aired in 1969-1970 as compared Squire, L. R., & Slater, P. C. Forgetting in very longterm memory as assessed by an improved questionto both earlier and more recent programs. naire technique. Journal of Experimental Psychology: Clinical implications of the present study Human Learning and Memory, 1975, 1, 50-54. include the possibility of utilizing similar Squire, L. R., Slater, P. C., & Chace, P. M. Retrograde amnesia: Temporal gradient in very long term procedures to uncover impairment of remote memory following electroconvulsive therapy. Science, memory in patients whose recollection of 1975, 187, 77-79. deeply ingrained memoranda (e.g., high school graduation) appears to be intact on routine Received June 14, 1976 •
Assessment of Long-Term Memory in Brain-Damaged Patients Harvey S. Levin, Robert G. Grossman, and Patrick J. Kelly Division of Neurosurgery, University of Texas Medical Branch, Galveston A standardized questionnaire that tested the ability to recognize the names of television programs broadcast for a single year was found to provide an efficient method of examining long-term memory in patients with brain damage of diverse common etiologies. Contrary to the widely accepted view that remote memory is relatively invulnerable to disruption caused by cerebral disease, recognition memory was least efficient for titles of older programs in both brain-damaged and control groups. The relative degree of deficit in patients with brain lesions proved to be minimal for the most recently aired programs as compared with more remote information. These findings are discussed with respect to studies of markedly amnesic patients. Methodological problems involved in the assessment of remote memory are also considered. Clinical assessment of long-term memory (LTM) has been complicated by the practical problems inherent in an extended learningretention interval. Consequently, clinicians have generally relied on anecdotal observations and interview material (e.g., birthplace, personal history) to evaluate LTM. In contrast to novel material presented to the patient when testing short-term memory (e.g., paragraphs, geometric designs), the uncontrolled approach to evaluating LTM. is generally confined to information that has been well rehearsed and that can be difficult to verify. Experiments on animals (Orbach & Fantz, 1958) and human neuropsychological studies (Benton, Levin, & Van Allen, 1974) have established that overlearned material is relatively invulnerable to disruption by subsequent brain lesions. Attempts to quantify and better control the assessment of LTM have largely consisted of recall and recognition tests for previous public events and photographs of faces of public This study was supported by National Institutes of Health Grant DHEW 2PO1 NS 07377-06. We are indebted to Larry Squire of the University of California School of Medicine, San Diego, for providing us with his television program questionnaire and to Valerie Buege, Paula Grosse, and Maury Kleiman for their assistance in testing patients. Requests for reprints should be sent to Robert G. Grossman, Division of Neurosurgery, University of Texas Medical 15ranch, Galveston, Texas 77550.
figures who were prominent in past decades (Marslen-Wilson & Teuber, 1975; Sanders & Warrington, 1971; Seltzer & Benson, 1974; Squire, 1974). Utilizing this procedure, gerontological studies (Sanders & Warrington, 1971; Squire, 1974) have yielded findings opposite to the dictum (Ribot, 1882) that the extent of memory loss for any past event is inversely related to the time since its occurrence. These studies have found that LTM in middle-aged and elderly normal adults is least efficient for the oldest or most remote events. Comparison of performance across age groups revealed a significant decline in LTM in elderly persons that was relatively constant in magnitude across varying levels of remoteness (Sanders & Warrington, 1971; Squire, 1974). Quantitative investigation of LTM in relation to cerebral pathology has been limited to testing patients with severe anterograde amnesia (impaired learning and retention of new information) secondary to Korsakoff's syndrome or bilateral temporal lobectomy on protocols concerning past events or photographs of public figures. Sanders and Warrington (1971) found that LTM in amnesic patients was impaired for information spanning a 50year period without evidence of less severe disruption of more remote items. In contrast, recent studies have shown that the degree of LTM deficit in amnesic patients is inversely related to the remoteness of the memoranda
684
LONG-TERM MEMORY
(Marslen-Wilson & Teuber, 1975; Seltzer & Benson, 1974). In the former study, LTM for events preceding the onset of brain damage was remarkably preserved. Similar procedures were recently used by Squire, Slater, and Chace (1975) to uncover disruption of LTM following electroconvulsive therapy in depressed psychiatric patients. Although it is clear that cerebral pathology may impair LTM, potential application of tests based on public events poses methodological problems. The assumption that acquisition of information about an event is temporally contiguous with its occurrence is tenuous; recently acquired historical information may account for recall of well-known past events. Equating the level of difficulty across time periods and cultural variation in following the news have also complicated attempts to use public events in evaluating LTM. Recently, Squire and Slater (1975) have attempted to circumvent these methodological problems by assessing LTM in terms of recognition of the names of television shows. Selection of television shows aired for a single season assumes that information tested on the questionnaire is acquired close to the time the events occurred. This assumption was supported by Squire's finding that students had inferior scores on items concerning programs aired when they were very young and that adults had low scores on questions concerning programs that were aired while they were living outside of the United States. Preliminary investigation by Squire and Slater (1975) supported the assumption that exposure of American audiences to programs from different years was approximately constant. The present study was undertaken to evaluate LTM in patients with brain damage of common etiologies, since previous studies of LTM in patients with brain lesions have been confined to patients with KorsakofFs syndrome or bilateral temporal lobectomy who comprise a small proportion of the population referred for neuropsychological assessment in most clinical settings. The findings yielded an estimate of the extent of LTM deficit in brain-damaged patients and provided a test of Ribot's (1882) postulation concerning the relative invulnerability of remote memories.
685 Method
Subjects Twenty-eight adult patients with evidence of brain damage who were treated by the Neurology and Neurosurgery Services, University of Texas Medical Branch at Galveston, were tested. The presence of a brain lesion was inferred from unequivocal neurologic deficits and the results of ncurodiagnostic procedures (e.g., electroencephalogram, brain scan). Surgical findings were also available for six of the brain-damaged patients. Patients were excluded from the study if they had a history of alcoholism or were unable to cooperate with the testing procedure. Table 1 shows the biographic data and indicates that head injury and neoplasm were the most frequent etiologies of brain damage in this sample. Although several patients had lateralized cerebral disease, no attempt was made to select cases with focal cerebral pathology. Patients admitted on the general medical service without evidence or history of cerebral disease or injury and normal subjects comprised the group. Analysis indicated that the medical patients did not differ in performance on the experimental task from other adults of comparable age and educational level. Participants in the control group were individually matched to brain-damaged patients on the basis of age and years of education. The age of patients with brain lesions (M = 32.14, SD = 13.35) did not significantly differ from that of the control group (M = 31.86, SD = 12.90) according to the I test. i'Mucational level in brain-damaged patients (M = 11.59, SD = 2.06) was also comparable to that of the control group (M = 11.86, 5W = 1.76). There were 19 men and 9 women in each group.
Procedure ' Long-term recognition memory was assessed by a multiple-choice test wherein the subject was asked to select television programs that were broadcast nationally for a single season. The instrument used was a modified version of the questionnaire constructed by Squire and Slater (1975), which was confined to weekly evening programs. The protocol consisted of 32 questions that were equally divided among four levels of remoteness: 1966-1967, 1968-1969, 1970-1971, and 1972-1973. Questions representing each level of remoteness were randomly interspersed. ICach question asked: "Which of the following was a TV show?" Three incorrect choices (fictitious programs) were presented with each show. The target programs were verified by their listings in issues of local newspapers printed in the relevant years and by consulting a television network affiliate in Houston. Details concerning development of the questionnaire have been published (Squire & Slater, 1975). Subjects were tested individually and were not given feedback regarding the correctness of their choices. No time limit was used; subjects were encouraged to guess rather than omit questions.
686
H. LEVIN, R. GROSSMAN, AND P. KELLY
Table 1
Biographic Data, Test Score, and Diagnosis for Brain-Damaged Patients Patient 1 2
3 4
5 6 7 8 9 10 11 12 13 14 15 16
Age
Education
30 35 20 19 32 20 28 19 19
12.0 12.0 12.0 12.0 12.0 11.0 13.0
17
11.0
16 26
9.0
20
51 43 23 51
17 18
36 35 37 30 53 43 61 35 58 17 26
19 20 21 22
23 24 25 26 27 28
10.0 11.0
13.0 12.0 7.0
11.5 13.5 7.0 12.0 16.0 16.0 12.0
12.0 12.0 12.0 11.0 10.0 9.0 13.5
Sex
Score
Diagnosis
Male Male Male Male Male Male Male Male Male
24 19 24 18 6 9
Female Male Male Female Female Female Female Male Male Male Female Female Male Female Female Male Male Male Male
17 12 16
CHI with right orbital fracture CHI with multiple skull fractures CHI with left temporal fracture CHI with right fron to-temporal fracture CHI with frontal and basilar fracture CHI with right frontal intracerebral hematoma CHI CHI with frontal and basilar fractures CHI with right fronto-parietal epidural hematoma CHI with brain stem injury CHI CHI Left temporal gunshot wound Right parieto-occipital meningioma Right occipital astrocytoma Fourth ventricle tumor Left temporo-parietal glioblastoma Bilateral frontal glioblastoma Subarachnoid hemorrhage Right parietal CVA Right frontal aneurysm Parkinson's disease Huntington's chorea Alzheimer's disease Encephalopathy-heavy metal toxicity Encephalopathy-drug toxicity Bacterial meningitis Seizure disorder —grand mal
28 16 18
26 12 21
26 9 16 15 19 16 14
18 6 11 11 12 12
Note. CHI = closed head i n j u r y ; CVA = cerebrovascular accident; a perfect test score = 32.
Results Means and standard deviations for the number of correct responses at each level of Table 2 Recognition Memory Scores for Programs Broadcast During Various Time Periods Time
Control
Brain damaged
5.21 1.40
3.71 1.51
6.71 1.24
4.82 2.02
5.61
3.50
1.55
1.86
5.25 2.03
4.11 2.13
1966-1967
M SD 1968-1969 M SD 1970-1971 M SD 1972-1973
M SD
Note, n = 28 for each group.
remoteness are given for the brain-damaged and control groups in Table 2; test scores of individual brain-damaged patients appear in Table 1. Figure 1 depicts the corresponding percentage of correct responses and shows that the performance of brain-damaged patients was consistently below that of the control group. The functions given in Figure 1 are nearly parallel and also do not suggest relative preservation of older memoranda. However, peak retention in both groups was obtained for programs in 1968-1969. A 2 X 2 analysis of variance of the test scores was undertaken because the hypothesis of homogeneity of variance could not be rejected (Table 2). This procedure yielded a highly significant main effect for groups, F(l, 54) = 28.33, p < .001; for year of program, F(3, 162) = 15.47, p < .001, and for Groups X Years, F(3, 162) = 17.19, p < .001. Pairwise contrasts disclosed significantly higher scores in the control group for programs aired in 1966-
LONG-TERM MEMORY
1967 (t = 4.86, p < .0001), 1968-1969 (t = 6.12, p < .0001), 1970-1971 (t = 6.83, p < .0001), and 1972-1973 (t = 3.69, p < .001). Inspection of Figure 1 for sources of the interaction suggests that the magnitude of the difference in scores between the braindamaged and control groups was attenuated for the most recent programs (1972-1973) as compared with more remote information. Comparison of the group differences for programs in 1972-1973 with the differences obtained for other years yielded a significant effect only in relation to 1968-1969 (t = 2.43, p < .02) and 1970-1971 (/ = 3.12, p < .01). Pairwise contrasts did not disclose any other sources of interaction. Figure 1 depicts a nonmonotonic relationship between memory score and time period of programs; there is no consistent trend toward greater preservation of the most remote information. Recognition of programs aired in 1968-1969 was superior to the scores obtained for other years in both the brain-damaged (p < .01) and control (p < .01) groups. Further analysis did not demonstrate any other significant differences between time periods within either group. Scores for programs aired in 1966-1967 were compared to those aired in 1972-1973 in an attempt to uncover impressive instances of preservation of old memories. Within the control group, the greatest intraindividual decline in scores between 1966-1967 and 19721973 was from 7 to 1 (86% loss). By comparison, the brain-damaged patient manifesting the greatest decline had scores of 5 and 1 in 1966-1967 and 1972-1973, respectively (a reduction of 80%). Supplementary analysis was undertaken to compare the performance of patients with acute onset (post-1973) of brain damage with that of patients whose brain disease was slow in developing and presumably caused disruption of storage of information about the recent programs in short-term memory or disruption of transfer to LTM. Of the patients described in Table 1, the 13 cases of head injury were selected as the acute onset (Mdn duration of injury-test interval = 30 days) subgroup. The slow-onset (Mdn duration of illness = 270 days) subgroup consisted of the five patients with neoplasm and the three patients with Parkinson's disease, Huntington's chorea, or
687
,
, Control (n = 2Q)
X
x Braindamaged (n=28)
t 60e> o
«
50-
V
1966-1967
1968-1969
1970-1971
1972-1973
TIME PERIOD OF PROGRAM
Figure 1. Percent correct recognition memory as a function of the time period of the television program.
Alzheimer's disease. Reasonably accurate estimation of the onset of illness was not possible in the remaining cases. Preliminary comparison revealed that patients in the slow-onset group (M age = 45.13, SD = 11.74) were significantly older than recently injured patients (M age = 23.15, SD = 6.24; t = 4.89, p < .002), and educational level was comparable in the two subgroups. Although there was a trend suggesting higher total scores in the head-injured group (M = 17.92, SD = 6.50) than in the slow-onset patients (M = 15.25, SD = 6.48), the difference was not significant (t = .92). Separate comparisons of these groups for programs within each time period yielded no significant findings. Discussion The present study used a convenient instrument to evaluate recognition memory following an extended retention interval. Previous findings of an LTM deficit in brain-damaged patients with severe anterograde amnesia (Marslen-Wilson & Teuber, 1975; Sanders & Warrington, 1971; Seltzer & Benson, 1974) were extended to a sample of patients with brain lesions of diverse etiologies. No patient in this series was known to have a marked amnesic syndrome, though deficits in memory
688
H. LEVIN, R. GROSSMAN, AND P. KELLY
were suspected. The results indicate that examination. By comparison with tests based memory deficit in patients with cerebral on public events, questionnaires concerning disease or injury is not confined to short-term network programs aired for a single year are memory or to transfer of information to long- probably less affected by cultural variation, term storage. Although impairment of initial since 97% of American households had a storage of information about the recent television set in 1972 (Squire & Slater, 1975). programs and transfer to LTM may have Moreover, Squire has argued cogently that contributed to the difficulty encountered by this approach facilitates test construction patients with slow onset of illness, their per- wherein items sampled from different time formance did not differ impressively from that periods are comparable in difficulty. Although of patients with recent head injuries. This application of this technique is limited to iinding should be interpreted with caution television viewers, it should be noted that inasmuch as duration of illness was confounded occasional viewing provides an opportunity for by age in these patients. Extending the incidental learning as numerous programs are series of head-injured patients studied in our advertised. Extensive use of a television laboratory may clarify the relative contribu- questionnaire would require separate normations of short-term memory impairment versus tive data for subjects of varying ages (Sanders retrieval from LTM. & Warrington, 1971; Squire, 1974). Moreover, Contrary to Ribot's (1882) postulation annual updating of the instrument is necessary of the invulnerability of remote memory in to maintain a constant retention interval. patients with cerebral disease, LTM in patients It would also be imperative to verify locally with brain lesions was relatively preserved that the programs were televised during the for the most recently aired programs. Our designated time periods. results corroborate previous findings in normal adults (Sanders & Warrington, 1971; Squire, References 1974; Squire & Slater, 1975), which indicate that LTM is least efficient for remote memo- Benton, A. L., Levin, H. S., & Van Allen, M. W. Geographic orientation in patients with cerebral randa. Although two investigations (Marslendisease. Neuropsychohgia, 1974, 12, 183-191. Wilson & Teuber, 1975; Seltzer & Benson, Marslen-Wilson, W. U., & Teuber, H. L. Memory 1974) have reported relative preservation for remote events in anterograde amnesia: Recogniof remote memory in amnesic patients, neither tion of public figures from newsphotographs. Neuropsychologia, 1975, 13, 353-364. study could document that opportunity for exposure to the memoranda was restricted to Orbach, J., & Fantz, R. L. Differential effects of temporal neocortical resections -on overtrained and the nominal time period. In contrast, Squire non-trained visual habits in monkeys. Journal of and Slater (1975) found that normal subjects Comparative and Physiological Psychology, 1958, failed to recognize programs that were broad57, 126-129. cast while they were overseas or younger Ribot, T. Diseases of memory. New York: Appleton, 1882. than 9 years old. Functions relating accuracy Sanders, H. I., & Warrington, E. K. Memory for of LTM to year of program were nonmonotonic remote events in amnesic patients. Brain, 1971, 94, in both groups, with peak performance at an 661-668. intermediate level of remoteness. Consistent Seltzer, B., & Benson, D. F. The temporal pattern of retrograde amnesia in Korsakoff's disease. Neurology, with this finding, Squire et al. (1975) found 1974, 24, 527-530. that optimal performance in patients under- Squire, L. R., Remote memory as affected by aging, going electroconvulsive treatment was achieved Neuropsychologia, 1974, 12, 429-435. for programs aired in 1969-1970 as compared Squire, L. R., & Slater, P. C. Forgetting in very longterm memory as assessed by an improved questionto both earlier and more recent programs. naire technique. Journal of Experimental Psychology: Clinical implications of the present study Human Learning and Memory, 1975, 1, 50-54. include the possibility of utilizing similar Squire, L. R., Slater, P. C., & Chace, P. M. Retrograde amnesia: Temporal gradient in very long term procedures to uncover impairment of remote memory following electroconvulsive therapy. Science, memory in patients whose recollection of 1975, 187, 77-79. deeply ingrained memoranda (e.g., high school graduation) appears to be intact on routine Received June 14, 1976 •
