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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Recovery of orientation following closed-head injury a
b
Walter M. High Jr. , Harvey S. Levin & Howard E. Gary Jr.
c
a
Department of Neuropsychology , The Del Oro Institute for Rehabilitation , Houston, TX b
Division of Neurosurgery , University of Texas Medical Branch , Galveston, TX c
Center for Disease Control , Atlanta, GA Published online: 04 Jan 2008.
To cite this article: Walter M. High Jr. , Harvey S. Levin & Howard E. Gary Jr. (1990) Recovery of orientation following closed-head injury, Journal of Clinical and Experimental Neuropsychology, 12:5, 703-714, DOI: 10.1080/01688639008401013 To link to this article: http://dx.doi.org/10.1080/01688639008401013
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0168-8634~/1205-0703%3.00 0 Swets & Zeitlinger
H 1990, VOI. 12, NO. 5 , pp. 703-714
Recovery of Orientation Following Closed-Head Injury”
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Walter M. High, Jr.’, Harvey S. Levin2, and Howard E. Gary, Jr? Department of Neuropsychology, The Del Oro Institute for Rehabilitation, Houston, TX Division of Neurosurgery, University of Texas Medical Branch, Galveston, TX Center for Disease Control, Atlanta, GA.
ABSTRACT The pattern of recovery of orientation to person, place, and time was investigated in 84 patients who were initially disoriented while hospitalized on the neurosurgery service after sustaining a closed-head injury (CHI) of varying seventy. Results of daily administration of the Galveston Orientation and Amnesia Test revealed that the most common sequence of recovery of orientation was person, place, and time, accounting for about 70% of the patients. Return of orientation to time preceded reorientation to place in 13% of the patients while other orderings of reorientation were present in 11% of the cases. Temporal disorientation was initially characterized by backward displacement of the date from the actual date in 68% of the patients. The magnitude of this displacement progressively shrank as the patients became more oriented. Patients who exhibited the greatest backward displacement of the date had more severe and persistent impaired consciousness, were older and had longer durations of posttraumatic amnesia. These data support Ribot’s hypothesis that older memories are relatively resistant to cerebral insult.
INTRODUCTION Patients sustaining closed-head injuries often have difficulty recalling events which occurred before their injury. Russell (1932) observed that t h e loss o f previously acquired memories was partially reversible. This retrograde deficit, which can initially extend f o r months or years, typically “shrinks” to a brief interval (less than 30 minutes) as the patient’s confusion clears (Benson &
* This research was supported by grant NS-21889, Javits Neuroscience Investigator Award to the second author. We are indebted to Liz Zindler for manuscript preparation and Lori A. Baxter for assistance in data analysis. We also thank Dr. Felicia Goldstein for her review of an earlier version of the manuscript. Portions of this manuscript were part of the first author’s doctoral dissertation and were presented at the Seventeenth Annual Meeting of the International Neuropsychological Society, Vancouver, 1989. Address reprint requests to: Harvey S.Levin, Ph.D., Division of Neurosurgery D-73, The University of Texas Medical Branch, Galveston, Texas 77550, USA. Accepted for publication: November 17, 1989.
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Geschwind, 1967; Russell, 1935; Russell & Nathan, 1946). The observations of Russell and his co-workers (Russell, 1932, 1935, 1971; Russell & Nathan, 1946; Russell & Smith, 1961) were extended by Levin et al. (1985) who found that recently acquired autobiographical infomation was more vulnerable to disruption by head injury than older autobiographical material. The pattern of retrograde memory loss has been examined in other clinical populations. Daniel, Crovitz, and Weiner (1987) studied the recovery of orientation to person, place, and time in patients undergoing a course of electroconvulsive therapy (ECT) for depression. These investigators confirmed that orientation to person returned first, followed by orientation to place, and then orientation to time. The pattern of retrograde memory loss after ECT was reflected by the patients’ estimates of their age and current date which were displaced backwards in time, suggesting an inability to access more recently acquired information. Consistent with Ribot’s law (see Levin, Peters, & Wulkonen, 1983 for a historical review) of older memories being more impervious to cerebral insult than more recently acquired memories, the discrepancy progressively “shrank” between the patients’ estimate of their age and the date as compared to their true age and the true date. The study of Daniel et al. (1987) raised the issue of whether a similar pattern of resolution of retrograde amnesia (RA) is present after head injury. We have serially investigated the recovery of orientation to person, place, and time in head injured patients. The recovery pattern of retrograde memory loss was indexed by the relationship between the patients’ estimates of the current date and resolution of anterograde amnesia. Second, the effect of subject variables such as age, severity of injury, and focal pathology on recovery of RA and posttraumatic amnesia (PTA) was examined to elucidate possible underlying mechanisms. METHODS Subjects Recovery of orientation to person, place, and date was studied in 84 patients who were hospitalized on the neurosurgery service after sustaining a closed-head injury (CHI) of varying seventy. The patients had an average age of 24.8 (SD = 6.5) and average education of 11.8 (SO = 1.9) years. Table 1 shows the demographic and neurologic features of the patients according to severity of injury. Fifty-one patients sustained severe head injuries as evidenced by a GCS score of I 8.16 patients sustained moderate head injuries (GCS score between 9 and 12) and 17 patients had mild injuries (i.e., GCS scores in the 13 to 15 range). Eight of the mild injuries were complicated by intracranial lesions visualized by computed tomography (CT), whereas 9 were uncomplicated injuries. These patients had no premorbid history of drug or alcohol abuse, previous neuropsychiatric disorder, or previous head injury. None of the patients suffered from severe aphasic disturbance at the time of testing. Procedure All patients were administered the Galveston Orientation and Amnesia Test (GOAT) (Levin. O’Donnell, & Grossman, 1979), a brief standardized test of orientation, daily
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Table 1. Demographic and Neurological Findings of Closed-Head-Injured Patients Severe CHI ( n = 51; 45 men, 6 women): Age Educ.GCS IC PTA ITIGOAT1 ITIGOAT2 ITIGOAT3 ITIGOAT4 Mean 23.9 11.3 6.1 11.9 36.2 24.7 30.5 40.2 62.1 SD 6.0 2.0 1.3 15.0 25.9 19.6 23.2 28.0 55.8
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Moderate CHI (n = 16; 11 men, 5 women): Age Educ.GCS IC PTA ITIGOATl ITIGOAT2 ITIGOAT3 ITIGOAT4 Mean 24.9 12.3 10.4 4.6 30.0 13.9 19.0 25.9 41.8 SD 8.3 1.3 1.2 10.9 28.1 16.5 18.1 23.2 36.9 Mild CHI with Complications+(n = 8; 7 men, 1 woman): Age Educ.GCS IC PTA ITIGOATl ITIGOAT2 ITIGOAT3 ITIGOAT4 Mean 28.1 13.0 13.9 .19 15.3 3.6 6.1 13.4 17.9 SD 6.2 1.9 .4 .53 9.3 1.1 1.8 5.8 9.8 Mild CHI (n = 9; 8 men, Age Educ.GCS Mean 26.6 12.2 13.9 SD 5.6 1.3 .6
1 woman):
IC .13 .33
PTA ITIGOATl ITIGOAT2 ITIGOAT3 ITIGOAT4 11.9 2.8 5.4 9.9 19.1 10.7 2.3 3.6 5.4 10.9
Total CHI (N = 84) Educ. = Education (years); GCS = Glasgow Coma Scale Score; IC = Impaired Consciousness (days); PTA = Posttraumatic Amnesia (days); ITI = Injury Test Interval (days) +
Complications included intracranial lesions visualized by CT, depressed skull fracture.
from the time they were able to follow verbal commands until their scores were in the normal range for two consecutive days. Patients included in the study were disoriented on their first GOAT examination and were evaluated at least four times during their hospitalization. Patients were considered oriented to person when they were able to correctly identify who they were and their birthday on two consecutive testings. Patients were considered oriented to place when they could correctly identify the name of the city they were in and were cognizant of being in a hospital on two consecutive occasions. If a patient's estimate of the date was within five days of the actual date on two consecutive tests, they were considered to be oriented to time.
RESULTS
Sequence of Recovery of Orientation Figure 1 shows that the dominant ordering of return of orientation was person, place and then time accounting for approximately 70% of the cases. Return of orientation to time preceded the return of orientation to place in 13% of the
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patients. Other orderings of the return of orientation accounted for 11% of the CHI patients, including 7% in which the return of orientation to place or time preceded the return of orientation to person. Ten percent of the patients did not know their name at some point during their recovery. Six percent of the patients were discharged before an ordering could be established. Analysis of subgroups of patients revealed that findings among the severely injured patients closely paralleled those of the entire sample. The moderate and mild injury groups were also similar in that their orientation returned in the order person, place, time in 60 to 70% of the cases and the ordering person, time, place was not systematically related to locus of lesion.
Displacement of Date in Temporal Disorientation When disoriented patients were asked what the date was, they typically gave a date which had occurred earlier than the date of testing. On their initial GOAT, 68% of the patients’ estimates of the date were displaced backwards in time. The discrepancy between the estimated date and the actual date (estimated date minus the actual date) averaged 7.3 years in the past. In contrast, some estimates were placed as much as 10 years in the future. Figure 2, which plots the discrep-
Order of Return of Oriontation Person. Place. Tim. Ezs Penon. Tlme. Placo L?ZJ Other Ordering D Undotomined Ordering
=
All CHI (n=84)
Severe CHI
Moderate CHI
Mild CHI
(n=51)
(n=16)
(n=17)
Fig. 1. Order of Return of Orientation: Overall and by Severity of Head Injury.
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RECOVERY OF ORIENTATION
U
a I
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...*
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-90
.. 0
1
I
I
I
I
1
20
40
60
80
100
120
Days Post Injury Fig. 2,Scatterplot of the Discrepancy between Estimated and Actual Date and Days Post Injury: All Patients (N = 84).
ancy between the patients’ estimates of the date and the actual date versus days postinjury, represents 692 data points from 84 patients. Although most of the estimates of the date tend to be displaced backwards in time, this error was not invariably a reduplication of time. Some patients displaced the date to a time before they were born or to a date in the future. This pattern is observed most clearly among the severely injured and to a lesser extent among the moderately and mildly jured. To better appreciate the shapes of the distributions and to examine the recovery of orientation to time, box-plots of the discrepancy between the estimated and actual dates at four points during recovery are shown in Figure 3. For the purposes of some analysis only four data points were considered. The first data point (Tl) represents the first GOAT given to the patient and T4 represents the last. The two middle data points T2 and T3 were taken at dates equidistant between T1 and T4. In these plots the bottom of the box represents the 25th centime whereas the top of the box marks the 75th centime. The filled circle denotes the median or 50th centime. The “whiskers” of the box were drawn to represent the remaining values to the extremes of the distributions due to the large number of outliers and extreme values. The Y-axis was resealed with respect to Figure 2 to emphasize that the majority of the estimates of the date were displaced backwards in time 5 years or less. The backward displacement of the
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WALTER M.HIGH ET AL.
i 1 1 T2 73 T 4
All CHI (n=84)
T1 12 13 14
11 12 13 T4
Severe
Moderate
CHI
CHI
(n=51)
(n=16)
T1
M T3 14 Mild
CHI (n=17)
Fig. 3.Box-Plot of the Discrepancy between Estimated and Actual Date at Four Points during Recovery: Overall and by Seventy of Head Injury. Vertical lines extend to the most extreme scores in each group.
date and the shrinkage of the discrepancy are most clearly seen among the patients with severe injuries although the trend is still apparent to a lesser degree among the patients who sustained moderate and mild injuries. Another remarkable feature of these box-plots is length of the “whiskers” at both ends of the distribution. At the initial testing, 14 (17%) of the patients gave estimates of the date which were displaced more than 10 years before the actual date. In contrast, 13 (15%)of the patients gave estimates of the date which were 2 months or more into the future. To test the hypothesis that the patients’ estimates of the date were displaced backwards in time and that the discrepancies between their estimates and the actual date “shrank” as the patients became more oriented, a nonparametric approach was utilized. For each subject the discrepancies across the four time penods were ranked such that the estimate which was furthest in the past was ranked number one and the estimate which was closest to the date of testing was ranked number 4. The ordering of the median ranks was evaluated by Page’s test (Hettmansperger, 1984), a nonparametric statistic which tested the hypothesis that at least one successive median was greater than a previous median and that
709
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the medians were ordered. This statistic is distributed as a Z and was calculated to be 3.95, p < .OOOl.Bonferroni corrected post hoc comparisons indicated that the median rank on the fourth occasion was significantly different from the median rank on the first ( Z = 3.68, p < .OO01) and second (Z = 2.90, p < 0.002) occasions. This pattern of performance was confirmed for severe and moderate injuries, but not for mild injuries. The relationship between the patient’s age and the discrepancy between estimates of the date and the actual date is shown in Figure 4. A Spearman Rank Order Correlation coefficient was significant (rho = -.20, p < .03,one-tailed test), indicating that the older the patient was at the time of injury, the more the patient’s estimate of the date was likely to be displaced backwards in time. Age was also related to the duration of impaired consciousness, rho = -.22, p < .05. To investigate whether there were any systematic differences related to exhibiting backward displacement in temporal orientation, patients whose backward displacement was greater than the median displacement at T1 (34 days) were compared to patients with backward displacements less than the median or patients whose estimates were displaced into the future. Figure 5 shows a comparison of the two groups of patients on demographic and neurological variables. Analysis of variance applied to the ranked variables indicated that patients ex-
-0
0
0)-
-30
m o
10
20
30
40
50
Age (years) Fig. 4.Scatterplot of the Discrepancy between Estimated and Actual Date and Age at Injury: All Patients (N = 84).
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hibiting the greatest backward displacement of the date were significantly older than patients who did not show unequivocal backward displacement, F (1,82)= 7.85,p < 0.007. The median education of the groups did not differ. The group showing the greater backward displacement of the date was more severely injured as indicated by their GCS scores (F (1,82)= 5.53, p < .03), duration of impaired consciousness (F (1$2) = 6.47, p c .02),and duration of PTA (F (1 $2) = 15.1 1,p < .0002).A trend for a greater percentage of patients with focal mass lesions in the group which showed greater backward displacement fell short of significance (Fisher's Exact Test, p c .06). To evaluate the effects of lateralized focal mass lesions on the backward displacement of patients' estimates of the date and on the duration of PTA, 11 patients with lesions restricted to the left hemisphere were compared to 13 patients with lesions confined to the right hemisphere and 25 patients who had sustained diffuse injuries. These three groups of patients did not differ with respect to age, education, lowest GCS score, or duration of impaired consciousness. Despite a tendency toward greater backward displacement of date at T1 in
16
30
15
10
25
8
20
10
n
%-6
@
v)
m15 4
5
0
-
1'1I
0
U
5 4
0
>.
-0
0 c3
10
Y)
0
2 L
-
CHI with date discrepancies below the median n-42
0CHI with date discrepancies
above the median {n=42{
Fig. 5. Comparison of Patients Who Displace the Date Backward in Time vs Those Who DO Not: All Patients.
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the patients with left focal lesions (median - 86 days vs. 38 days in patients with right hemisphere focal lesions and 14 days in patients with diffuse CHI), no lateralized effects were found for the duration of PTA, the extent of the backward displacement of the date or duration of disorientation to place. The contribution of frontal and temporal lobe lesions to impaired consciousness and erroneous placement of the date was also evaluated. Table 2 shows 41 CHI patients who were classified according to whether focal injuries were radiologically visualized in the frontal, temporal, or fronto-temporal regions. These patients were compared to 11 patients with focal mass lesions which did not extend into the frontal or temporal regions and 32 patients who had no lesions visualized on CT. Analysis of variance on the ranked variables revealed no differences across the five groups in age, education, or lowest GCS score. Significant differences were found, however, for impaired consciousness (F (4,79) = 3.14, p < .02) and duration of PTA (F (4,79) = 3.1 1, p c .02). Post-hoc analyses revealed that the group with frontal lesions had longer duration of impaired consciousness and PTA than the group with lesions sparing the frontal or temporal areas and the group with no visualized mass lesions (p < .05). Although the discrepancy between the estimated and actual date did not significantly differ overall across the localization groups (F (4,79) = 1.94, p = .ll), the backward
Table 2. Comparison of CHI Patients with Frontal, Temporal, Fronto-temporal or OtherFocal Mass Lesions and Patients with Diffuse Injuries Frontal Focal Injuries
Temporal Focal Injuries ( n = 8) ( n =20) Med. IQR Med. IQR 28.0 9.0 Age Education(yrs) 12.0 2.5 GCS score 7 2.5 Impaired Consciousness 5.0'*b 10.5 (days) PTA (days) 31Cod 27.5 Discrepancy
21.2 12.0 9.5
5.0 2.0 6
2.0 22.8 20 28.5
Frontotemporal Focal Injuries
Other Focal Injuries
Mild and Diffuse Injuries
( n = 13)
(n = 11) Med. IQR
Med. IQR
Med.
IQR
27.8 11.1 11.0 3.0 7 5
24.1 12.0 8
3.7 19.0 33 25
1.0' 14'
( n = 32)
6.1 23.8 4 . 0 12.0 7 8
8.5 1.8 6
3.0 l.Ob 4.4 13 19Sd 27
in Date
(days)
-68
4358
-7"
50
-309'" 4324 -120
12572
Medians which share superscripts are significantly different (p < .05). Med. = median; IQR = interquartile range; GCS = Glasgow Coma Scale; PTA = duration of posttraumatic amnesia; Discrepancy in date = (date of test - estimated date)
-15,5'361
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displacement of estimates by fronto-temporal patients exceeded that of the temporal lobe lesion patients and the diffuse group (p c 0.05).
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DISCUSSION
For 70% of the disoriented CHI patients studied, the return of orientation to person preceded or coincided with the return of orientation to place, which occurred before or concurrent with the return of orientation to time. An unexpected finding was that 13% of the patients were able to give an estimate of the date which was within 5 days of the actual date on consecutive testings before they were able to reliably answer questions concerning geographic location. While the data are consistent with the clinical impression that orientation to person is less vulnerable to disruption than orientation to place, which is less vulnerable than orientation to time, the order of return was not invariant. The sequential return of orientation to person, place, and time may be explained by the patients’ongoing retrograde and anterograde memory difficulties. Orientation to person is less vulnerable to disruption than orientation to place and time because it requires access to older, overlearned information. Previous research (Levin et al., 1985) has shown that early autobiographical information is relatively well preserved following CHI even during PTA. These data support Ribot’s (1885) hypothesis that older memories are relatively resistant to cerebral insult. Orientation to place and time may be more vulnerable to disruption than orientation to person because of the greater dependence on retention of new information which is severely impaired in patients during the initial stage of recovery from CHI. Geographic information remains invariant during the hospitalization (apart from transfers), whereas the date changes daily. Accordingly, rehearsal of place is more frequent than rehearsal of a particular date. The differential rehearsal of place and time is mitigated somewhat by the requirement that the time estimate need only be within five days of the correct date. This criterion was used based on the work of Natelson. Haupt, Fleischer, and Grey (1979) which showed that it was not uncommon for normal individuals to err as much as five days from the actual date. The generous leeway of this criterion accounts for, at least in part, the large number of reversals in the return of orientation to place and time. The present findings confirm the hypothesis that disoriented patients typically estimate the date to be earlier than the actual date. Nearly 70% of the patients initially gave estimates of the date which preceded the actual date. As the patients became more oriented over time, the discrepancy between the estimated and actual date “shrank”. These results may be explained, in part, by retrograde memory loss and the greater vulnerability of recently acquired memories to disruption as compared to older memories. When a disoriented patient is asked the date, memories for recent dates before the injury are unavailable for
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retrieval. In addition, information concerning the current date supplied by family and hospital personnel is rapidly forgotten (Levin, High, & Eisenberg, 1988). The patient therefore retrieves a date which precedes the period for which they are amnesic. As the patient becomes more oriented, the RA “ s h r i n k s ” and dates closer in time to the actual date become available for retrieval. Our temporal orientation data extend a previous study (Levin et a].. 1985) of impaired remote memory following CHI which disclosed relative preservation of older autobiographic memories as compared to more recently acquired memories. These findings, combined with the data for relative preservation of memory for information concerning person, support Ribot’s postulation that older memories are less vulnerable to disruption than more recent memories. Rehearsal and overlearning may strengthen memories over time making them less vulnerable. Unlike our previous findings (Levin et al., 1985), however, the current data cannot be completely explained by rehearsal and overlearning. For example, there is no reason to suppose that dates from 1983 were more rehearsed than dates from 1987. Despite the greater opportunity for normal decay, dates from 1983 appear to be more available than dates from 1987. It should also be noted that retrograde memory loss as indexed by the discrepancy between the patient’s estimate of the date and the actual date is not vulnerable to confounding by item difficulty as are remote memory questionnaires for public events or famous faces (Albert, Butters, & Levin, 1979). In studies using these questionnaire techniques it is unclear if the apparent preservation of older memories was due to their relative resilience or due to the variation in the difficulty of items chosen for the earlier time periods (Sanders & Warrington, 1971). The present findings, along with the recent investigation of patients undergoing ECT (Daniel et al., 1987) offer important confirmation of Ribot’s counterintuitive clinical observations. These data require explanation as well as incorporation into current models of memory. Patients who showed the pattern of misplacing the date backward in time were older, more severely injured, and were more likely to have sustained focal mass lesions as compared to patients who did not show this pattern. No differences in age, GCS score, duration of impaired consciousness, PTA, or discrepancy in the date were noted for patients with right- versus left-hemisphere mass lesions. Contrary to expectations, patients with frontal lesions had longer durations of impaired consciousness and PTA than patients with lesions outside of the fronto-temporal region or diffuse injuries. This finding suggests the possibility that deficiencies in temporal judgement may contribute to disorientation. Patients with temporal lobe imvolvement did not differ in orientation scores from patients with other focal lesions or patients with diffuse injuries. Although the explanation for this finding is unclear, there were only eight patients in the temporal lobe group including two patients in whom the lesions were visualized on MRI but not CT. The small number of cases and the possibility of undetected temporal lobe lesions in the other groups (Levin et al., 1987) may have mitigated against the effects of lesions in this region.
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CONCLUSIONS
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These results extend the findings of Russell and Nathan (1946) of “shrinking” RA in CHI patients studied prospectively. Our findings indicate that the discrepancy between the patients’ estimates of the date as compared to the actual date is a measure of retrograde memory loss. In addition, the findings confirm in a quantified and systematic way the clinical impression that disoriented patients tend to misplace the date backwards in time and that restitution of orientation generally proceeds in the order of person, place, and then finally time. REFERENCES Albert, M.S.. Butters, N.. & Levin, J. (1979). Temporal gradients in the retrograde amnesia of patients with alcoholic Korsakoff‘s disease. Archives of Neurology, 36, 211216. Benson, D.F., & Geschwind, N. (1967). Shrinking retrograde amnesia. Journal of Neurology, Neurosurgery, and Psychiatry, 30, 539-544. Daniel, W.F., Crovitz, H.F., & Weiner. R.D. (1987). Neuropsychological aspects of disorientation. Cortex, 23, 169-187. Hettmansperger, T.P. (1984). Statistical inference basedon r a h . New York: John Wiley. Levin, H.S., Amparo. E.. Eisenberg. H.M.. Williams, D.H., High, Jr.. W.M., McArdle, C.B., & Weiner. R.L. (1987). Magnetic resonance imaging and computed tomography in relation to the neurobehavioral sequelae of mild and moderate head injures. Journal of Neurosurgery, 66, 706-7 13. Levin. H.S., High, Jr., W.M., & Eisenberg, H.M. (1988). Learning and forgetting during posttraumatic amnesia in head injured patients. Journal of Neurology, Neurosurgery, and Psychiatry, 51, 14-20. Levin. H.S., High, W.M., Meyers, C.A., Von Laufen. A., Hayden, M.E., & Eisenberg. H.M. (1985). Impairment of remote memory after closed head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 48.556-563. Levin, H.S.,O’Donnell, V.M., & Grossman, R.G. (1979). The Galveston orientation and amnesia test: A practical scale to assess cognition after head injury. Journal of Nervous and Mental Disorders, 169, 675-684. Levin, H.S., Peters, B.H., & Hulkonen, D.A. (1983). Early concepts of anterograde and retrograde amnesia. Cortex, 19, 427-440. Natelson, B.H.,Haupt, E.J., Fleischer, L.G., & Grey (1979). Temporal orientation and education: A direct relationship in normal people. Archives of Neurology, 36, 444446. Ribot, T. (1885). Diseuses of memory. London: Kegan Paul, Trench & Co. Russell, W.R. (1932). Cerebral involvement in head injury. Brain, 55,549-603. Russell, W.R. (1935). Amnesia following head injuries. Lancet, 2, 762-763. Russell. W.R. (1971). The traumatic amnesias. New York: Oxford University Press. Russell, W.R., & Nathan, P.W. (1946). Traumatic amnesia. Brain, 69, 183-187. Russell. W.R.. & Smith, A. (1961). Post-traumatic amnesia. Archives of Neurology, 5 , 4-17. Sanders, H.I.. & Warrington, E.K.(1971). Memory for remote events in amnesiacs patients. Brain, 94,661-668.
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Recovery of orientation following closed-head injury a
b
Walter M. High Jr. , Harvey S. Levin & Howard E. Gary Jr.
c
a
Department of Neuropsychology , The Del Oro Institute for Rehabilitation , Houston, TX b
Division of Neurosurgery , University of Texas Medical Branch , Galveston, TX c
Center for Disease Control , Atlanta, GA Published online: 04 Jan 2008.
To cite this article: Walter M. High Jr. , Harvey S. Levin & Howard E. Gary Jr. (1990) Recovery of orientation following closed-head injury, Journal of Clinical and Experimental Neuropsychology, 12:5, 703-714, DOI: 10.1080/01688639008401013 To link to this article: http://dx.doi.org/10.1080/01688639008401013
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0168-8634~/1205-0703%3.00 0 Swets & Zeitlinger
H 1990, VOI. 12, NO. 5 , pp. 703-714
Recovery of Orientation Following Closed-Head Injury”
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Walter M. High, Jr.’, Harvey S. Levin2, and Howard E. Gary, Jr? Department of Neuropsychology, The Del Oro Institute for Rehabilitation, Houston, TX Division of Neurosurgery, University of Texas Medical Branch, Galveston, TX Center for Disease Control, Atlanta, GA.
ABSTRACT The pattern of recovery of orientation to person, place, and time was investigated in 84 patients who were initially disoriented while hospitalized on the neurosurgery service after sustaining a closed-head injury (CHI) of varying seventy. Results of daily administration of the Galveston Orientation and Amnesia Test revealed that the most common sequence of recovery of orientation was person, place, and time, accounting for about 70% of the patients. Return of orientation to time preceded reorientation to place in 13% of the patients while other orderings of reorientation were present in 11% of the cases. Temporal disorientation was initially characterized by backward displacement of the date from the actual date in 68% of the patients. The magnitude of this displacement progressively shrank as the patients became more oriented. Patients who exhibited the greatest backward displacement of the date had more severe and persistent impaired consciousness, were older and had longer durations of posttraumatic amnesia. These data support Ribot’s hypothesis that older memories are relatively resistant to cerebral insult.
INTRODUCTION Patients sustaining closed-head injuries often have difficulty recalling events which occurred before their injury. Russell (1932) observed that t h e loss o f previously acquired memories was partially reversible. This retrograde deficit, which can initially extend f o r months or years, typically “shrinks” to a brief interval (less than 30 minutes) as the patient’s confusion clears (Benson &
* This research was supported by grant NS-21889, Javits Neuroscience Investigator Award to the second author. We are indebted to Liz Zindler for manuscript preparation and Lori A. Baxter for assistance in data analysis. We also thank Dr. Felicia Goldstein for her review of an earlier version of the manuscript. Portions of this manuscript were part of the first author’s doctoral dissertation and were presented at the Seventeenth Annual Meeting of the International Neuropsychological Society, Vancouver, 1989. Address reprint requests to: Harvey S.Levin, Ph.D., Division of Neurosurgery D-73, The University of Texas Medical Branch, Galveston, Texas 77550, USA. Accepted for publication: November 17, 1989.
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Geschwind, 1967; Russell, 1935; Russell & Nathan, 1946). The observations of Russell and his co-workers (Russell, 1932, 1935, 1971; Russell & Nathan, 1946; Russell & Smith, 1961) were extended by Levin et al. (1985) who found that recently acquired autobiographical infomation was more vulnerable to disruption by head injury than older autobiographical material. The pattern of retrograde memory loss has been examined in other clinical populations. Daniel, Crovitz, and Weiner (1987) studied the recovery of orientation to person, place, and time in patients undergoing a course of electroconvulsive therapy (ECT) for depression. These investigators confirmed that orientation to person returned first, followed by orientation to place, and then orientation to time. The pattern of retrograde memory loss after ECT was reflected by the patients’ estimates of their age and current date which were displaced backwards in time, suggesting an inability to access more recently acquired information. Consistent with Ribot’s law (see Levin, Peters, & Wulkonen, 1983 for a historical review) of older memories being more impervious to cerebral insult than more recently acquired memories, the discrepancy progressively “shrank” between the patients’ estimate of their age and the date as compared to their true age and the true date. The study of Daniel et al. (1987) raised the issue of whether a similar pattern of resolution of retrograde amnesia (RA) is present after head injury. We have serially investigated the recovery of orientation to person, place, and time in head injured patients. The recovery pattern of retrograde memory loss was indexed by the relationship between the patients’ estimates of the current date and resolution of anterograde amnesia. Second, the effect of subject variables such as age, severity of injury, and focal pathology on recovery of RA and posttraumatic amnesia (PTA) was examined to elucidate possible underlying mechanisms. METHODS Subjects Recovery of orientation to person, place, and date was studied in 84 patients who were hospitalized on the neurosurgery service after sustaining a closed-head injury (CHI) of varying seventy. The patients had an average age of 24.8 (SD = 6.5) and average education of 11.8 (SO = 1.9) years. Table 1 shows the demographic and neurologic features of the patients according to severity of injury. Fifty-one patients sustained severe head injuries as evidenced by a GCS score of I 8.16 patients sustained moderate head injuries (GCS score between 9 and 12) and 17 patients had mild injuries (i.e., GCS scores in the 13 to 15 range). Eight of the mild injuries were complicated by intracranial lesions visualized by computed tomography (CT), whereas 9 were uncomplicated injuries. These patients had no premorbid history of drug or alcohol abuse, previous neuropsychiatric disorder, or previous head injury. None of the patients suffered from severe aphasic disturbance at the time of testing. Procedure All patients were administered the Galveston Orientation and Amnesia Test (GOAT) (Levin. O’Donnell, & Grossman, 1979), a brief standardized test of orientation, daily
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Table 1. Demographic and Neurological Findings of Closed-Head-Injured Patients Severe CHI ( n = 51; 45 men, 6 women): Age Educ.GCS IC PTA ITIGOAT1 ITIGOAT2 ITIGOAT3 ITIGOAT4 Mean 23.9 11.3 6.1 11.9 36.2 24.7 30.5 40.2 62.1 SD 6.0 2.0 1.3 15.0 25.9 19.6 23.2 28.0 55.8
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Moderate CHI (n = 16; 11 men, 5 women): Age Educ.GCS IC PTA ITIGOATl ITIGOAT2 ITIGOAT3 ITIGOAT4 Mean 24.9 12.3 10.4 4.6 30.0 13.9 19.0 25.9 41.8 SD 8.3 1.3 1.2 10.9 28.1 16.5 18.1 23.2 36.9 Mild CHI with Complications+(n = 8; 7 men, 1 woman): Age Educ.GCS IC PTA ITIGOATl ITIGOAT2 ITIGOAT3 ITIGOAT4 Mean 28.1 13.0 13.9 .19 15.3 3.6 6.1 13.4 17.9 SD 6.2 1.9 .4 .53 9.3 1.1 1.8 5.8 9.8 Mild CHI (n = 9; 8 men, Age Educ.GCS Mean 26.6 12.2 13.9 SD 5.6 1.3 .6
1 woman):
IC .13 .33
PTA ITIGOATl ITIGOAT2 ITIGOAT3 ITIGOAT4 11.9 2.8 5.4 9.9 19.1 10.7 2.3 3.6 5.4 10.9
Total CHI (N = 84) Educ. = Education (years); GCS = Glasgow Coma Scale Score; IC = Impaired Consciousness (days); PTA = Posttraumatic Amnesia (days); ITI = Injury Test Interval (days) +
Complications included intracranial lesions visualized by CT, depressed skull fracture.
from the time they were able to follow verbal commands until their scores were in the normal range for two consecutive days. Patients included in the study were disoriented on their first GOAT examination and were evaluated at least four times during their hospitalization. Patients were considered oriented to person when they were able to correctly identify who they were and their birthday on two consecutive testings. Patients were considered oriented to place when they could correctly identify the name of the city they were in and were cognizant of being in a hospital on two consecutive occasions. If a patient's estimate of the date was within five days of the actual date on two consecutive tests, they were considered to be oriented to time.
RESULTS
Sequence of Recovery of Orientation Figure 1 shows that the dominant ordering of return of orientation was person, place and then time accounting for approximately 70% of the cases. Return of orientation to time preceded the return of orientation to place in 13% of the
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patients. Other orderings of the return of orientation accounted for 11% of the CHI patients, including 7% in which the return of orientation to place or time preceded the return of orientation to person. Ten percent of the patients did not know their name at some point during their recovery. Six percent of the patients were discharged before an ordering could be established. Analysis of subgroups of patients revealed that findings among the severely injured patients closely paralleled those of the entire sample. The moderate and mild injury groups were also similar in that their orientation returned in the order person, place, time in 60 to 70% of the cases and the ordering person, time, place was not systematically related to locus of lesion.
Displacement of Date in Temporal Disorientation When disoriented patients were asked what the date was, they typically gave a date which had occurred earlier than the date of testing. On their initial GOAT, 68% of the patients’ estimates of the date were displaced backwards in time. The discrepancy between the estimated date and the actual date (estimated date minus the actual date) averaged 7.3 years in the past. In contrast, some estimates were placed as much as 10 years in the future. Figure 2, which plots the discrep-
Order of Return of Oriontation Person. Place. Tim. Ezs Penon. Tlme. Placo L?ZJ Other Ordering D Undotomined Ordering
=
All CHI (n=84)
Severe CHI
Moderate CHI
Mild CHI
(n=51)
(n=16)
(n=17)
Fig. 1. Order of Return of Orientation: Overall and by Severity of Head Injury.
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Days Post Injury Fig. 2,Scatterplot of the Discrepancy between Estimated and Actual Date and Days Post Injury: All Patients (N = 84).
ancy between the patients’ estimates of the date and the actual date versus days postinjury, represents 692 data points from 84 patients. Although most of the estimates of the date tend to be displaced backwards in time, this error was not invariably a reduplication of time. Some patients displaced the date to a time before they were born or to a date in the future. This pattern is observed most clearly among the severely injured and to a lesser extent among the moderately and mildly jured. To better appreciate the shapes of the distributions and to examine the recovery of orientation to time, box-plots of the discrepancy between the estimated and actual dates at four points during recovery are shown in Figure 3. For the purposes of some analysis only four data points were considered. The first data point (Tl) represents the first GOAT given to the patient and T4 represents the last. The two middle data points T2 and T3 were taken at dates equidistant between T1 and T4. In these plots the bottom of the box represents the 25th centime whereas the top of the box marks the 75th centime. The filled circle denotes the median or 50th centime. The “whiskers” of the box were drawn to represent the remaining values to the extremes of the distributions due to the large number of outliers and extreme values. The Y-axis was resealed with respect to Figure 2 to emphasize that the majority of the estimates of the date were displaced backwards in time 5 years or less. The backward displacement of the
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i 1 1 T2 73 T 4
All CHI (n=84)
T1 12 13 14
11 12 13 T4
Severe
Moderate
CHI
CHI
(n=51)
(n=16)
T1
M T3 14 Mild
CHI (n=17)
Fig. 3.Box-Plot of the Discrepancy between Estimated and Actual Date at Four Points during Recovery: Overall and by Seventy of Head Injury. Vertical lines extend to the most extreme scores in each group.
date and the shrinkage of the discrepancy are most clearly seen among the patients with severe injuries although the trend is still apparent to a lesser degree among the patients who sustained moderate and mild injuries. Another remarkable feature of these box-plots is length of the “whiskers” at both ends of the distribution. At the initial testing, 14 (17%) of the patients gave estimates of the date which were displaced more than 10 years before the actual date. In contrast, 13 (15%)of the patients gave estimates of the date which were 2 months or more into the future. To test the hypothesis that the patients’ estimates of the date were displaced backwards in time and that the discrepancies between their estimates and the actual date “shrank” as the patients became more oriented, a nonparametric approach was utilized. For each subject the discrepancies across the four time penods were ranked such that the estimate which was furthest in the past was ranked number one and the estimate which was closest to the date of testing was ranked number 4. The ordering of the median ranks was evaluated by Page’s test (Hettmansperger, 1984), a nonparametric statistic which tested the hypothesis that at least one successive median was greater than a previous median and that
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the medians were ordered. This statistic is distributed as a Z and was calculated to be 3.95, p < .OOOl.Bonferroni corrected post hoc comparisons indicated that the median rank on the fourth occasion was significantly different from the median rank on the first ( Z = 3.68, p < .OO01) and second (Z = 2.90, p < 0.002) occasions. This pattern of performance was confirmed for severe and moderate injuries, but not for mild injuries. The relationship between the patient’s age and the discrepancy between estimates of the date and the actual date is shown in Figure 4. A Spearman Rank Order Correlation coefficient was significant (rho = -.20, p < .03,one-tailed test), indicating that the older the patient was at the time of injury, the more the patient’s estimate of the date was likely to be displaced backwards in time. Age was also related to the duration of impaired consciousness, rho = -.22, p < .05. To investigate whether there were any systematic differences related to exhibiting backward displacement in temporal orientation, patients whose backward displacement was greater than the median displacement at T1 (34 days) were compared to patients with backward displacements less than the median or patients whose estimates were displaced into the future. Figure 5 shows a comparison of the two groups of patients on demographic and neurological variables. Analysis of variance applied to the ranked variables indicated that patients ex-
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Age (years) Fig. 4.Scatterplot of the Discrepancy between Estimated and Actual Date and Age at Injury: All Patients (N = 84).
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hibiting the greatest backward displacement of the date were significantly older than patients who did not show unequivocal backward displacement, F (1,82)= 7.85,p < 0.007. The median education of the groups did not differ. The group showing the greater backward displacement of the date was more severely injured as indicated by their GCS scores (F (1,82)= 5.53, p < .03), duration of impaired consciousness (F (1$2) = 6.47, p c .02),and duration of PTA (F (1 $2) = 15.1 1,p < .0002).A trend for a greater percentage of patients with focal mass lesions in the group which showed greater backward displacement fell short of significance (Fisher's Exact Test, p c .06). To evaluate the effects of lateralized focal mass lesions on the backward displacement of patients' estimates of the date and on the duration of PTA, 11 patients with lesions restricted to the left hemisphere were compared to 13 patients with lesions confined to the right hemisphere and 25 patients who had sustained diffuse injuries. These three groups of patients did not differ with respect to age, education, lowest GCS score, or duration of impaired consciousness. Despite a tendency toward greater backward displacement of date at T1 in
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CHI with date discrepancies below the median n-42
0CHI with date discrepancies
above the median {n=42{
Fig. 5. Comparison of Patients Who Displace the Date Backward in Time vs Those Who DO Not: All Patients.
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the patients with left focal lesions (median - 86 days vs. 38 days in patients with right hemisphere focal lesions and 14 days in patients with diffuse CHI), no lateralized effects were found for the duration of PTA, the extent of the backward displacement of the date or duration of disorientation to place. The contribution of frontal and temporal lobe lesions to impaired consciousness and erroneous placement of the date was also evaluated. Table 2 shows 41 CHI patients who were classified according to whether focal injuries were radiologically visualized in the frontal, temporal, or fronto-temporal regions. These patients were compared to 11 patients with focal mass lesions which did not extend into the frontal or temporal regions and 32 patients who had no lesions visualized on CT. Analysis of variance on the ranked variables revealed no differences across the five groups in age, education, or lowest GCS score. Significant differences were found, however, for impaired consciousness (F (4,79) = 3.14, p < .02) and duration of PTA (F (4,79) = 3.1 1, p c .02). Post-hoc analyses revealed that the group with frontal lesions had longer duration of impaired consciousness and PTA than the group with lesions sparing the frontal or temporal areas and the group with no visualized mass lesions (p < .05). Although the discrepancy between the estimated and actual date did not significantly differ overall across the localization groups (F (4,79) = 1.94, p = .ll), the backward
Table 2. Comparison of CHI Patients with Frontal, Temporal, Fronto-temporal or OtherFocal Mass Lesions and Patients with Diffuse Injuries Frontal Focal Injuries
Temporal Focal Injuries ( n = 8) ( n =20) Med. IQR Med. IQR 28.0 9.0 Age Education(yrs) 12.0 2.5 GCS score 7 2.5 Impaired Consciousness 5.0'*b 10.5 (days) PTA (days) 31Cod 27.5 Discrepancy
21.2 12.0 9.5
5.0 2.0 6
2.0 22.8 20 28.5
Frontotemporal Focal Injuries
Other Focal Injuries
Mild and Diffuse Injuries
( n = 13)
(n = 11) Med. IQR
Med. IQR
Med.
IQR
27.8 11.1 11.0 3.0 7 5
24.1 12.0 8
3.7 19.0 33 25
1.0' 14'
( n = 32)
6.1 23.8 4 . 0 12.0 7 8
8.5 1.8 6
3.0 l.Ob 4.4 13 19Sd 27
in Date
(days)
-68
4358
-7"
50
-309'" 4324 -120
12572
Medians which share superscripts are significantly different (p < .05). Med. = median; IQR = interquartile range; GCS = Glasgow Coma Scale; PTA = duration of posttraumatic amnesia; Discrepancy in date = (date of test - estimated date)
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displacement of estimates by fronto-temporal patients exceeded that of the temporal lobe lesion patients and the diffuse group (p c 0.05).
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DISCUSSION
For 70% of the disoriented CHI patients studied, the return of orientation to person preceded or coincided with the return of orientation to place, which occurred before or concurrent with the return of orientation to time. An unexpected finding was that 13% of the patients were able to give an estimate of the date which was within 5 days of the actual date on consecutive testings before they were able to reliably answer questions concerning geographic location. While the data are consistent with the clinical impression that orientation to person is less vulnerable to disruption than orientation to place, which is less vulnerable than orientation to time, the order of return was not invariant. The sequential return of orientation to person, place, and time may be explained by the patients’ongoing retrograde and anterograde memory difficulties. Orientation to person is less vulnerable to disruption than orientation to place and time because it requires access to older, overlearned information. Previous research (Levin et al., 1985) has shown that early autobiographical information is relatively well preserved following CHI even during PTA. These data support Ribot’s (1885) hypothesis that older memories are relatively resistant to cerebral insult. Orientation to place and time may be more vulnerable to disruption than orientation to person because of the greater dependence on retention of new information which is severely impaired in patients during the initial stage of recovery from CHI. Geographic information remains invariant during the hospitalization (apart from transfers), whereas the date changes daily. Accordingly, rehearsal of place is more frequent than rehearsal of a particular date. The differential rehearsal of place and time is mitigated somewhat by the requirement that the time estimate need only be within five days of the correct date. This criterion was used based on the work of Natelson. Haupt, Fleischer, and Grey (1979) which showed that it was not uncommon for normal individuals to err as much as five days from the actual date. The generous leeway of this criterion accounts for, at least in part, the large number of reversals in the return of orientation to place and time. The present findings confirm the hypothesis that disoriented patients typically estimate the date to be earlier than the actual date. Nearly 70% of the patients initially gave estimates of the date which preceded the actual date. As the patients became more oriented over time, the discrepancy between the estimated and actual date “shrank”. These results may be explained, in part, by retrograde memory loss and the greater vulnerability of recently acquired memories to disruption as compared to older memories. When a disoriented patient is asked the date, memories for recent dates before the injury are unavailable for
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retrieval. In addition, information concerning the current date supplied by family and hospital personnel is rapidly forgotten (Levin, High, & Eisenberg, 1988). The patient therefore retrieves a date which precedes the period for which they are amnesic. As the patient becomes more oriented, the RA “ s h r i n k s ” and dates closer in time to the actual date become available for retrieval. Our temporal orientation data extend a previous study (Levin et a].. 1985) of impaired remote memory following CHI which disclosed relative preservation of older autobiographic memories as compared to more recently acquired memories. These findings, combined with the data for relative preservation of memory for information concerning person, support Ribot’s postulation that older memories are less vulnerable to disruption than more recent memories. Rehearsal and overlearning may strengthen memories over time making them less vulnerable. Unlike our previous findings (Levin et al., 1985), however, the current data cannot be completely explained by rehearsal and overlearning. For example, there is no reason to suppose that dates from 1983 were more rehearsed than dates from 1987. Despite the greater opportunity for normal decay, dates from 1983 appear to be more available than dates from 1987. It should also be noted that retrograde memory loss as indexed by the discrepancy between the patient’s estimate of the date and the actual date is not vulnerable to confounding by item difficulty as are remote memory questionnaires for public events or famous faces (Albert, Butters, & Levin, 1979). In studies using these questionnaire techniques it is unclear if the apparent preservation of older memories was due to their relative resilience or due to the variation in the difficulty of items chosen for the earlier time periods (Sanders & Warrington, 1971). The present findings, along with the recent investigation of patients undergoing ECT (Daniel et al., 1987) offer important confirmation of Ribot’s counterintuitive clinical observations. These data require explanation as well as incorporation into current models of memory. Patients who showed the pattern of misplacing the date backward in time were older, more severely injured, and were more likely to have sustained focal mass lesions as compared to patients who did not show this pattern. No differences in age, GCS score, duration of impaired consciousness, PTA, or discrepancy in the date were noted for patients with right- versus left-hemisphere mass lesions. Contrary to expectations, patients with frontal lesions had longer durations of impaired consciousness and PTA than patients with lesions outside of the fronto-temporal region or diffuse injuries. This finding suggests the possibility that deficiencies in temporal judgement may contribute to disorientation. Patients with temporal lobe imvolvement did not differ in orientation scores from patients with other focal lesions or patients with diffuse injuries. Although the explanation for this finding is unclear, there were only eight patients in the temporal lobe group including two patients in whom the lesions were visualized on MRI but not CT. The small number of cases and the possibility of undetected temporal lobe lesions in the other groups (Levin et al., 1987) may have mitigated against the effects of lesions in this region.
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CONCLUSIONS
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These results extend the findings of Russell and Nathan (1946) of “shrinking” RA in CHI patients studied prospectively. Our findings indicate that the discrepancy between the patients’ estimates of the date as compared to the actual date is a measure of retrograde memory loss. In addition, the findings confirm in a quantified and systematic way the clinical impression that disoriented patients tend to misplace the date backwards in time and that restitution of orientation generally proceeds in the order of person, place, and then finally time. REFERENCES Albert, M.S.. Butters, N.. & Levin, J. (1979). Temporal gradients in the retrograde amnesia of patients with alcoholic Korsakoff‘s disease. Archives of Neurology, 36, 211216. Benson, D.F., & Geschwind, N. (1967). Shrinking retrograde amnesia. Journal of Neurology, Neurosurgery, and Psychiatry, 30, 539-544. Daniel, W.F., Crovitz, H.F., & Weiner. R.D. (1987). Neuropsychological aspects of disorientation. Cortex, 23, 169-187. Hettmansperger, T.P. (1984). Statistical inference basedon r a h . New York: John Wiley. Levin, H.S., Amparo. E.. Eisenberg. H.M.. Williams, D.H., High, Jr.. W.M., McArdle, C.B., & Weiner. R.L. (1987). Magnetic resonance imaging and computed tomography in relation to the neurobehavioral sequelae of mild and moderate head injures. Journal of Neurosurgery, 66, 706-7 13. Levin. H.S., High, Jr., W.M., & Eisenberg, H.M. (1988). Learning and forgetting during posttraumatic amnesia in head injured patients. Journal of Neurology, Neurosurgery, and Psychiatry, 51, 14-20. Levin. H.S., High, W.M., Meyers, C.A., Von Laufen. A., Hayden, M.E., & Eisenberg. H.M. (1985). Impairment of remote memory after closed head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 48.556-563. Levin, H.S.,O’Donnell, V.M., & Grossman, R.G. (1979). The Galveston orientation and amnesia test: A practical scale to assess cognition after head injury. Journal of Nervous and Mental Disorders, 169, 675-684. Levin, H.S., Peters, B.H., & Hulkonen, D.A. (1983). Early concepts of anterograde and retrograde amnesia. Cortex, 19, 427-440. Natelson, B.H.,Haupt, E.J., Fleischer, L.G., & Grey (1979). Temporal orientation and education: A direct relationship in normal people. Archives of Neurology, 36, 444446. Ribot, T. (1885). Diseuses of memory. London: Kegan Paul, Trench & Co. Russell, W.R. (1932). Cerebral involvement in head injury. Brain, 55,549-603. Russell, W.R. (1935). Amnesia following head injuries. Lancet, 2, 762-763. Russell. W.R. (1971). The traumatic amnesias. New York: Oxford University Press. Russell, W.R., & Nathan, P.W. (1946). Traumatic amnesia. Brain, 69, 183-187. Russell. W.R.. & Smith, A. (1961). Post-traumatic amnesia. Archives of Neurology, 5 , 4-17. Sanders, H.I.. & Warrington, E.K.(1971). Memory for remote events in amnesiacs patients. Brain, 94,661-668.
