Journal of Neurology, Neurosurgery, and Psychiatry 1997;62:163-168 163 Diencephalic temporal order amnesia J Department of Neurology, University of Cincinnati, Ohio, USA J E Shuren Tufts University School of Medicine, Boston, Massachusetts, USA D H Jacobs Center for Neuropsychological Studies, the Department of Neurology, University of Florida and Veterans Administration Medical Center, Gainesville, Florida, USA J E Shuren D H Jacobs K M Heilman Correspondence to: Dr D H Jacobs, Department of Neurology, New England Medical Center Box 314, 750 Washington St, Boston, MA, USA. Received 26 February 1996 and in revised form 2 July 1996 Accepted 11 July 1996 E Shuren, D H Jacobs, K M Heilman Abstract occurred in temporal relation to another-for Objective-Amnesia for temporal rela- example, which of two items was seen most tions may occur without amnesia for con- recently). Material specific temporal order tent memories. The aim was to determine amnesias have also been reported with unilatwhether a patient with mild memory loss eral frontal lobe lesions.910 The dorsomedial due to a thalamic lesion had amnesia for nucleus has extensive connections with the temporal relations, and whether the frontal lobes. In particular, the lateral parvoamnesia was specific for particular mater- cellular region of the dorsomedial nucleus has ial. connections with the dorsolateral frontal corMethods-A male patient had an isolated tex"I making the dorsomedial nucleus a possible right dorsomedial thalamic infarct and participant in the neuronal system that mediresolving amnesia. He was tested on tasks ates temporal order memory processing. relating to content (what) and temporal We report a man with a mild, transient (when) memories for both verbal and amnesia from a single right thalamic infarct, non-verbal material, three and seven affecting predominantly the lateral parvocellumonths after his infarct. lar region of the dorsomedial nucleus. We Results-Three months after his infarct, wanted to determine whether this patient the man had amnesia for temporal, but would be impaired on tasks measuring the not content memories using non-verbal temporal ordering of information and whether stimuli, and normal performance using the material specificity of the amnesia for temverbal stimuli. Seven months after his poral ordering of information would be preinfarct, he had a normal performance sent in this patient with a thalamic lesion. using verbal and non-verbal stimuli. Conclusions-Patients with thalamic lesions may have a material specific Methods amnesia for temporal relations in the CASE HISTORY absence of amnesia for content. A 25 year old right handed man was admitted to hospital after an episode of lightheadedness, nausea, fatigue, and headache that had devel(_ Neurol Neurosurg Psychiatry 1997;62:163-168) oped near the pits at a motor race. He was on no medication and had had 12 years of educaKeywords: amnesia; thalamus; stroke; dementia tion. On admission to the hospital he was disoriented and had slurred speech. During the The dorsomedial nucleus of the thalamus has succeeding days he returned to a normal level been implicated as a structure important for of arousal without evidence of visual loss, focal subserving memory. 1-3 Prominent amnesia weakness, or sensory loss. A limited neuropsymay result from a single thalamic lesion if the chological evaluation performed during the lesion is located anteriorly thereby interrupting first week after the event was remarkable for the mammillothalamic tract (connections with impaired copying of the Rey-Osterreith comhippocampal related structures) and the ven- plex figure'2 (score 28-5, < 10th percentile) as tral part of the internal medullary lamina that well as poor immediate recall (score of 13; contains fibres from the anterior and inferior < 10th percentile) and delayed recall (13-5; thalamic peduncles, due to disconnection of < 10th percentile) of the figure that could not the dorsomedial nucleus from the neocortex.45 be explained by his impaired copying ability Unilateral thalamic damage may result in alone (normative data from Lezak'3). By conmaterial specific amnesias, wherein right sided trast with deficits in non-verbal memory, verlesions produce a non-verbal amnesia, and left bal memory as assessed by the California sided lesions produce a verbal amnesia or a verbal learning test'4 was normal. Finger tapglobal verbal and non-verbal amnesia.6 7 ping was normal bilaterally.'5 Brain CT taken Graff-Radford et a18 have proposed that the five days after admission showed a hypodense thalamus may be especially important in pro- area in the right thalamus consistent with an cessing the contextual aspects of memory, infarct. Laboratory studies including serum including memory for temporal order, due to electrolytes, complete blood count, clotting the extensive conections between the thalamus factors, sedimentation rate, antinuclear antiand the frontal cortex. Previous studies have bodies, fluorescent treponemal antibody, suggested that damage to the frontal lobes antiphospholipid antibodies, lupus anticoaguresults in deficits in the memory of temporal lant, protein C, and lipid profile were normal. order (memory of when one stimulus or event Chest radiography, ECG, Holter monitor, and 164 (A) T2 weighted MRI image in the axial plane of the patient's right thalamic infarct; (B) mapping of the infarct in the axial (Hd +8-0), and (C) in the coronal planes (left Fp + 5 0, rightFp + 10 0) using the atlas of Schaltenbrand and Bailey. 6 A.pr = anteroventral nucleus; Ce mc, Ce pc = centromedian nucleus (one of the intralaminar nuclei); D. c = lateral posterior nucleus; D.im.e, D.im.i = ventrolateral nucleus; D.o.e, D.o.i = ventral anterior nucleus; La. m. c, La. m. ip = internal medullary lamina; L.po.s = ventral anterior nucleus; M.fa.a, M.fa.p, M.c.e = lateral parvocellular region of the dorsomedial nucleus; M.fi.a, M.fi.p, M.c.i = medial magnocellular region of the dorsomedial nucleus; Pu. 1, Pu. m, Pu. o.l, Pu. o. m = lateral posterior nucleus and dorsal parts of the pulvinar nucleus; Rt. c, Rt.po, Rt.pu = reticular nucleus; V.c.e, V.c.i = ventral posterolateral nucleus; V.im.e, V.im.i = ventrolateral nucleus; Z. c. e, Z. c. i = ventral posterolateral nucleus; Z. irn. e, Z. im. i = parts of the ventrolateral and ventral posterolateral nuclei. Shuren, _Jacobs, Heilman ) A B C two dimensional transthoracic and transoesophageal echocardiograms were also nor- mal. When we first examined the patient, three months after his stroke, he was alert and fully oriented and attentive and had a digit span of eight digits forwards and six digits backwards. He recalled three of three words after a five minute delay. Spontaneous speech, comprehension, repetition, and naming were normal. He could copy simple figures. There was no evidence of right-left disorientation, finger agnosia, apraxia, or hemispatial neglect. He could perform simple calculations accurately. The remainder of his neurological examination was normal. MRI ANALYSIS Brain MRI was performed on a 1. 5-Tesla scanner about three months after his stroke. Diencephalic temporal order amnesia 165 Neuropsychology test scores at three months after stroke Test Raw score Wechsler adult intelligence scale-revised: Digit span 9 (scaled score) Object assembly 12 (scaled score) Block design 9 (scaled score) Digit symbol 7 (scaled score) Digit span: Forward 8 Backward 6 Visual span Forward 9 Backward 8 Complex figure test Copy 33 (60th percentile) Immediate 30 (98th percentile) Delayed 31 (100th percentile) Continuous visual memory test: d-Prime 2 12 Total score 82 Trailmaking test: Part A 35 s Part B 68 s Facial recognition test 49 Judgment of line orientation 22 "A" Cancellation 50 Line cancellation 60 Multilingual aphasia examination: Repetition 12 Naming 52 Stroop: Read words 49 s Name colours 62 s Interference 128 s Test Raw score Wechsler memory scale revised: Visual reproductions Immediate 37 Delay 37 Logical memory Immediate 29 Delay 27 California verbal learning test: Total (1-5) 59 Trial 5 Trial 1 Delay 1 Delay 2 Semantic Short Long Levels of processing test: Verbal Nonverbal Design fluency: Free Fixed Wisconsin card sorting test: Categories Correct Errors Non-perseverative Perseverative Florida affect battery - tasks: Facial identity discrimination Facial affect discrimination Non-emotional prosody discriminatson Emotional prosody discrimination Imagery tasks: Facial emotional imagery Object imagery task 14 8 13 13 13 13 35 29 24 22 7 19 11 19 95% 85% 60% 100% All test scores are normal for age and education. All tests are referenced within the text.' 84% 85% aphasia and he performed in the low normal range on the naming and repetition subtests of the multilingual aphasia examination.26 MEMORY TESTS (TABLE) Verbal memory, evaluated using the California verbal learning test and logical stories from the Wechsler memory scale revised,27 was normal. A task using the levels of processing paradigm of Craik and Tulving28 was administered to the patient utilising semantic, orthographic, and phonemic cues to aid encoding of 36 words. Recall was subsequently assessed with a recognition task. His performance was normal. Non-verbal memory, evaluated using the immediate and delayed recall of the ReyOsterreich complex figure, visual reproductions from the Wechsler memory scale revised, and the continuous visual memory test,29 was normal. The patient was given a levels of processing paradigm in which he viewed 30 faces one at a time making a judgment on either the occupation (for example, "Would this person make a good teacher?"), affective expression (for example, "Is this a happy person?"), or gender (for example, "Is this person female?") of each face. Recognition on this task was normal. TEMPORAL ORDER MEMORY TESTS Experimental methods Temporal order memory was evaluated using temporal order and recency judgment tasks from Bowers et al.30 These experimental tasks were originally designed for Bowers et al 's Axial, coronal, and sagittal 4 mm sections 1988 study. The television test3l was also given through the lesion were obtained (figure). The to assess remote memory. All tests were lesion was mapped on to plates from the atlas administered to five male normal controls of Schaltenbrand and Bailey.'6 The mapping matched for age2427 and education (11-12 was highly consistent among planes. years) after informed consent had been The lesion was mapped to a discrete area obtained. The temporal order and recency within the right dorsomedial nucleus affecting judgment tasks had previously been administhe lateral parvocellular region and a small tered to 33 people (mean age = 39-2 years; area of the medial magnocellular region. The mean educational level = 15-7 years) by lateral border of the lesion extended into the Bowers et al.30 Scores for the controls are preinternal medullary lamina in the coronal and sented as mean values. sagittal planes and barely abutted on the internal medullary lamina in the axial plane. The TEMPORAL ORDER JTJDGMENT TASK mammillary bodies, mammillothalamic tract, The patient and controls viewed each of eight intralaminar nuclei, and anterior thalamic different stimuli (list 1) for two seconds. Thirty nuclei were spared. minutes later they viewed another eight stimuli (list 2). Two minutes after the presentation of NEUROPSYCHOLOGICAL ASSESSMENT THREE list 2, a 32 item list composed of the 16 stimuli MONTHS AFTER INJURY from list 1 or 2 randomly intermixed with 16 More extensive neuropsychological testing was distractors was presented and the patient was performed three months after his stroke. The asked to determine whether or not he had table gives all the scores. The tests showed res- been presented with the stimulus before olution of previously seen abnormalities on (recognition) and, if he had, whether or not visuoperceptual and visuospatial tasks as evi- the stimulus had been on list 1 or list 2 (temdenced by normal performances on the facial poral order). Both verbal and non-verbal recognition test,'7 judgment of line orienta- forms of the test were given. Thirty two simple tion,'8 letter cancellation test,'9 line cancella- declarative sentences (for example, "The tion test,20 copy of the Rey-Osterreith complex cooks burned the bread") were used in the figure, and the object assembly and block verbal task and 32 unfamiliar male faces from a design subtests from the Wechsler adult intelli- medical school yearbook were used for the gence scale revised.2' Executive function as non-verbal task. Recognition accuracy and assessed by the Wisconsin card sorting test,22 accuracy of temporal order judgments were Stroop test,23 and design fluency24 was also calculated. Temporal order judgments were normal. His performance on the trail making assessed only on items on which an accurate test25 was normal. There was no evidence of recognition was previously made. Shuren, _Jacobs, Heilman 166 RECENCY JUDGMENT TASK Each word from a list of concrete words was printed on a card and presented one at a time to the patient and controls, who were asked to read each word aloud. Immediately afterwards they were shown a card with two words (both nouns) printed on it of which one word came from the list and one did not (test of recognition) or both words were from the list (test of recency). The patient and controls were asked which word had been read more recently. A word was not used more than once during the test. In the recency judgment trials the two stimuli were always separated on the list by five words but the number of words from the second stimulus to the end of the list varied. The first stimulus was always presented as the first, second, third, or fourth item on the list. In condition I the second stimulus word was the last item on the list. In conditions II-IV the number of intervening words from the second stimulus to the end of the list were four, eight, and 16 respectively. Total list length therefore varied from eight to 26 items. Conditions I-IV were also repeated for recognition judgment trials. Six lists were used for each recency condition and four lists for each recognition condition (40 lists total). A non-verbal analogue of the verbal recency judgment task was also designed using unfamiliar faces from a medical school yearbook. Lists contained only all male or all female faces. Each face was shown for three seconds. However, this task differed from the original task of Bowers et aV30 in that we used unfamiliar faces whereas Bowers et al used pictures of objects. We chose not to use object pictures because real objects can be verbally encoded. In all other respects the tasks were identical. but his accuracy of temporal order judgments was below chance (26-6%; MC 59-5 (2 0)%, MCB 63 (11-2)%). The patient's performance was consistent with a deficit in making nonverbal temporal order judgments. Although his accuracy in making such judgments was below chance, there was no systematic bias in the errors he made (for example, consistently choosing the second list v consistently choosing the first list as the source of the stimulus). RECENCY JUDGMENT TASK Both the patient and controls recognised all target words in all conditions (100%). On recency judgments both the patient and controls showed a progressive decline in performance (patient condition I 100%, condition II 83-3%, condition III 83-3%, condition IV 66-7%; mean for controls condition I 92%, condition II 88%, condition III 72%, condition IV 60%; controls of Bowers et alV0 condition I 96%, condition II 74%, condition III 63%, condition IV 62%). The non-verbal (face) recognition accuracy for the patient was 100% in conditions I-II and 83-3% in conditions III-IV. For the controls, face recognition accuracy was 100% in condition I, 92% in condition II, and 80% in condition III-condition IV. However, the patient's accuracy of recency judgments differed from that of the controls by more than 2SD. The mean (SD) accuracy for controls was condition I 100%, condition II 88 (SD 8-1)%, condition III 72 (SD 8 5)%, and condition IV 65 (SD 1-7)%. The patient's accuracy was condition I 100%, condition II 66-7%, condition III 33-3%, and condition IV 50%. His performance was consistent with an impaired ability to make nonverbal recency judgments. TELEVISION TEST TELEVISION TEST The patient and controls were given the 1991 version of the television test of Squire and Slater to assess remote memory. They were given a 72 question four item multiple choice test in which they were to choose which of the four items had been a show on television. The correct response was always a show that had been on television for only one year. There were 15 shows from 1988 to 1990 (I), 14 from 1985 to 1987 (II), 13 from 1982 to 1984 (III), 14 from 1979 to 1981 (IV), and 15 from 1976 to 1978 (V). The percentage correct for each time period was calculated. Our normative data were combined with those of eight subjects (mean age 23-5, mean education 14 1 years) tested in Dr Squire's laboratory. The patient's scores were 53 3% (I), 35 7% (II), 30 8% (III), 50% (IV), and 40% (V) compared with the controls' mean (SD) scores of 48 (10-7)% (I), 59.3 (13 5)% (II), 53-1(15-1)% (III), 47-5 (10-4)% (IV), and 41-3 (10-7)% (V). The patient's scores were within 2 SD of the scores of the controls. Therefore, the patient's remote memory was in the low range of normal to mildly impaired. In summary, the patient showed a non-verbal anterograde temporal order amnesia with relatively preserved remote memory three months after his stroke. 3 Results TEMPORAL ORDER JUDGMENT TASK On the verbal task the patient had a recognition accuracy of 91 % (mean (SD) for controls (MC) 90 (1 6)%; mean for controls of Bowers et aP30 (MCB) 85 (12 9)%), and an accuracy of temporal order judgments of 93 7% (MC 78 (5*8)%; MCB 78 (10-7)%). On the non-verbal task the patient had a recognition accuracy of 78-1% (MC 69 (4-7)%; MCB 75-3 (9 1)%) TESTING AT SEVEN MONTHS AFTER STROKE The temporal order judgment task was readministered to the patient seven months after his stroke. On the verbal task his recognition accuracy was 91 % and his temporal order judgment accuracy was 100%. On the nonverbal task his recognition accuracy was 81 % and his temporal order judgment accuracy was 81 % which are superior to the performance of both our controls and those of Bowers et al.'O Discussion Our patient initially developed a selective Diencephalic temporal order amnesia amnesia for non-verbal content due to a right thalamic infarct. Three months later the amnesia for content had resolved. However, a material specific amnesia for temporal ordering of non-verbal material was evident. Both short term (impaired recency judgment) and long term (impaired temporal order judgment) anterograde temporal order memory were impaired without abnormal performance on the recognition (content) portion of those two tasks. This performance suggests a reproducible anterograde material specific amnesia for temporal ordering of non-verbal stimuli. The patient performed normally on a third task, the television test, that differs from the two other tasks as it measures whether a retrograde component existed for the amnesia in this patient. The results suggest that such a component did not exist. In agreement with Milner et al,'2 we have found that temporal order amnesia can be material specific, with the new additional finding that the material specificity of the amnesia for temporal ordering exists in patients with thalamic lesions. The role of the thalamus in processing contextual aspects of memory has also been considered by Shinamura and Squire, who found that a group of patients with Korsakoffs syndrome performed poorly on a source memory task in which patients were asked to identify the source of a memory." Moreover, their performances did not correlate with their ability to recall facts, suggesting that contextual memories and fact memories measure slightly different abilities. Kopelman34 showed that patients with Korsakoff's syndrome as well as patients with Alzheimer's disease did poorly on a task of providing temporal context about a memory as well as being amnestic for the content of the memory. Hunkin et al35 reported that amnesics with diencephalic lesions did worse than those with temporal lobe lesions on a temporal discrimination task. Content (what) memories and temporal (when) memories may be processed differently.9 36 37 Milner et al9 32 found that patients with unilateral left temporal excisions had impaired verbal recognition memory but preserved verbal recency judgments, whereas patients with left frontal excisions had impaired verbal recency judgments but preserved verbal recognition memory. Patients with right temporal or frontal excisions showed the same patterns of deficits as their left sided counterparts except that the processing deficits were only for non-verbal rather than verbal material. Poor recency judgment followed removal of the midlateral frontal cortex. One amnesic patient, who had bilateral temporal excisions, had relative sparing of temporal order memory in the presence of profound deficits for recognition (content) memory.'6 The double dissociations described above make much less likely the possibility that patients perform worse on a temporal ordering task because it is more difficult; it would then be impossible to explain the performance of those patients with temporal excisions who did worse on the recognition memory tasks than on the recency judgment tasks. Moreover, our 167 patient showed normal to superior performance on other comparably difficult tasks that involved either memory (for example, verbal recency judgment tasks and temporal order judgment tasks, immediate and delayed recall of the Rey-Osterreich complex figure) or non-memory processing (for example, the Wisconsin card sorting test). Therefore his performance cannot be attributed to a generalised memory or cognitive abnormality. Whereas the thalamus seems to be important for processing the temporal aspects of memory, Bowers et al30 showed temporal order amnesia in a patient with a lesion in the retrosplenial cortex, an area that has extensive connections to the thalamus. Sagar et al reported that patients with Parkinson's disease had abnormalities on tasks of temporal ordering.38 Therefore, a variety of extralimbic structures in addition to the frontal lobes may be important for processing the context of memories, including the temporal ordering of information. The thalamus may be important for both the content and the context of memory. Kritchevsky et al noted that patients with medial thalamic damage affecting only the dorsomedial nucleus may have mild and transient amnesias.39 Similarly, Von Cramon et at4 suggested that thalamic lesions of the anterior nucleus of the thalamus are more likely than those of the dorsomedial nucleus to produce severe target amnesias (amnesia for content of memories). Whereas others have noted that large dorsomedial lesions, particularly those that also impinge on the mammilothalamic tract, may also produce a lasting amnesia,8 our patient and others with circumscribed lesions within the dorsomedial nucleus of the thalamus have recovered relatively well from their amnesias. Therefore, our patient's performance on memory tasks is like that of other reported patients. Mennemeier et at40 proposed that an attentional-amnestic disturbance may be associated with a thalamic intralaminar nucleus lesion. Our patient did not, at three months after injury, show evidence of either impaired content memory of abnormal attention on digit span or the trailmaking test (table). Therefore, the available evidence does not support the alternative explanation that our patient had an attentional disturbance. Arguably, our results could have been an artifact of our test design. Temporal order and recency judgments may require recall whereas the recognition paradigm does not. However, on both the recall paradigms of the Rey-Osterreich complex figure and the Wechsler memory scale revised, our patient scored in the high normal range. Secondly, his performance on the verbal temporal order and recency judgment paradigms was normal. Therefore, other tasks that were given do not strongly support this interpretation, as he performed normally on other recall tasks. MECHANISM OF TEMPORAL ORDER AMNESIA The mechanism of temporal ordering is unknown. Several suggestions have been made Shuren, _Jacobs, Heilman 168 regarding the possible mechanism. Recalling when an event took place may occur through an indirect means whereby a mechanism either discriminates or compares two events and determines which event occurred before or after the other4' 4 or reconstructs the order of events using general knowledge (deductive reasoning) about other events that may have occurred at that time (for example, "I must have taken the test in December because it was given a few days before Christmas").4 Alternatively, a direct means may be used whereby specific temporal information is recalled (for example, "The gun was fired on Monday at 10 o'clock in the morning").4546 Based on our data, it is not possible to determine which mechanism might be impaired in our patient. Sagar et al36 propose that temporal order memory processing by indirect means is subserved by the frontal lobes whereas temporal order memory processing by direct means is subserved by limbic-diencephalic structures. Both the frontal lobes and the limbic system have connections with the dorsomedial thalamic nucleus. The dorsomedial nucleus can be divided into medial and lateral regions. The lateral, parvocellular region of the dorsomedial nucleus, the portion that was damaged the most in our patient, has connections with the lateral prefrontal cortex, whereas the medial magnocellular region has connections with medial prefrontal and orbitofrontal cortices, amygdala (ventroamygdalofugal pathway), entorhinal, perirhinal, and temporal polar cortices.47 Damage to the lateral region of the dorsomedial nucleus may result in the loss of temporal order memories in isolation, perhaps due to disrupted dorsolateral prefrontal connections. 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