Impaired recall and preserved encoding in prominent amnesic syndrome: A case of basal forebrain amnesia Article abstract-We describe a patient who developed amnesia following extensive basal forebrain infarct. He completely recovered from the infarct 32 days postonset. He had poor spontaneous recall and preserved recognition of recent as well as more remote events. Surprisingly, he could recall events in sequence during the postictal amnesic period after recovery. We speculate that encoding and recall may employ different neural systems. NEUROLOGY 1998;50:539-541 Reiko Fukatsu, MD; Atsushi Yamadori, MD; and Toshikatsu Fujii, MD The basal forebrain plays a special role in human We cared for a patient with severe amnesia after basal forebrain infarction; fortunately he recovered. Surprisingly he could recall events from his morbid period once the amnesic syndrome cleared. Patient report. A 70-year-old right-handed man, a practicing gynecologist, became suddenly confused on June 25, 1995, and was admitted to the Sendai National Hospital the next day. On admission he was alert, but was disoriented to time and place. General physical and neurologic examinations were unremarkable. He wandered around the ward believing he was in his own clinic. From day 4 onward we evaluated his neuropsychological status. Amnesic period. Initially he showed a pure amnesic syndrome characterized by severe anterograde amnesia coupled with retrograde amnesia, despite normal intelligence. He showed no other cognitive impairment. His digit and block-tapping span were both 5. Retrograde amnesia extended back 5 to 10 years, judging from the autobiographic memory inter vie^.^ On day 15, the Public Event Test devised by us8 revealed that his memory up to the 1970s was preserved a t an above-average rate. It declined for the 1980s but was still within normal range. Memory testing for each year after 1990 showed that his recall for the 1990s was very impaired, but recognition was fairly accurate (table). The table summarizes the results of our memory and general neuropsychological assessment. His performance both on verbal and visual memory tests was impaired. However, surprisingly, his recognition memory on the Auditory Verbal Learning Test (AVLT) was well preserved. The patient and his wife allowed us to read his diary, which he kept up even after the amnesic ictus. No correct records were entered. Everyday he wrote about his mother’s funeral held 5 years previously, mentioning: staying i n Miyako City [where his mother died], attending Mother’s funeral at 6:30 PM, visiting a grave in the morning and receiving friends at home in the afternoon and seeing them off to a nearby station. His main subjects concerned Miyako City or his mother’s funeral. The diary was discontinued on day 17. Clearing of amnesia. Severity of the amnesia remained essentially the same for 23 days. On day 24 retrograde amnesia decreased for several weeks. Memory after the ictus (postictal amnesia) and anterograde memory were still strikingly poor. On day 32 anterograde amnesia showed a dramatic recovery. He correctly answered that he was to be discharged that day, that he saw a profes- sional baseball game on TV the previous night, and he gave the correct name of the MVP. Most surprisingly, his postictal amnesia started to ameliorate. He was able to recall correctly several events that occurred after admission. He remembered the correct name of the hospital, the date of admission, the name of the neurologist, and two MRI examinations, one of which was done in the basement of the hospital and the other a t another hospital. These recollections occurred spontaneously on questioning, not by forced choice or cuing. Confabulatory responses became prominently less. He resumed his practice on day 37 without any trouble. On day 39 he recalled that he received an EEG twice-one right after admission and the other 25 days after admission. The second AVLT yielded the scores of 3, 5 , 9, 7, 10, and 5 for the first to sixth trials, and a perfect score (15) for recognition. Thus the objective evaluation obtained using the AVLT corroborated the clinical improvement. On day 46 retrograde amnesia was less than 10 days. Postictal amnesia showed further improvement. He recalled correctly the cerebral arteriographic examination on day 5 and his doctor’s explanation of injection of contrast material. He recalled the Holter ECG examination on day 8 and the ECG on day 10. He hesitantly recalled that he played “Igo” games with his wife in the hospital and won, which was accurate. When referring t o events during his stay in the hospital, he often used wording such as “it seems,” “I think,” or “I presume,” reflecting his uncertainty about his recall, which was a radical departure from his richly confabulated responses. Neuroirnaging examination. On day 17 an MRI with gadolinium revealed lesions in the corpus callosum extending from the genu to the rostrum, bilateral heads of the caudate nucleus, bilateral nucleus accumbens, bilateral columns of fornix, part of the left anterior limb of the internal capsule, bilateral subcallosal areas, rostra1 part of the septa1 area, and the medial anterior hypothalamus. The distribution of the lesions remained essentially same, although much smaller, on MRI 4 months later (figure). Cerebral angiography revealed occlusions a t the left anterior communicating artery and A2 portion of the left anterior cerebral artery. Perforating arteries of the anterior communicating artery and the left Heubner’s artery were not visualized. Discussion. The amnesic syndrome during its active period occurred as follows: (1) severe impairment of memory for current events (i.e., anterograde amnesia), (2) difficulty recalling episodes that occurred after the ictus (which we call postictal amFebruary 1998 NEUROLOGY 50 539 Table Memory and general neuropsychology during the patient’s amnesic period Memory ROCF (day 11) COPY Immediate 40-min delay AVLT (day 15) 1st-5th trial 6th trial Recognition BVRT (day 18) Immediate 15-see delay Recognition (15-sec delay) Public Event Test (day 15) 1950-1989 (Recognition) % correct 1990-1995 Free recall Recognition PSMT (day 18) Background information Childhood Early adult life Recent information WMS-R (day 19) MQ Verbal memory Visual memory Language SLTA (day 8 ) Auditory comprehension Repetition Naming Oral reading (KanjUKana) Writing to dictation (KanjUKana) Frontal lobe functions WCST (day 15) Categories achieved Perseverative errors Verbal fluency (day 15) Animal Intelligence WAIS-R (day 20) Full IQ VIQ PIQ RCPM (day 20) 33/36 7/36 6136 4,3,4,6,4/15 0115 13/15 3 correct, 13 errors 4 correct, 16 errors 7/16 50s 60s 70s 80s 80 80 90 70 90 91 92 93 94 95 113 113 013 113 113 113 313 213 313 313 213 313 23/23 2 1121 14/21 5121 68 57 95 100% correct 100%correct 100% correct 100%correct 100% correct 3 34 16lmin 98 101 94 32136 ROCF = Rey-Osterrieth Complex Figure Test; AVLT = Auditorj Verbal Learning Test; BVRT = Benton Visual Retention Test; PSMT = Personal Semantic Memory Test; WMS-R = Wechsler Memory Scale-Revised; MQ = memory quotient; SLTA = Standard Language Test of Aphasia; WCST = Wisconsin Card Sorting Test; WAIS-R = Wechsler Adult Intelligence Scale-Revised; VIQ = verbal intelligence quotient; PIQ = performance intelligence quotient; RCPM = Raven Colored Progressive Matrices. 540 NEUROLOGY 50 February 1998 Figure. (A-C) Coronal (A), axial (B), and sagittal (C) TIweighted M R images with gadolinium performed on day 17 (upper row) and on day 105 (lower row). In the coronal and axial sections, the left side of the images corresponds to the right side of the brain. I n the sagittal sections, the first and second images represent the right hemisphere, and the third and fourth images represent the left hemisphere. nesia after Russell’s post-traumatic amnesia9 t o separate it from memory impairment for ongoing events), (3) retrograde amnesia going back 10 years, and (4)a strong dissociation between poor spontaneous recall and preserved recognition memory. The most impressive feature of our patient was the fact that he could keep encoding moment-tomoment events at the very time when his amnesia was the most acute. After recovery he could recall not only events, but also context, including temporal, spatial, and personal aspects, although with some uncertainty. On examination during the amnesic period he could not recall where he was or what he did during the day, and he kept a completely confabulatory diary. Yet after recovery he could recall when, where, and what kind of laboratory examinations he had received, who examined him, and when he was granted leave and how often. In amnesic syndromes affecting the basal forebrain area, Damasio et a1.2 noted that cuing helps recall some of the memory traces, indicating a possibility that the encoding and recalling processes are separate. However, prognosis in basal forebrain amnesia is generally poor, and no cases of recovery have been reported to our knowledge, making it impossible to determine how much information can actually be stored during the amnesic period. This is the first patient report in which preservation of the encoding process during the amnesic period was unequivocally confirmed thanks to good recovery. Recently Vuilleumier et a1.l0 reported a similar dissociation between encoding and recall in a patient with nonconvulsive status epilepticus, although the clinical pattern and etiology are different from our patient. Their patient and ours indicate that memorizing and recalling events are two distinct processes mobilizing different neural systems. For voluntary recall of the stored episodes, the basal forebrain region may play a crucial role. Because our patient recovered well, we believe that the neighboring structures that became dysfunctional i n the acute stage, but survived permanent damage, may be more critical in producing the peculiar pattern of amnesia. Preservation of the encoding process may reflect the fact that the hippocampal as well as diencephalic regions were spared. These regions may automatically encode continuous events together with its context. Passive recall, like recognition, may also be possible if the temporoparieto-occipital processing systems are coactive with the posterior memory systems, including the hippocampus. On rare occasions some distinct lesions in the basal forebrain with pre- served hippocampal-diencephalic structures may produce pure recall amnesia. Acknowledgment We express our gratitude to Dr Y. Sakurai, Director of Neurosurgery, Sendai National Hospital, for permission to investigate the patient. From the Department of Neurology (Dr. Fukatsu), Miyagi National Hospital; and the Section of Neuropsychology (Drs. Yamadori and Fujii), Division of Disability Science, Tohoku University Graduate School of Medicine, Sendai, Japan. Received February 12, 1997. Accepted in final form July 14, 1997. Address correspondence and reprint requests t o Dr. Reiko Fukatsu, Department of Neurology, Miyagi National Hospital, Yamamoto-cho, Watari-gun, Miyagi 989-22, Japan. References 1. Alexander MP, Freedman M. Amnesia after anterior communicating artery aneurysm rupture. Neurology 1984;34:752757. 2. Damasio AR, Graff-Radford NR, Eslinger P J , Damasio H, Kassell N. Amnesia following basal forebrain lesions. Arch Neurol 1985;42:263-271. 3. Phillips S, Sangalang V, Sterns G. Basal forebrain infarction: a clinicopathologic correlation. Arch Neurol 1987;44:11341138. 4. Irle E, Wowra B, Kunert HJ, Hampl J , Kunze S. Memory disturbances following anterior communicating artery rupture. Ann Neurol 1992;31:473-480. 5. Morris MK, Bowers D, Chatterjee A, Heilman KM. Amnesia following a discrete basal forebrain lesion. Brain 1992;115: 1827-1847. 6. Miyake H, Tanaka T, Yamadori A. A case of basal forebrain amnesia (in Japanese). Jpn J Neuropsychol 199430: 153-159. 7. Kopelman MD, Wilson BA, Baddeley AD. The autobiographical memory interview: a new assessment of autobiographical and personal semantic memory in amnesic patients. J Clin Exp Neuropsychol 1989;11:724-744. 8. 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I 1 February 1998 NEUROLOGY 50 641 Impaired recall and preserved encoding in prominent amnesic syndrome: A case of basal forebrain amnesia Reiko Fukatsu, Atsushi Yamadori and Toshikatsu Fujii Neurology 1998;50;539-541 DOI 10.1212/WNL.50.2.539 This information is current as of February 1, 1998 Updated Information & Services including high resolution figures, can be found at: http://www.neurology.org/content/50/2/539.full.html Citations This article has been cited by 2 HighWire-hosted articles: http://www.neurology.org/content/50/2/539.full.html##otherarticles Permissions & Licensing Information about reproducing this article in parts (figures,tables) or in its entirety can be found online at: http://www.neurology.org/misc/about.xhtml#permissions Reprints Information about ordering reprints can be found online: http://www.neurology.org/misc/addir.xhtml#reprintsus Neurology ® is the official journal of the American Academy of Neurology. 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