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Transient Retrograde Amnesia: A focal and selective (but temporary) loss of memory for autobiographical events
c o r t e x 6 4 ( 2 0 1 5 ) 4 2 6 e4 2 8
Available online at www.sciencedirect.com
ScienceDirect Journal homepage: www.elsevier.com/locate/cortex
Clinical postcard
Transient Retrograde Amnesia: A focal and selective (but temporary) loss of memory for autobiographical events Rosaleen A. McCarthy* and George Pengas Wessex Neurological Centre, Southampton General Hospital, University Hospitals NHS Foundation Trust, United Kingdom
Transient memory disorders are not all global. Temporary disruption may affect procedural knowledge (Stracciari, Guarino, & Pazzaglia, 1997), semantic memory (Hodges, 1997); verbal learning and memory (Nishiyama, Kurisaki, Bandoh, Ishikawa, & Sugishita, 1993); autobiographical knowledge (Venneri & Caffarra, 1998); people (Kapur, Katifi, elZawawi, Sedgwick, & Barker, 1994) and topographical orienciga et al., 2002). We have recently learned of a tation (Gil-Ne case of focal Transient Retrograde Amnesia (TRAM) that appears to have spared the patient's anterograde memory as well as retrograde familiarity for friends and family. Frances is a 62 year old, right handed retired professional woman who has been under investigation at the Wessex Neurological Unit following three episodes of transient global amnesia (TGA). In 2011 she had been investigated for paraesthesia and vertigo, undergoing an MRI scan. The first episode of TGA (13/03/12) lasted for approximately 4 h and occurred at a family funeral: Frances repeatedly greeted the same friends as if they had just arrived and repetitively asked whether certain people were going to attend. She made a full recovery. After the event, Frances listened to a CD recording of the funeral but did not experience any recognition. Two further, similar episodes of TGA occurred in May and August 2014. The episode of Transient Retrograde Amnesia (TRAM) occurred at the reception following another family funeral (15/ 09/14). Frances's TRAM event differed very clearly from the previous three TGA occurrences due to sparing of Frances's anterograde memory and new learning:
There was no repetitive questioning Frances clearly remembered the immediate past and present Older memories from the previous day and earlier were not retrieved. Frances's husband recorded the details of the event and his notes are reproduced below (with minimal editing to preserve anonymity). Frances was in conversation with a relative who asked her something like “What did the consultants say last week?” Frances said, “I don't know” and smiled. Her husband asked “Do you really not know?” and Frances confirmed she could not remember. “We sit down with M (a close friend) and go through some questions. Frances could remember everything that has happened that morning e (including a conversation and the name of one of the people who had sent flowers)” “Frances knows where she is, why she is there and everyone in the room. Frances cannot remember her previous medical appointments, who is currently staying with us (Tom and Laura had arrived the previous afternoon to stay and were planning to visit the Boat Show). Frances could not remember what we did Saturday afternoon/evening (visiting neighbours for a barbeque).” “After 5 minutes Frances began to remember some details from the weekend - seeing Tina and Joe on Saturday and then Carol
DOIs of original article: http://dx.doi.org/10.1016/j.cortex.2014.12.011, http://dx.doi.org/10.1016/j.cortex.2014.12.003. * Corresponding author. E-mail addresses: [email protected] (R.A. McCarthy), [email protected] (G. Pengas). http://dx.doi.org/10.1016/j.cortex.2014.12.012 0010-9452/© 2015 Published by Elsevier Ltd.
427
c o r t e x 6 4 ( 2 0 1 5 ) 4 2 6 e4 2 8
Table 1 e Frances's scores on measures of anterograde and retrograde memory. Anterograde verbal BMIPB story 1 immediate BMIPB story 1 delay -CVLT Trial 1e5 List B Short-delay free Short-delay cued Long-delay free Long-delay cued Intrusions Total hits False positives Recognition d’ -Warrington RMT words Anterograde non-verbal -Digit symbol paired recall -Digit symbol free recall -Warrington RMT faces
Percentile
Retrograde
Score
50 50e75
Famous names alive/dead Face familiarity Face identification Face naming Public events (N ¼ 33) ◦ 1981e1985 ◦ 1986e1990 ◦ 1991e1995 ◦ 1996e2000 ◦ 2005e2012 -Autobiographical events -Flashbulb: Diana's death -Flashbulb: 9/11 attack Graded naming test Verbal fluency FAS Semantic Switch
100% 75/75 73/75 65/75 Mean (max 2) 1.75 1.71 1.4 1.83 1.86 Good Good Good 95th percentile
79 7 50 50 16 31 31 2 16 2 75 >50 >50 75
91st percentile 98th percentile 84th percentile
Results of memory tests carried out two days after Frances's episode of TRAM. Anterograde memory test scores are converted to the nearest equivalent percentile rank (from Z and T values) in order to facilitate comparisons.
and Jeff and then the barbeque …. Remembers some details unprompted (“I made salads”). Remembers Tom and Laura arriving to stay. After 10e15 minutes she was back to normal.” MRI scanning in 2011 showed a small ischemic infarct in the right centrum semiovale; there was no change in 2014. EEG was normal. Frances was seen in Neuropsychology two days after her period of TRAM. Frances had clear recall of the TRAM episode and remembered that, at the time, she felt distressed at her difficulties. She scored within her expected range on measures of intellectual function (WAIS III) with scores at a superior level on Vocabulary, and average on Similarities and Digit Span. France's Non-Verbal subtest scores were all average. On tests of anterograde memory Frances's scores were mostly good (see Table 1). She made an increased number of false positives and missed a number of targets on the yes/no recognition phase of the California Verbal Learning Test (CVLT). Frances's retrograde memory was tested by measures of Famous Face recognition and naming and by questioning about “public” events spanning the previous thirty-five years (e.g., Why was there concern about Volcanic Ash in the UK?). Frances's knowledge of personal events was evaluated across the same era using pictures and details of events provided by her husband (e.g., holidays, weddings and family gettogethers). Frances could give the same information as her husband in regard to these items. We were led to conclude that her retrograde memory had fully recovered to its good pre TRAM level. The characteristics of Frances's amnesia differ from those reported in psychogenic memory loss in terms of age of onset duration (very brief) and the apparent sparing of personal semantic knowledge including recognition of friends and family (Stracciari, Fonti, & Guarino, 2008). We have found no evidence of temporal lobe seizure semiology, nor of features of Transient Epileptic Amnesia (such as confusional state in
the mornings, persisting remote autobiographical episodic memory loss or lacunes, nor accelerated forgetting) (review in Elliott, Isaac, & Muhlert, 2014). Her autobiographical memory was clearly affected but we cannot ascertain whether her retrograde amnesia extended to include public events as well. We are also unable to be sure of the duration of her TRAM as the amnesia only became apparent to others when Frances was directly asked to recall a specific event of the previous week. At a minimum the episode lasted for 20 min and at a maximum it may have lasted for around 2 h. It is possible that Frances herself only became aware of her autobiographical retrograde amnesia following direct questioning. Frances's preserved memory for events earlier in the day may have been due to the relative preservation of her ability to acquire new memories (anterograde memory) despite the onset of her un-detected TRAM. The qualitative characteristics of Frances's TRAM are very similar to those observed in cases of chronic retrograde memory loss. Specifically, Frances showed an inability to retrieve autobiographical events and episodes with relative sparing of personal semantic knowledge and familiarity for family members and places (e.g., McCarthy, Kopelman, & Warrington, 2005). We would argue that Frances's TRAM lies at one extreme of the range of possible presentations of TGA. Whereas classical TGA has its major impact on anterograde memory, Frances TRAM affects her retrograde memory and spares her anterograde memory.
references
Elliott, G., Isaac, C. L., & Muhlert, N. (2014). Measuring forgetting: a critical review of accelerated long-term forgetting studies. Cortex, 54, 6e32. ciga, E., Alberca, R., Boza, F., Montes, E., Sa nchez, B., Garcı´a Gil-Ne Lozano, R., et al. (2002). Transient topographical Disorientation. European Neurology, 48, 191e199.
428
c o r t e x 6 4 ( 2 0 1 5 ) 4 2 6 e4 2 8
Hodges, J. R. (1997). Transient semantic amnesia: a new syndrome? Journal of Neurology, Neurosurgery, and Psychiatry, 63, 548e549. http://dx.doi.org/10.1136/jnnp.63.4.548. Kapur, N., Katifi, H., el-Zawawi, H., Sedgwick, M., & Barker, S. (1994). Transient memory loss for people. Journal of Neurology, Neurosurgery, and Psychiatry, 57, 862e864. McCarthy, R. A., Kopelman, M. D., & Warrington, E. K. (2005). Remembering and forgetting of semantic knowledge in amnesia: a 16-year follow-up investigation of RFR. Neuropsychologia, 43, 356e372. Nishiyama, K., Kurisaki, H., Bandoh, M., Ishikawa, T., & Sugishita, M. (1993). Transient partial verbal amnesia. Journal of Neurology, Neurosurgery and Psychiatry, 56, 1234e1235. Stracciari, A., Fonti, C., & Guarino, M. (2008). When the past is lost: focal retrograde amnesia. Focus on the “functional” form.
Behavioral Neurology, 20, 113e125. http://dx.doi.org/10.3233/ BEN-2008-0222. Stracciari, A., Guarino, M., & Pazzaglia, P. (1997). Transient procedural amnesia. The Italian Journal of Neurological Sciences, 18, 35e36. Venneri, A., & Caffarra, P. (1998). Transient autobiographical amnesia: EEG and single-photon emission CT evidence of an organic etiology. Neurology, 50, 186e191.
Received 26 November Reviewed 26 November Revised 3 December Accepted 17 December
2014 2014 2014 2014
Available online at www.sciencedirect.com
ScienceDirect Journal homepage: www.elsevier.com/locate/cortex
Clinical postcard
Transient Retrograde Amnesia: A focal and selective (but temporary) loss of memory for autobiographical events Rosaleen A. McCarthy* and George Pengas Wessex Neurological Centre, Southampton General Hospital, University Hospitals NHS Foundation Trust, United Kingdom
Transient memory disorders are not all global. Temporary disruption may affect procedural knowledge (Stracciari, Guarino, & Pazzaglia, 1997), semantic memory (Hodges, 1997); verbal learning and memory (Nishiyama, Kurisaki, Bandoh, Ishikawa, & Sugishita, 1993); autobiographical knowledge (Venneri & Caffarra, 1998); people (Kapur, Katifi, elZawawi, Sedgwick, & Barker, 1994) and topographical orienciga et al., 2002). We have recently learned of a tation (Gil-Ne case of focal Transient Retrograde Amnesia (TRAM) that appears to have spared the patient's anterograde memory as well as retrograde familiarity for friends and family. Frances is a 62 year old, right handed retired professional woman who has been under investigation at the Wessex Neurological Unit following three episodes of transient global amnesia (TGA). In 2011 she had been investigated for paraesthesia and vertigo, undergoing an MRI scan. The first episode of TGA (13/03/12) lasted for approximately 4 h and occurred at a family funeral: Frances repeatedly greeted the same friends as if they had just arrived and repetitively asked whether certain people were going to attend. She made a full recovery. After the event, Frances listened to a CD recording of the funeral but did not experience any recognition. Two further, similar episodes of TGA occurred in May and August 2014. The episode of Transient Retrograde Amnesia (TRAM) occurred at the reception following another family funeral (15/ 09/14). Frances's TRAM event differed very clearly from the previous three TGA occurrences due to sparing of Frances's anterograde memory and new learning:
There was no repetitive questioning Frances clearly remembered the immediate past and present Older memories from the previous day and earlier were not retrieved. Frances's husband recorded the details of the event and his notes are reproduced below (with minimal editing to preserve anonymity). Frances was in conversation with a relative who asked her something like “What did the consultants say last week?” Frances said, “I don't know” and smiled. Her husband asked “Do you really not know?” and Frances confirmed she could not remember. “We sit down with M (a close friend) and go through some questions. Frances could remember everything that has happened that morning e (including a conversation and the name of one of the people who had sent flowers)” “Frances knows where she is, why she is there and everyone in the room. Frances cannot remember her previous medical appointments, who is currently staying with us (Tom and Laura had arrived the previous afternoon to stay and were planning to visit the Boat Show). Frances could not remember what we did Saturday afternoon/evening (visiting neighbours for a barbeque).” “After 5 minutes Frances began to remember some details from the weekend - seeing Tina and Joe on Saturday and then Carol
DOIs of original article: http://dx.doi.org/10.1016/j.cortex.2014.12.011, http://dx.doi.org/10.1016/j.cortex.2014.12.003. * Corresponding author. E-mail addresses: [email protected] (R.A. McCarthy), [email protected] (G. Pengas). http://dx.doi.org/10.1016/j.cortex.2014.12.012 0010-9452/© 2015 Published by Elsevier Ltd.
427
c o r t e x 6 4 ( 2 0 1 5 ) 4 2 6 e4 2 8
Table 1 e Frances's scores on measures of anterograde and retrograde memory. Anterograde verbal BMIPB story 1 immediate BMIPB story 1 delay -CVLT Trial 1e5 List B Short-delay free Short-delay cued Long-delay free Long-delay cued Intrusions Total hits False positives Recognition d’ -Warrington RMT words Anterograde non-verbal -Digit symbol paired recall -Digit symbol free recall -Warrington RMT faces
Percentile
Retrograde
Score
50 50e75
Famous names alive/dead Face familiarity Face identification Face naming Public events (N ¼ 33) ◦ 1981e1985 ◦ 1986e1990 ◦ 1991e1995 ◦ 1996e2000 ◦ 2005e2012 -Autobiographical events -Flashbulb: Diana's death -Flashbulb: 9/11 attack Graded naming test Verbal fluency FAS Semantic Switch
100% 75/75 73/75 65/75 Mean (max 2) 1.75 1.71 1.4 1.83 1.86 Good Good Good 95th percentile
79 7 50 50 16 31 31 2 16 2 75 >50 >50 75
91st percentile 98th percentile 84th percentile
Results of memory tests carried out two days after Frances's episode of TRAM. Anterograde memory test scores are converted to the nearest equivalent percentile rank (from Z and T values) in order to facilitate comparisons.
and Jeff and then the barbeque …. Remembers some details unprompted (“I made salads”). Remembers Tom and Laura arriving to stay. After 10e15 minutes she was back to normal.” MRI scanning in 2011 showed a small ischemic infarct in the right centrum semiovale; there was no change in 2014. EEG was normal. Frances was seen in Neuropsychology two days after her period of TRAM. Frances had clear recall of the TRAM episode and remembered that, at the time, she felt distressed at her difficulties. She scored within her expected range on measures of intellectual function (WAIS III) with scores at a superior level on Vocabulary, and average on Similarities and Digit Span. France's Non-Verbal subtest scores were all average. On tests of anterograde memory Frances's scores were mostly good (see Table 1). She made an increased number of false positives and missed a number of targets on the yes/no recognition phase of the California Verbal Learning Test (CVLT). Frances's retrograde memory was tested by measures of Famous Face recognition and naming and by questioning about “public” events spanning the previous thirty-five years (e.g., Why was there concern about Volcanic Ash in the UK?). Frances's knowledge of personal events was evaluated across the same era using pictures and details of events provided by her husband (e.g., holidays, weddings and family gettogethers). Frances could give the same information as her husband in regard to these items. We were led to conclude that her retrograde memory had fully recovered to its good pre TRAM level. The characteristics of Frances's amnesia differ from those reported in psychogenic memory loss in terms of age of onset duration (very brief) and the apparent sparing of personal semantic knowledge including recognition of friends and family (Stracciari, Fonti, & Guarino, 2008). We have found no evidence of temporal lobe seizure semiology, nor of features of Transient Epileptic Amnesia (such as confusional state in
the mornings, persisting remote autobiographical episodic memory loss or lacunes, nor accelerated forgetting) (review in Elliott, Isaac, & Muhlert, 2014). Her autobiographical memory was clearly affected but we cannot ascertain whether her retrograde amnesia extended to include public events as well. We are also unable to be sure of the duration of her TRAM as the amnesia only became apparent to others when Frances was directly asked to recall a specific event of the previous week. At a minimum the episode lasted for 20 min and at a maximum it may have lasted for around 2 h. It is possible that Frances herself only became aware of her autobiographical retrograde amnesia following direct questioning. Frances's preserved memory for events earlier in the day may have been due to the relative preservation of her ability to acquire new memories (anterograde memory) despite the onset of her un-detected TRAM. The qualitative characteristics of Frances's TRAM are very similar to those observed in cases of chronic retrograde memory loss. Specifically, Frances showed an inability to retrieve autobiographical events and episodes with relative sparing of personal semantic knowledge and familiarity for family members and places (e.g., McCarthy, Kopelman, & Warrington, 2005). We would argue that Frances's TRAM lies at one extreme of the range of possible presentations of TGA. Whereas classical TGA has its major impact on anterograde memory, Frances TRAM affects her retrograde memory and spares her anterograde memory.
references
Elliott, G., Isaac, C. L., & Muhlert, N. (2014). Measuring forgetting: a critical review of accelerated long-term forgetting studies. Cortex, 54, 6e32. ciga, E., Alberca, R., Boza, F., Montes, E., Sa nchez, B., Garcı´a Gil-Ne Lozano, R., et al. (2002). Transient topographical Disorientation. European Neurology, 48, 191e199.
428
c o r t e x 6 4 ( 2 0 1 5 ) 4 2 6 e4 2 8
Hodges, J. R. (1997). Transient semantic amnesia: a new syndrome? Journal of Neurology, Neurosurgery, and Psychiatry, 63, 548e549. http://dx.doi.org/10.1136/jnnp.63.4.548. Kapur, N., Katifi, H., el-Zawawi, H., Sedgwick, M., & Barker, S. (1994). Transient memory loss for people. Journal of Neurology, Neurosurgery, and Psychiatry, 57, 862e864. McCarthy, R. A., Kopelman, M. D., & Warrington, E. K. (2005). Remembering and forgetting of semantic knowledge in amnesia: a 16-year follow-up investigation of RFR. Neuropsychologia, 43, 356e372. Nishiyama, K., Kurisaki, H., Bandoh, M., Ishikawa, T., & Sugishita, M. (1993). Transient partial verbal amnesia. Journal of Neurology, Neurosurgery and Psychiatry, 56, 1234e1235. Stracciari, A., Fonti, C., & Guarino, M. (2008). When the past is lost: focal retrograde amnesia. Focus on the “functional” form.
Behavioral Neurology, 20, 113e125. http://dx.doi.org/10.3233/ BEN-2008-0222. Stracciari, A., Guarino, M., & Pazzaglia, P. (1997). Transient procedural amnesia. The Italian Journal of Neurological Sciences, 18, 35e36. Venneri, A., & Caffarra, P. (1998). Transient autobiographical amnesia: EEG and single-photon emission CT evidence of an organic etiology. Neurology, 50, 186e191.
Received 26 November Reviewed 26 November Revised 3 December Accepted 17 December
2014 2014 2014 2014