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Extensive and Temporally Ungraded Retrograde Amnesia in Encephalitis Associated with Antibodies to Voltage-Gated Potassium Channels

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Extensive and Temporally Ungraded Retrograde Amnesia in Encephalitis Associated with Antibodies to Voltage-Gated Potassium Channels ORIGINAL CONTRIBUTION Extensive and Temporally Ungraded Retrograde Amnesia in Encephalitis Associated With Antibodies to Voltage-Gated Potassium Channels Dennis Chan, PhD, MRCP; Susie M. D. Henley, MA; Martin N. Rossor, MD, FRCP; Elizabeth K. Warrington, DSc, FRS Background: Encephalitis associated with antibodies test in which patients were required to identify individu- to voltage-gated potassium channels (VGKC-Ab) is char- als from the recent and remote past. acterized by epilepsy, behavioral changes, and antero- grade memory impairment. Magnetic resonance imaging Results: All 3 patients were found to have temporally reveals abnormal signal predominantly restricted to the ungraded retrograde amnesia dating back more than 20 mediotemporal lobes. years. Magnetic resonance imaging in all patients re- vealed high-signal abnormalities predominantly affect- Objective: To determine the temporal extent and po- ing the hippocampi. Subsequent testing performed after tential reversibility of retrograde amnesia in 3 patients immunotherapy revealed subjective improvement but no with VGKC-Ab–associated encephalitis. evidence of a temporal gradient in the recovery of past memories. Design: Case report. Conclusions: Encephalitis associated with VGKC-Ab re- Setting: Clinical. sults in extensive and temporally ungraded retrograde Patients: Three patients diagnosed as having VGKC- amnesia that is partially reversible with immuno- Ab–associated encephalitis underwent cognitive testing therapy. Magnetic resonance imaging high-signal abnor- before and after immunotherapy. malities were primarily restricted to the hippocampi. These data are supportive of theories postulating a role for the Main Outcome Measures: In addition to standard neu- hippocampus in the storage and retrieval of all past memo- ropsychological tests, retrograde memory was assessed ries, irrespective of age, rather than theories of memory using 2 novel tests. Memory for past newsworthy events consolidation that propose an involvement of the hip- was assessed using a public events test; test material was pocampus only in the temporary storage of memories. divided into epochs of 5 years and spanned approxi- mately 25 years. This was complemented by a famous faces Arch Neurol. 2007;64:404-410 NCEPHALOPATHY ASSOCI- Brain magnetic resonance (MR) ated with antibodies to volt- imaging typically reveals abnormally high age-gated potassium chan- signal within the mediotemporal lobes.2 nels (VGKC-Ab) is a recently Follow-up imaging (after immuno- described and potentially re- therapy) reveals partial or full resolution Author Affiliations: 1 Department of Neurology, Royal Eversible nonparaneoplastic encephalitis. of the signal abnormalities but a degree of Sussex County Hospital, Patients with VGKC-Ab–associated en- mediotemporal lobe atrophy. Brighton (Dr Chan), and cephalitis typically are initially seen with Although patients are initially seen pri- Dementia Research Centre, subacute loss of episodic memory, usually marily with impairment of anterograde Department of Clinical in association with confusion, epileptic memory, several patients in the 2 major case Neurology, Institute of seizures, neuropsychiatric symptoms, and series2,3 to date also described a loss of re- Neurology, Queen Square a syndrome of inappropriate secretion of cent and remote memories, often dating (Drs Chan, Rossor, and 2 Warrington and Ms Henley); antidiuretic hormone. Approximately 50% back several years from the time of their and Department of Neurology, of patients showed a marked response to acute illness, indicative of an additional im- Faculty of Medicine, Imperial immunotherapy with improvement in an- pairment of retrograde memory. The docu- College (Dr Rossor), London, terograde memory and cessation or reduc- mentation of retrograde amnesia is of ma- England. tion of seizures. jor theoretical interest given the particular (REPRINTED) ARCH NEUROL / VOL 64, MAR 2007 WWW.ARCHNEUROL.COM 404 ©2007 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 involvement of the hippocampus in this condition. While the hippocampus is universally acknowledged to play a criti- cal role in memory function, the extent of this role re- mains a subject of intense debate, and one of the major is- sues concerns the involvement of the hippocampus in the storage and retrieval of remote memories. This is exem- plified by the conflicting theories of hippocampal func- tion, which differ in terms of the temporal extent of the hippocampal involvement in retrograde memory. Theo- ries of memory consolidation4,5 contend that the hippo- campus acts as a temporary memory store for new memo- ries, while permanent memories are stored instead in the neocortex. Consolidation of memories over time results in a progressive transfer of memories from the hippocampus to the neocortex. Hippocampal damage is predicted to re- sult in a temporally graded loss of retrograde memory, with greater loss of more recent, less consolidated memories. Opposing theories propose that the hippocampus is involved in the storage and retrieval of past memories, irrespective of the age of the memory. Warrington and Weiskrantz6 considered the hippocampus as the point of interaction of episodic and semantic memory systems. Figure 1. T1-weighted image of patient KC1 after treatment. Given that memory for contemporary events and recall of remote events requires interaction between the 2 sys- tems, disconnection of the 2 systems resulting from hip- Initial informal questioning revealed that patient KC1 pocampal damage would disrupt retrieval of episodic had no memory of past events occurring in his personal memories independent of the age of the memories. More life or in the public domain dating back more than 10 recently, Nadel and Moscovitch7 developed the mul- years from the onset of his illness. When questioned about tiple trace theory, which posits that experiential recall news events of the prior 2 decades, he was able only to of episodic memories results in the formation of a trace, remember that Princess Diana had died and that there or pattern, of synaptic activation within the hippocam- had been a terrorist attack on the Twin Towers but was pus. Subsequent recall produces multiple traces stored unable to provide further details. within the hippocampus such that it is always involved He was treated initially in June 2002 with oral predni- in the storage and retrieval of memories regardless of the sone. He underwent a course of plasma exchange in Oc- age of the memories. Accordingly, hippocampal dam- tober 2002 but developed an anaphylactic reaction, and cor- age would also be predicted to result in the loss of re- ticosteroid therapy was recommenced. Immunotherapy cent and remote memories in the form of temporally un- resulted in a progressive decrease in the VGKC-Ab titer to graded retrograde amnesia. 453 pmol in September 2002 and to 180 pmol in March The issue of retrograde amnesia occurring in the con- 2003. Concurrent with this decrease in antibody titer, there text of VGKC-Ab–associated encephalitis is explored by was gradual subjective improvement in his episodic memory. analysis of 3 affected patients who were noted to have im- The initial 2002 brain MR imaging revealed high sig- paired retrograde memory in addition to the characteris- nal within both hippocampi with additional diffuse ce- tic clinical features of this disorder. Two of these patients rebral atrophy and associated enlargement of both lat- (patients KC1 and KC2) were included in the review ar- eral ventricles. Magnetic resonance imaging was repeated ticle by Vincent et al,3 and patient KC1 was described in a in December 2003 and in June 2004; bilateral hippocam- separate report.8 Patient KC3 is 1 of several patients de- pal atrophy was noted on the 2003 MR images, and the scribed in a separate study on spatial memory.9 2004 MR images did not reveal any change in the de- gree of diffuse cerebral atrophy or in the hippocampal atrophy (Figure 1). REPORT OF CASES PATIENT KC2 PATIENT KC1 Patient KC2 was a right-handed finance officer aged 43 Patient KC1 was a right-handed woodcarver aged 52 years years at the time of his initial presentation. He was seen at the onset of his illness. He was initially seen in Janu- in October 2001 with a 1-year history of progressive im- ary 2002 with confabulation, generalized seizures, com- pairment of episodic memory affecting at first his ability plex visual hallucinations, and impairment of episodic to recall details of important work-related events, as well memory associated with topographical disorientation. In as difficulty in remembering the names and faces of ac- April 2002, he was transferred to The National Hospital quaintances. Subsequently, he began to get lost in famil- for Neurology and Neurosurgery, London, England. The iar places. By early 2002, he started to confabulate, and initial VGKC-Ab titer was found to be 4005 pmol (ref- he became increasingly aggressive and irascible, with oc- erence range, Ͻ100 pmol). casional inappropriate behavior. (REPRINTED) ARCH NEUROL / VOL 64, MAR 2007 WWW.ARCHNEUROL.COM 405 ©2007 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 He was transferred from his local hospital to The Na- This was associated with subjective improvement in his tional Hospital for Neurology and Neurosurgery in Oc- episodic memory. tober 2002. Investigations performed at this stage in- Subsequent brain MR imaging, performed
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