
What is ALF?
Accelerated Long-term Forgetting (ALF) is a memory impairment that manifests only after several hours or days have elapsed (Elliott et al, 2014). People with ALF typically can remember experiences or things they are told for a short period, but within a day or two find they can remember almost nothing. This pattern differs from the more common pattern of gradually losing information from the time of encoding.
ALF was first noted in patients with epilepsy (Kapur et al., 1997) and particularly in those with a syndrome called Transient Epileptic Amnesia, where there are recurrent losses of all memories for a recent significant life event often independent of any overt evidence of a seizure (Butler et al., 2008). These types of memory impairments can be quite traumatic, and ALF is often linked with depression and anxiety. Some people would complain about memory problems, but clinicians could not substantiate these using traditional memory tests, with maximum delays of 30 min (Piazzini et al., 2001). Detection of ALF only became possible once more was known about the normal rate of forgetting over longer delays.
In conjunction with colleagues at Royal Prince Alfred Hospital, we established measures and normative values that would help other clinicians identify ALF (Miller et al., 2015). Now, ALF is a well-recognised potential problem, especially for some people with epilepsy. It has also been found in other types of patients, including those with Acquired Brain Injury caused by stroke (Geurts et al., 2019) or head injury (Lah et al., 2017). A small percentage of otherwise healthy people also display this phenomenon.
Associated Factors
One factor that have been shown to be associated with ALF in people with epilepsy is the appearance of abnormal electrical discharges on the EEG between seizures (i.e., “interictal discharges”) (Fitzgerald et al., 2013a for a review). Abnormal sleep patterns have also been linked with poor long-term memory (Gais and Born, 2004). Normally, the hippocampus re-plays new memories subconsciously or during sleep to form more stable representations. The re-playing function may be necessary for short term memories to be transferred to longer term storage. Thus, it seems likely that longer term stores are reduced in people with ALF, because this re-playing function is interrupted by interictal discharges and possibly the disruption of normal sleep patterns.
Also, for those with epilepsy, ALF also seems more likely to be detected in older and, interestingly, in more intelligent people (Fitzgerald et al., 2013a). Anti-seizure medication can sometimes help restore memory functioning in these patients.
Typical Cases of ALF
Case CC
When I first met CC, at the age of 64, he told me that his memory problems started 5 years earlier, when he had an abrupt episode of retrograde amnesia: CC forgot his daughter's wedding, 4 days earlier, though he had participated in it normally! One year later, there was another clear retrograde amnesic episode (he forgot his mother's recent death and funeral). These symptoms are characteristic of Transient Epileptic Amnesia. From around this time onwards, he noticed that he would rapidly forget recent life events. For example, he could have dinner with friends or see a movie and be unable to remember anything about the events a week later. This ongoing rapid forgetting was a possible sign of ALF.
CC had worked as a senior executive in several international companies. He held a Bachelor of Commerce degree and was a Chartered Accountant. He had retired at the age of 60, because of his memory problems. He subsequently developed depression.
At the time of his neuropsychology assessment, PET imaging had indicated lowered activity in both temporal lobes, but an MRI revealed no structural abnormalities. There were no indications of an autoimmune process. CC had never had a witnessed seizure, but an EEG revealed frequent abnormal discharges (mostly during sleep).
Case KG
KG was a 65 year-old man who started to experience episodes of disorientation, confusion and memory problems 10 years prior to his appointment with me. Partial epilepsy was diagnosed and he was started on anti-seizure medication. He remained on this for several years with good seizure control and a resolution in his memory problems. However, 2 years before I saw him, KG was weaned off the anti-seizure medication and the memory problems gradually returned. KG had lost all memory for a number of major life events (e.g., a family camping trip 9 months earlier). He endorsed symptoms to indicate moderate levels of anxiety and depression.
In the past, KG had completed a master’s degree and had worked as a high school teacher and manager. He was retired, but remained active in volunteer teaching and continuing education activities. With regard to his investigations, KG's MRI and PET scans were normal. An EEG at the time of this study indicated infrequent abnormal discharges in drowsiness and sleep. KG had not had any known seizures for several years.
Case PS
PS developed memory problems 18 months prior to meeting me. His wife reported that he would have poor memory for events that had occurred a few weeks earlier. Gradually, he and his wife became aware that he also had a poor memory for much of his life (e.g., he could not recall holiday trips even after being shown photographs). Several months prior to memory problems being noticed, PS had a first-ever (grand mal) seizure in his sleep. He was started on medication to prevent seizures, but he stopped taking any anti-seizure medication a few months prior to memory difficulties being noticed. PS did not experience anxiety or depression. Instead, he described being in a constant state of euphoria!
PS was 72 at the time of his appointment and had retired at the age of 61. He had a Bachelor of Commerce degree and had worked as a high-level computer consultant/programmer. He spoke three languages. His neurological tests yielded no clear underlying pathology. An EEG at the time of the study showed nothing abnormal. An MRI revealed only a benign arachnoid cyst in the left temporal lobe. An autoimmune condition was considered unlikely, and he had no other significant neurological history.
For all three men, a classic pattern of ALF was confirmed using a word list-learning test. In this test, one listens to and then recalls a 15-item word list 5 times over. Thirty minutes later, all the men were able to recall a good number of words (9-10). However, they all failed to remember any words when asked again a week later.
Things that might help people with ALF
There are several strategies that can be applied to help reduce the amount of forgetting that occurs over time. Our research indicated that if newly learned material (e.g., a story that one hears) is recalled repeatedly over days and weeks, people with ALF retain information much longer (see Ricci et al., 2019 for a description of how this technique benefitted the three men described above). For this reason, patients with ALF should be advised to try and establish routines that encourage regular recall. For example, writing in a diary at the end of each day something about the day’s events or having a short discussion with one’s partner at the end of each day about recent experiences should help with retention. Then, even if memory fails, a diary or one’s significant other can serve as an external reference or to prompt the memory. Spaced retrieval, also known as “staggered rehearsal”, is a good way to learn something new and this is likely to help those with ALF as well. This technique involves studying something new, then testing one’s own recall at increasingly longer intervals. All these strategies are covered in the memory training program offered by MEMORehab.
If sleep disturbance is an issue, adaptation of good sleep habits and hygiene (Baranwal et al., 2023) as well as consultation with a sleep expert might be helpful. Interestingly, we found that napping during the day was associated with better long-term memory (Fitzgerald et al. 2013b).
A group in Toronto have been working to create an external memory device/app called the “HippoCamera” (Martin et al., 2022) to try to help people with memory problems such as ALF. The HippoCamera app can be downloaded for free and is used to record videos of events each day along with a short description. These can later be re-played through the app for the person to view, in an attempt to replicate how the hippocampus normally reviews new memories. The usefulness of this app for people with ALF is still under investigation.
Summary
ALF is a memory impairment that can be found in patients with a variety of neurological conditions, but seems most common in those with epilepsy. It is often noted in conjunction with the syndrome known as Transient Epileptic Amnesia. Detecting ALF requires the testing of retention over long delays. Some of the factors related to ALF seem to include disrupted sleep patterns and (in patients with epilepsy) interictal discharges.
There are a number of mental strategies and external memory aids that are likely to help people with ALF retain memories longer; these are covered in MEMORehab’s program. Maximising sleep efficiency, using the HippoCamera app and taking a daytime nap might also be helpful! For those with other evidence of a seizure disorder, consultation with a neurologist about anti-seizure medication is also strongly recommended.
References
Baranwal, N., Yu, P.K., & Siegel, N.S. (2023). Sleep physiology, pathophysiology, and sleep hygiene. Progress in Cardiovascular Diseases, 77, 59-69.
Butler, C. R., & Zeman, A. Z. (2008). Recent insights into the impairment of memory in epilepsy: Transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment. Brain, 131(Pt 9), 2243-2263.
Elliott, G., Isaac, C. L., & Muhlert, N. (2014). Measuring forgetting: A critical review of accelerated long-term forgetting studies. Cortex, 54, 16–32.
Fitzgerald, Z., Mohamed, A., Ricci, M., Thayer, Z., Miller, L. (2013a). Accelerated long-term forgetting: A newly identified memory impairment in epilepsy. Journal of Clinical Neuroscience, 20, 1486-1491.
Fitzgerald, Z., Thayer, Z., Mohamed, A. and Miller, L.A. (2013b). Examining factors related to accelerated long-term forgetting in epilepsy using ambulatory EEG monitoring. Epilepsia, 54, 819-827.
Gais S, Born J. (2004) Declarative memory consolidation: mechanisms acting during human sleep. Learning and Memory,11, 679–85.
Geurts, S., van der Werf, S. P., Kwa, V. I., & Kessels, R. P. (2019). Accelerated long-term forgetting after TIA or minor stroke: A more sensitive measure for detecting subtle memory dysfunction? Cortex, 110, 150-156.
Kapur N, Millar J, Colbourn C, et al. (1997). Very long-term amnesia in association with
temporal lobe epilepsy: evidence for multiple-stage consolidation processes.
Brain and Cognition, 35, 58–70.
Lah S, Black C, Gascoigne MB, Gott C, Epps A, Parry L. (2017). Accelerated long-term forgetting is not epilepsy specific: evidence from childhood traumatic brain injury. Journal of Neurotrauma, 34(17), 2536–44.
Martin, C.B., Hong, B., Newsome, R.N., Savel, K., Meade, M.E., Xia, A., Honey, C.J., & Barense, M.D. (2022). A smartphone intervention that enhances real-world memory and promotes differentiation of hippocampal activity in older adults. Proceedings of the National Academy of Sciences, 119(51), https://doi.org/10.1073/pnas.2214285119
Miller, L.A., Flanagan, E., Mothakunnel, A., Mohamed, A. and Thayer, Z. (2015). Old dogs with new tricks: Detecting accelerated long term forgetting by extending traditional measures. Epilepsy and Behavior, 45, 205-211.
Piazzini A, Canevini MP, Maggiori G, Canger R. (2001) The perception of
memory failures in patients with epilepsy. European Journal of Neurology, 8, 613–620.
Ricci, M.,Wong, T., Nikpour, A. and Miller, L.A. (2019). Testing the effectiveness of cognitive interventions in alleviating accelerated long term forgetting (ALF). Cortex, 110, 37-46.