A contextual binding theory of episodic memory: systems consolidation reconsidered

Abstract

Episodic memory reflects the ability to recollect the temporal and spatial context of past experiences. Episodic memories depend on the hippocampus but have been proposed to undergo rapid forgetting unless consolidated during offline periods such as sleep to neocortical areas for long-term storage. Here, we propose an alternative to this standard systems consolidation theory (SSCT) - a contextual binding account - in which the hippocampus binds item-related and context-related information. We compare these accounts in light of behavioural, lesion, neuroimaging and sleep studies of episodic memory and contend that forgetting is largely due to contextual interference, episodic memory remains dependent on the hippocampus across time, contextual drift produces post-encoding activity and sleep benefits memory by reducing contextual interference.

Fig. 1 |. Contextual binding theory.

a | Contextual binding theory assumes that the hippocampus (red) is necessary for episodic memory because it binds together the item and context information that makes up the study event. The hippocampus receives information from various regions including the perirhinal cortex and the ventral ‘what’ stream, and is thought to provide information about the items in an event (e.g., objects and people), the amygdala (dotted yellow) which provides information about the emotional aspects of the event, and the parahippocampal cortex (green) which receives spatial information from the dorsal ‘where’ stream. The regions outside the hippocampus are assumed to support the learning of simple associations, and so can learn about regularities and occurrences in the environment, whereas the hippocampus is unique in supporting memory for individual episodes, and so is said to support complex or high-resolution bindings, in the sense that it links together the multiple objects and detailed contextual information that makes up an event. This approach is consistent with neurocomputational models that propose that the hippocampus supports memory via a process of pattern separation and completion^,,. b | According to the CB model, context can reflect any aspect of the study episode that links the test item to the specific study event, such as the spatial, temporal or cognitive details of that event. Some aspects of context can change quickly like moving to a new room or initiating a new cognitive task (e.g., the blue arrow), whereas other aspects of context can change gradually like changes in the subject’s mood or changes in lighting throughout the day. Because context gradually drifts, the study event will extend in time beyond the occurrence of the study items themselves. In this way, forgetting is assumed to be due to interference from other memories that share similar content or context. That is, because episodic memory requires subjects to recollect which items (i.e., snowboarder, clock, cat) occurred in a specific experimental context (i.e., the related portion of the context arrows), other episodic memories that share a similar context to the studied items (i.e., umbrella and snowman) or that have similar content (i.e., stopwatch) will interfere with memory retrieval because they are confusable and effectively compete with each other. Importantly, because forgetting is the result of contextual interference, forgetting will be produced not only by events that occur after the study event, but also by events that occur prior to the study event (i.e., top-hat and umbrella). In addition, manipulations that reduce the encoding of interfering materials, such as allowing subjects to rest or sleep, are expected to benefit memory by reducing contextual interference. Moreover, if an item is repeated (e.g., the item may be re-studied or the initial event may be remembered) it will be re-encoded along with new context information. Finally, neural activity that is related to the encoding of the study event will be temporally extended because of the gradually changing context, such that encoding related activity will linger after the nominal study event is over (i.e., re-activation), and in fact, may even be observed prior to the onset of the study event (i.e., pre-activation).

Fig. 2 |. Results that have historically been taken as evidence in support of systems consolidation theory.

a | Graded retroactive interference. Forgetting of an event is greater when subsequent interfering information is encountered shortly after encoding. Müller and Pilzecker presented subjects with nonsense syllables (represented here by letters) and tested cued recall after a 1.5 hour retention interval. Importantly, they found that if subjects were presented with additional nonsense syllables to learn shortly after the initial encoding phase (top row; left on graph), subjects recalled fewer of the initial items than if the additional nonsense syllables were presented later in the retention interval (bottom row; right on graph). The finding can be explained if the interpolated task disrupts consolidation, or if it produces more contextual interference. b | Retrograde amnesia. Amnesic patients may be, impaired at retrieving memory from recent but not remote periods (i.e., graded retrograde amnesia) - a pattern consistent with SC - but they may also be impaired at retrieving memories for both remote and recent events (i.e., flat retrograde amnesia) or they may be unimpaired for both time periods (i.e., absent retrograde amnesia). c | Reports of graded retrograde amnesia in patients with selective hippocampal damage are rare. A number of patients with selective hippocampal damage have been assessed on standard tests of retrograde amnesia^,,–. In the famous faces test, only 2 patients (i.e., patients LM and WH) out of 10 revealed evidence of graded retrograde amnesia. Similarly, in tests of memory for public events, only 4 patients (i.e. GD, LM & WH, and patient YK) out of 11 showed evidence of a temporal gradient. On the autobiographical memory interview (AMI), only one patient out of 8 (i.e., YK^,) exhibited a greater impairment for recent than remote periods. Interestingly, the authors of the lattermost study indicated that YK’s memory reports were entirely lacking in episodic details, suggesting impairments in both remote and recent autobiographical memory. Four additional patients with selective hippocampal damage were assessed on the AMI, and were unimpaired at the remote period, but the recent period results were not reported, so they are not included in this figure. Nevertheless, in a subsequent reanalysis, those patients were included with additional patients that could not be scanned and as a group they exhibited only a mild memory impairment for recent items that was limited to autobiographical memory questions and not the personal semantic memory items of the AMI. d | Retrieval related hippocampal activity for remote and recent memories. Human neuroimaging studies suggest that the hippocampus is involved in retrieving both recent and remote memories. That is, the most common finding is that the hippocampus is similarly involved during the retrieval of both remote and recent memories^–,–. A few studies reported either greater^– or less^– hippocampal activity for recent than for remote memories, whereas others reported mixed results^– such as the left hippocampus being equally involved in remote and recent memories whereas the right hippocampus was more active for recent than remote memory (the figure was based on an informal review by searching Pubmed using the search string “(remote) AND (memory) AND (hippocampus)”, as well as well as examining citations and references. These studies are characterized in more detail in supplementary Table 1). e | The effects of sleep on forgetting in episodic memory (based on Table 3 from Jenkins and Dallenbach, 1924). Subjects learned a sequence of nonsense syllables and were then tested for recall after delays varying in length from 1 to 8 hours that were filled either with sleep or wake. Compared to the awake condition, subjects who slept exhibited significantly slower forgetting rates. The finding can be explained if sleep facilitates consolidation or if it reduces the encoding of interfering information.

Fig. 2 |. Results that have historically been taken as evidence in support of systems consolidation theory.

a | Graded retroactive interference. Forgetting of an event is greater when subsequent interfering information is encountered shortly after encoding. Müller and Pilzecker presented subjects with nonsense syllables (represented here by letters) and tested cued recall after a 1.5 hour retention interval. Importantly, they found that if subjects were presented with additional nonsense syllables to learn shortly after the initial encoding phase (top row; left on graph), subjects recalled fewer of the initial items than if the additional nonsense syllables were presented later in the retention interval (bottom row; right on graph). The finding can be explained if the interpolated task disrupts consolidation, or if it produces more contextual interference. b | Retrograde amnesia. Amnesic patients may be, impaired at retrieving memory from recent but not remote periods (i.e., graded retrograde amnesia) - a pattern consistent with SC - but they may also be impaired at retrieving memories for both remote and recent events (i.e., flat retrograde amnesia) or they may be unimpaired for both time periods (i.e., absent retrograde amnesia). c | Reports of graded retrograde amnesia in patients with selective hippocampal damage are rare. A number of patients with selective hippocampal damage have been assessed on standard tests of retrograde amnesia^,,–. In the famous faces test, only 2 patients (i.e., patients LM and WH) out of 10 revealed evidence of graded retrograde amnesia. Similarly, in tests of memory for public events, only 4 patients (i.e. GD, LM & WH, and patient YK) out of 11 showed evidence of a temporal gradient. On the autobiographical memory interview (AMI), only one patient out of 8 (i.e., YK^,) exhibited a greater impairment for recent than remote periods. Interestingly, the authors of the lattermost study indicated that YK’s memory reports were entirely lacking in episodic details, suggesting impairments in both remote and recent autobiographical memory. Four additional patients with selective hippocampal damage were assessed on the AMI, and were unimpaired at the remote period, but the recent period results were not reported, so they are not included in this figure. Nevertheless, in a subsequent reanalysis, those patients were included with additional patients that could not be scanned and as a group they exhibited only a mild memory impairment for recent items that was limited to autobiographical memory questions and not the personal semantic memory items of the AMI. d | Retrieval related hippocampal activity for remote and recent memories. Human neuroimaging studies suggest that the hippocampus is involved in retrieving both recent and remote memories. That is, the most common finding is that the hippocampus is similarly involved during the retrieval of both remote and recent memories^–,–. A few studies reported either greater^– or less^– hippocampal activity for recent than for remote memories, whereas others reported mixed results^– such as the left hippocampus being equally involved in remote and recent memories whereas the right hippocampus was more active for recent than remote memory (the figure was based on an informal review by searching Pubmed using the search string “(remote) AND (memory) AND (hippocampus)”, as well as well as examining citations and references. These studies are characterized in more detail in supplementary Table 1). e | The effects of sleep on forgetting in episodic memory (based on Table 3 from Jenkins and Dallenbach, 1924). Subjects learned a sequence of nonsense syllables and were then tested for recall after delays varying in length from 1 to 8 hours that were filled either with sleep or wake. Compared to the awake condition, subjects who slept exhibited significantly slower forgetting rates. The finding can be explained if sleep facilitates consolidation or if it reduces the encoding of interfering information.