Sarah DuBrow

Resistance to forgetting associated with hippocampus-mediated reactivation during new learning

One of the reasons why we forget past experiences is because we acquire new memories in the interim. Although the hippocampus is thought to be important for acquiring and retaining memories, there is little evidence linking neural operations during new learning to the forgetting (or remembering) of earlier events. We found that, during the encoding of new memories, responses in the human hippocampus are predictive of the retention of memories for previously experienced, overlapping events. This brain-behavior relationship is evident in neural responses to individual events and in differences across individuals. We found that the hippocampus accomplishes this function by reactivating older memories as new memories are formed; in this case, reactivating neural responses that represented monetary rewards associated with older memories. These data reveal a fundamental mechanism by which the hippocampus tempers the forgetting of older memories as newer memories are acquired.

How the hippocampus preserves order: the role of prediction and context.

Remembering the sequence of events is critical for deriving meaning from our experiences and guiding behavior. Prior investigations into the function of the human hippocampus have focused on its more general role in associative binding, but recent work has focused on understanding its specific role in encoding and preserving the temporal order of experiences. In this review we summarize recent work in humans examining hippocampal contributions to sequence learning. We distinguish the learning of sequential relationships through repetition from the rapid, episodic acquisition of sequential associations. Taken together, this research begins to clarify the link between hippocampal representations and the preservation of the order of events.

Attention during Memory Retrieval Enhances Future Remembering

Memory retrieval is a powerful learning event that influences whether an experience will be remembered in the future. Although retrieval can succeed in the presence of distraction, dividing attention during retrieval may reduce the power of remembering as an encoding event. In the present experiments, participants studied pictures of objects under full attention and then engaged in item recognition and source memory retrieval under full or divided attention. Two days later, a second recognition and source recollection test assessed the impact of attention during initial retrieval on long-term retention. On this latter test, performance was superior for items that had been tested initially under full versus divided attention. More importantly, even when items were correctly recognized on the first test, divided attention reduced the likelihood of subsequent recognition on the second test. The same held true for source recollection. Additionally, foils presented during the first test were also less likely to be later recognized if they had been encountered initially under divided attention. These findings demonstrate that attentive retrieval is critical for learning through remembering.

Temporal memory is shaped by encoding stability and intervening item reactivation.

Making sense of previous experience requires remembering the order in which events unfolded in time. Prior work has implicated the hippocampus and medial temporal lobe cortex in memory for temporal information associated with individual episodes. However, the processes involved in encoding and retrieving temporal information across extended sequences is relatively poorly understood. Here we used fMRI during the encoding and retrieval of extended sequences to test specific predictions about the type of information used to resolve temporal order and the role of the hippocampus in this process. Participants studied sequences of images of celebrity faces and common objects followed by a recency discrimination test. The main conditions of interest were pairs of items that had been presented with three intervening items, half of which included an intervening category shift. During encoding, hippocampal pattern similarity across intervening items was associated with subsequent successful order memory. To test for evidence of associative retrieval, we trained a classifier to discriminate encoding patterns associated with faces versus objects and applied the classifier on fMRI patterns during recency discrimination. We found evidence that the category content of intervening items was reactivated during recency judgments, and this was related to hippocampal encoding-retrieval similarity. A follow-up behavioral priming experiment revealed additional evidence for intervening item reinstatement during temporal order judgments. Reinstatement did not differ according to whether the items occurred within a single context or across context boundaries. Thus, these data suggest that inter-item associative encoding and retrieval mediated by the hippocampus contribute to temporal order memory.

The influence of context boundaries on memory for the sequential order of events.

Episodic memory allows people to reexperience the past by recovering the sequences of events that characterize those prior experiences. Although experience is continuous, people are able to selectively retrieve and reexperience more discrete episodes from their past, raising the possibility that some elements become tightly related to each other in memory, whereas others do not. The current series of experiments was designed to ask how shifts in context during an experience influence how people remember the past. Specifically, we asked how context shifts influence the ability to remember the relative order of past events, a hallmark of episodic memory. We found that memory for the order of events was enhanced within, rather than across, context shifts, or boundaries (Experiment 1). Next, we showed that this relative enhancement in order memory was eliminated when across-item associative processing was disrupted (Experiment 2), suggesting that context shifts have a selective effect on sequential binding. Finally, we provide evidence that the act of making order memory judgments involves the reactivation of representations that bridged the tested items (Experiment 3). Together, these data suggest that boundaries may serve to parse continuous experience into sequences of contextually related events and that this organization facilitates remembering the temporal order of events that share the same context.

Temporal binding within and across events.

Remembering the order in which events occur is a fundamental component of episodic memory. However, the neural mechanisms supporting serial recall remain unclear. Behaviorally, serial recall is greater for information encountered within the same event compared to across event boundaries, raising the possibility that contextual stability may modulate the cognitive and neural processes supporting serial encoding. In the present study, we used fMRI during the encoding of consecutive face and object stimuli to elucidate the neural encoding signatures supporting subsequent serial recall behavior both within and across events. We found that univariate BOLD activation in both the middle hippocampus and left ventrolateral prefrontal cortex (PFC) was associated with subsequent serial recall of items that occur across event boundaries. By contrast, successful serial encoding within events was associated with increased functional connectivity between the hippocampus and ventromedial PFC, but not with univariate activation in these or other regions. These findings build on evidence implicating hippocampal and PFC processes in encoding temporal aspects of memory. They further suggest that these encoding processes are influenced by whether binding occurs within a stable context or bridges two adjacent but distinct events.

Deconstructing the effect of self-directed study on episodic memory

Self-directed learning is often associated with better long-term memory retention; however, the mechanisms that underlie this advantage remain poorly understood. This series of experiments was designed to “deconstruct” the notion of self-directed learning, in order to better identify the factors most responsible for these improvements to memory. In particular, we isolated the memory advantage that comes from controlling the content of study episodes from the advantage that comes from controlling the timing of those episodes. Across four experiments, self-directed learning significantly enhanced recognition memory, relative to passive observation. However, the advantage for self-directed learning was found to be present even under extremely minimal conditions of volitional control (simply pressing a button when a participant was ready to advance to the next item). Our results suggest that improvements to memory following self-directed encoding may be related to the ability to coordinate stimulus presentation with the learner’s current preparatory or attentional state, and they highlight the need to consider the range of cognitive control processes involved in and influenced by self-directed study.

Commentary: Distinct neural mechanisms for remembering when an event occurred

Citation: DuBrow S and Davachi L (2017) Commentary: Distinct neural mechanisms for remembering when an event occurred. Memory for the relative order of events is a critical feature of episodic remembering that is thought to rely on hippocampal processes (Eichenbaum, 2013; Davachi and DuBrow, 2015). However, there are multiple ways in which the hippocampus may support order memory. Here, we review a recent fMRI paper by Jenkins and Ranganath (2016) investigating two potential memory mechanisms that may support recency discrimination. To briefly summarize, participants were scanned while encoding sequences of object images and were subsequently tested on which of two objects had been presented more recently. The authors examined neural patterns during encoding that predicted later recency judgments and found evidence that item strength and context differentiation support order memory. Our goal here is to provide a theoretical perspective on these and related findings to highlight how numerous mechanisms may support order memory and how fMRI can be leveraged to test competing theories. Perhaps the most intuitive way to evaluate the order of two items is to compare how strong they are in memory. Since memory strength decays over time, an items current strength can provide an estimate of how much time passed since it was encountered (Hinrichs, 1970). To determine which of two items occurred more recently, one strategy might be to simply select the one that has the higher activation strength (Hintzman, 2005, c.f. Hintzman, 2010). Jenkins and Ranganath (2016) found evidence in line with a strength-based temporal representation in the prefrontal (PFC) and medial temporal lobe cortices including the perirhinal cortex, which has been consistently implicated in encoding item strength Specifically, these regions showed greater activation during the initial encoding of items later endorsed as more recent regardless of their true temporal position. While these results are consistent an item-strength comparison account of recency judgments, an alternative retrieval process called scanning could show similar effects at encoding. Backwards scanning models propose that memoranda are sequentially sampled from the end until reaching an item with a sufficient match to one of the recency probes (Hacker, 1980; Howard et al., 2015). Thus, if the more recent item was not encoded strongly enough, it could be bypassed in favor of the stronger, earlier item, consistent with the findings of Jenkins and Ranganath. Another possibility is that recency judgments could be supported by a comparison of the contexts associated with the …

Does mental context drift or shift

Theories of episodic memory have generally proposed that individual memory traces are linked together by a representation of context that drifts slowly over time. Recent data challenge the notion that contextual drift is always slow and passive. In particular, changes in ones external environment or internal model induce discontinuities in memory that are reflected in sudden changes in neural activity, suggesting that context can shift abruptly. Furthermore, context change effects are sensitive to top-down goals, suggesting that contextual drift may be an active process. These findings call for revising models of the role of context in memory, in order to account for abrupt contextual shifts and the controllable nature of context change.

Differential patterns of contextual organization of memory in first-episode psychosis

Contextual information is used to support and organize episodic memory. Prior research has reliably shown memory deficits in psychosis; however, little research has characterized how this population uses contextual information during memory recall. We employed an approach founded in a computational framework of free recall to quantify how individuals with first episode of psychosis (FEP, N = 97) and controls (CON, N = 55) use temporal and semantic context to organize memory recall. Free recall was characterized using the Hopkins Verbal Learning Test-Revised (HVLT-R). We compared FEP and CON on three measures of free recall: proportion recalled, temporal clustering, and semantic clustering. Measures of temporal/semantic clustering quantified how individuals use contextual information to organize memory recall. We also assessed to what extent these measures relate to antipsychotic use and differentiated between different types of psychosis. We also explored the relationship between these measures and intelligence. In comparison to CON, FEP had reduced recall and less temporal clustering during free recall (p < 0.05, Bonferroni-corrected), and showed a trend towards greater semantic clustering (p = 0.10, Bonferroni-corrected). Within FEP, antipsychotic use and diagnoses did not differentiate between free recall accuracy or contextual organization of memory. IQ was related to free recall accuracy, but not the use of contextual information during recall in either group (p < 0.05, Bonferroni-corrected). These results show that in addition to deficits in memory recall, FEP differed in how they organize memories compared to CON.Psychosis: Memory deficits in first-episode patientsFirst-episode psychosis patients exhibit impaired memory recall and deviation in how context is used to support recall ability. A US team of researchers led by the University of Pittsburgh’s Vishnu Murty examined how FEP affects an individual’s ability to organize memory based on context, by noting how well patients could recall words from a spoken list. Alongside recollection accuracy, Murty’s team assesed participant ability to recall words said proximally in sequence, and the ability to recall words from the same category—measuring ‘temporal clustering’ and ‘semantic clustering.’ The researchers found that patients with FEP had reduced recall ability and less temporal clustering. Recall accuracy and IQ were also found to be related. This study increases knowledge of FEP-related cognitive changes and could help to target specific therapies.