Mariam Aly

Recollection and Familiarity: Examining Controversial Assumptions and New Directions

It is well accepted that recognition memory reflects the contribution of two separable memory retrieval processes, namely recollection and familiarity. However, fundamental questions remain regarding the functional nature and neural substrates of these processes. In this article, we describe a simple quantitative model of recognition memory (i.e., the dual‐process signal detection model) that has been useful in integrating findings from a broad range of cognitive studies, and that is now being applied in a growing number of neuroscientific investigations of memory. The model makes several strong assumptions about the behavioral nature and neural substrates of recollection and familiarity. A review of the literature indicates that these assumptions are generally well supported, but that there are clear boundary conditions in which these assumptions break down. We argue that these findings provide important insights into the operation of the processes underlying recognition. Finally, we consider how the dual‐process approach relates to recent neuroanatomical and computational models and how it might be integrated with recent findings concerning the role of medial temporal lobe regions in other cognitive functions such as novelty detection, perception, implicit memory and short‐term memory.

The effects of sleep on episodic memory in older and younger adults

Evidence on sleep-dependent benefits for episodic memory remains elusive. Furthermore we know little about age-related changes on the effects of sleep on episodic memory. The study we report is the first to compare the effects of sleep on episodic memories in younger and older adults. Memories of stories and personal events were assessed following a retention interval that included sleep and following an equal duration of wakefulness. Both older and younger adults have superior memory following sleep compared to following wakefulness for both types of material. Amount of forgetting of personal events was less during wakefulness in older adults than in younger adults, possibly due to spontaneous rehearsal. Amount of time spent sleeping correlated highly with sleep benefit in older adults, suggesting that quantity of total sleep, and/or time spent in some stages of sleep, are important contributors to age-related differences in memory consolidation or protection from interference during sleep.

Detecting changes in scenes: The hippocampus is critical for strength-based perception

Recent findings have ignited a controversy over whether the hippocampus is critical for visual perception as well as memory. Some studies have shown that hippocampal damage impairs perception of scenes, but others found no evidence for hippocampal involvement. These studies measured perception as a unitary phenomenon, but recent findings indicate that perceptual discriminations can be based on two kinds of information: states of perceiving local differences or global strength of relational match. In the current study, we separated state- and strength-based perception using a change detection paradigm with scenes. Patients with selective hippocampal damage exhibited significant reductions in strength-based perception but showed spared state-based responses. In a follow-up neuroimaging study, hippocampal activation linearly tracked confidence in strength-based perception, and was not differentially associated with state-based responses. The hippocampus therefore plays a selective role in perception, contributing high-resolution strength information possibly through its role in the representation of relational information.

Bridging consciousness and cognition in memory and perception: evidence for both state and strength processes.

Subjective experience indicates that mental states are discrete, in the sense that memories and perceptions readily come to mind in some cases, but are entirely unavailable to awareness in others. However, a long history of psychophysical research has indicated that the discrete nature of mental states is largely epiphenomenal and that mental processes vary continuously in strength. We used a novel combination of behavioral methodologies to examine the processes underlying perception of complex images: (1) analysis of receiver operating characteristics (ROCs), (2) a modification of the change-detection flicker paradigm, and (3) subjective reports of conscious experience. These methods yielded converging results showing that perceptual judgments reflect the combined, yet functionally independent, contributions of two processes available to conscious experience: a state process of conscious perception and a strength process of knowing; processes that correspond to recollection and familiarity in long-term memory. In addition, insights from the perception experiments led to the discovery of a new recollection phenomenon in a long-term memory change detection paradigm. The apparent incompatibility between subjective experience and theories of cognition can be understood within a unified state-strength framework that links consciousness to cognition across the domains of perception and memory.

Attention promotes episodic encoding by stabilizing hippocampal representations

Significance Why does the brain store memories of some things but not others? At a cognitive level, attention provides an explanation: What aspects of an experience we focus on determines what information is perceived and available for encoding. But the mechanism of how attention alters memory formation at the neural level is unknown. With high-resolution neuroimaging, we show that attention alters the state of a key brain structure for memory, the hippocampus, and that the extent to which this occurs predicts whether the attended information gets stored in memory. The dependence of hippocampal encoding on attentional states reveals the broad involvement of the hippocampus in multiple cognitive processes, and highlights that the workings of the hippocampus are under our control. Attention influences what is later remembered, but little is known about how this occurs in the brain. We hypothesized that behavioral goals modulate the attentional state of the hippocampus to prioritize goal-relevant aspects of experience for encoding. Participants viewed rooms with paintings, attending to room layouts or painting styles on different trials during high-resolution functional MRI. We identified template activity patterns in each hippocampal subfield that corresponded to the attentional state induced by each task. Participants then incidentally encoded new rooms with art while attending to the layout or painting style, and memory was subsequently tested. We found that when task-relevant information was better remembered, the hippocampus was more likely to have been in the correct attentional state during encoding. This effect was specific to the hippocampus, and not found in medial temporal lobe cortex, category-selective areas of the visual system, or elsewhere in the brain. These findings provide mechanistic insight into how attention transforms percepts into memories.

Damage to the lateral prefrontal cortex impairs familiarity but not recollection

Frontal lobe lesions impair recognition memory but it is unclear whether the deficits arise from impaired recollection, impaired familiarity, or both. In the current study, recognition memory for verbal materials was examined in patients with damage to the left or right lateral prefrontal cortex. Words were incidentally encoded under semantic or phonological orienting conditions, and recognition memory was tested using a 6-point confidence procedure. Receiver operating characteristics (ROCs) were examined in order to measure the contributions of recollection and familiarity to recognition memory. In both encoding conditions, lateral prefrontal cortex damage led to a deficit in familiarity but not recollection. Similar deficits were observed in left and right hemisphere patients. The results indicate that the lateral prefrontal cortex plays a critical role in the monitoring or decision processes required for accurate familiarity-based recognition responses.

Faces are special but not too special: Spared face recognition in amnesia is based on familiarity

Most current theories of human memory are material-general in the sense that they assume that the medial temporal lobe (MTL) is important for retrieving the details of prior events, regardless of the specific type of materials. Recent studies of amnesia have challenged the material-general assumption by suggesting that the MTL may be necessary for remembering words, but is not involved in remembering faces. We examined recognition memory for faces and words in a group of amnesic patients, which included hypoxic patients and patients with extensive left or right MTL lesions. Recognition confidence judgments were used to plot receiver operating characteristics (ROCs) in order to more fully quantify recognition performance and to estimate the contributions of recollection and familiarity. Consistent with the extant literature, an analysis of overall recognition accuracy showed that the patients were impaired at word memory but had spared face memory. However, the ROC analysis indicated that the patients were generally impaired at high confidence recognition responses for faces and words, and they exhibited significant recollection impairments for both types of materials. Familiarity for faces was preserved in all patients, but extensive left MTL damage impaired familiarity for words. These results show that face recognition may appear to be spared because performance tends to rely heavily on familiarity, a process that is relatively well preserved in amnesia. In addition, the findings challenge material-general theories of memory, and suggest that both material and process are important determinants of memory performance in amnesia.

Neurocomputational account of memory and perception: Thresholded and graded signals in the hippocampus

Recent evidence suggests that the hippocampus, a region critical for long‐term memory, also supports certain forms of high‐level visual perception. A seemingly paradoxical finding is that, unlike the thresholded hippocampal signals associated with memory, the hippocampus produces graded, strength‐based signals in perception. This article tests a neurocomputational model of the hippocampus, based on the complementary learning systems framework, to determine if the same model can account for both memory and perception, and whether it produces the appropriate thresholded and strength‐based signals in these two types of tasks. The simulations showed that the hippocampus, and most prominently the CA1 subfield, produced graded signals when required to discriminate between highly similar stimuli in a perception task, but generated thresholded patterns of activity in recognition memory. A threshold was observed in recognition memory because pattern completion occurred for only some trials and completely failed to occur for others; conversely, in perception, pattern completion always occurred because of the high degree of item similarity. These results offer a neurocomputational account of the distinct hippocampal signals associated with perception and memory, and are broadly consistent with proposals that CA1 functions as a comparator of expected versus perceived events. We conclude that the hippocampal computations required for high‐level perceptual discrimination are congruous with current neurocomputational models that account for recognition memory, and fit neatly into a broader description of the role of the hippocampus for the processing of complex relational information.

Examining the Causes of Memory Strength Variability: Recollection, Attention Failure, or Encoding Variability?

A prominent finding in recognition memory is that studied items are associated with more variability in memory strength than new items. Here, we test 3 competing theories for why this occurs-the encoding variability, attention failure, and recollection accounts. Distinguishing among these theories is critical because each provides a fundamentally different account of the processes underlying recognition memory. The encoding variability and attention failure accounts propose that old item variance will be unaffected by retrieval manipulations because the processes producing this effect are ascribed to encoding. The recollection account predicts that both encoding and retrieval manipulations that preferentially affect recollection will affect memory variability. These contrasting predictions were tested by examining the effect of response speeding (Experiment 1), dividing attention at retrieval (Experiment 2), context reinstatement (Experiment 3), and increased test delay (Experiment 4) on recognition performance. The results of all 4 experiments confirm the predictions of the recollection account and are inconsistent with the encoding variability account. The evidence supporting the attention failure account is mixed, with 2 of the 4 experiments confirming the account and 2 disconfirming the account. These results indicate that encoding variability and attention failure are insufficient accounts of memory variance and provide support for the recollection account. Several alternative theoretical accounts of the results are also considered.

How Hippocampal Memory Shapes, and Is Shaped by, Attention

Attention has historically been studied in the context of sensory systems, with the aim of understanding how information in the environment affects the deployment of attention and how attention in turn affects the perception of this information. More recently, there has been burgeoning interest in how long-term memory can serve as a cue for attention, and ways in which attention influences long-term memory encoding and retrieval. In this chapter, we highlight this emerging body of human behavioral, neuroimaging, and neuropsychological work that elucidates these bidirectional interactions between attention and memory. Special emphasis will be given to recent findings on how the quintessential “memory system” in the brain—the hippocampus—influences and is influenced by attention.