Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats

The positive impact of sleep on memory consolidation has been shown for human subjects in numerous studies, but there is still sparse knowledge on this topic in rats, one of the most prominent model species in neuroscience research. Here, we examined the role of sleep in the object-place recognition task, a task closely comparable to tasks typically applied for testing human declarative memory: It is a one-trial task, hippocampus-dependent, not stressful and can be repeated within the same animal. A test session consisted of the Sample trial, followed by a 2-h retention interval and a Test trial, the latter examining the memory the rat had for the places of two objects presented at the Sample trial. In Experiment 1, each rat was tested twice, with the retention interval taking place either in the morning or evening, i.e., in the inactive or active phase, respectively. Rats showed significantly (p<0.01) better memory for object place after the Morning session. To control for confounding circadian factors, in Experiment 2 rats were tested four times, i.e., in the morning or in the evening while sleep was or was not deprived. Sleep during the retention interval was recorded polysomnographically. Rats only showed significant memory for the target object place in the Test trial after the Morning retention interval in the absence of sleep deprivation, and recognition performance in this condition was significantly superior to that in the three other conditions (p<0.05). EEG recordings during spontaneous morning sleep revealed increased slow oscillation (0.85-2.0 Hz) and upper delta (2.0-4.0 Hz), but reduced spindle band (10.5-13.5 Hz) activity, as compared to evening sleep. However, spindle band power was increased in the Morning retention interval in comparison to a Morning Baseline period (p<0.05). We conclude that consolidation of object-place memory depends on sleep, and presumably requires NonREM sleep rich in both slow wave and spindle activity.     

Slow wave sleep and recollection in recognition memory

Recognition memory performance reflects two distinct memory processes: a conscious process of recollection, which allows remembering specific details of a previous event, and familiarity, which emerges in the absence of any conscious information about the context in which the event occurred. Slow wave sleep (SWS) and rapid eye movement (REM) sleep are differentially involved in the consolidation of different types of memory. The study assessed the effects of SWS and REM sleep on recollection, by means of the "remember"/"know" paradigm. Subjects studied three blocks of 12 words before a 3-h retention interval filled with SWS, REM sleep or wakefulness, placed between 3 a.m. and 6 a.m. Afterwards, recognition and recollection were tested. Recollection was higher after a retention interval rich in SWS than after a retention interval rich in REM sleep or filled with wakefulness. The results suggest that SWS facilitates the process of recollection in recognition memory.     

Illusory recollection and dual-process models of recognition memory

Higham and Vokey (2000, Exps.1 & 3)demonstrated that a slight increase in the display duration of a briefly presented word prior to displaying it in the clear for a recognition response increased the bias to respond “old”. In the current research, three experiments investigated the phenomenology associated with this illusion of memory using the standard remember-know procedure and a new, independent-scales methodology. Contrary to expectations based on the fluency heuristic, which predicts effects of display duration on subjective familiarity only, the results indicated that the illusion was reported as both familiarity and recollection. Furthermore, manipulations of prime duration induced reports of false recollection in all experiments. The results—in particular, the implications of illusory recollection—are discussed in terms of dual-process, fuzzy-trace, two-criteria signal detection models and attribution models of recognition memory.     

Novelty effects on recollection and familiarity in recognition memory

Recognition memory is better for novel or distinctive items than for non-novel items. However, it is not known whether these effects reflect changes in recollection or in familiarity-based recognition judgments. Some previous results have indicated that recollection should be more sensitive to novelty than to familiarity, whereas other results have suggested the opposite. We used avon Restorff paradigm in which a small proportion of studied items were made novel by presenting them in a color different from that of the majority of the study items. Memory was tested using a remember-know procedure. Across two experiments, stimulus novelty was found to benefit both recollection and familiarity. The effects on familiarity were observed under intentional and incidental encoding conditions, whereas the effects on recollection were significantly reduced, and no longer significant, under incidental as compared with intentional encoding conditions. Thus, both processes benefit from stimulus novelty, but the extent to which recollection benefits from novelty depends on the encoding condition.     

Revisiting the role of recollection in item versus forced-choice recognition memory

Many memory theorists have assumed that forced-choice recognition tests can rely more on familiarity, whereas item (yes-no) tests must rely more on recollection. In actuality, several studies have found no differences in the contributions of recollection and familiarity underlying the two different test formats. Using word frequency to manipulate stimulus characteristics, the present study demonstrated that the contributions of recollection to item versus forced-choice tests is variable. Low word frequency resulted in significantly more recollection in an item test than did a forced-choice procedure, but high word frequency produced the opposite result. These results clearly constrain any uniform claim about the degree to which recollection supports responding in item versus forced-choice tests.     

Context effects in recognition memory: the role of familiarity and recollection

A variant of the process dissociation procedure was coupled with a manipulation of response signal lag to assess whether manipulations of context affect one or both of the familiarity and search processes described by the dual process model of recognition. Participants studied a list of word pairs (context+target) followed by a recognition test with target words presented in the same or different context, and in the same or different form as study (singular/plural). Participants were asked to recognize any target word regardless of changes to form (inclusion), or to only recognise words that were presented in the same form (exclusion). The standard context reinstatement effect was evident even at the short response lags. Analyses of the estimates of the contributions of familiarity and search processes suggest that the context effect demonstrated here can be attributed in part to the influence of familiarity on recognition, whereas the effect on recollection was less clear.     

Individual differences in forced-choice recognition memory: Partitioning contributions of recollection and familiarity

In forced-choice recognition memory, two different testing formats are possible under conditions of high target–foil similarity: Each target can be presented alongside foils similar to itself (forced-choice corresponding; FCC), or alongside foils similar to other targets (forced-choice noncorresponding; FCNC). Recent behavioural and neuropsychological studies suggest that FCC performance can be supported by familiarity whereas FCNC performance is supported primarily by recollection. In this paper, we corroborate this finding from an individual differences perspective. A group of older adults were given a test of FCC and FCNC recognition for object pictures, as well as standardized tests of recall, recognition, and IQ. Recall measures were found to predict FCNC, but not FCC performance, consistent with a critical role for recollection in FCNC only. After the common influence of recall was removed, standardized tests of recognition predicted FCC, but not FCNC performance. This is consistent with a contribution of only familiarity in FCC. Simulations show that a two-process model, where familiarity and recollection make separate contributions to recognition, is 10 times more likely to give these results than a single-process model. This evidence highlights the importance of recognition memory test design when examining the involvement of recollection and familiarity.     

Sleep preferentially enhances memory for emotional components of scenes

ABSTRACT— Central aspects of emotional experiences are often well remembered at the expense of background details. Previous studies of such memory trade-offs have focused on memory after brief delays, but little is known about how these components of emotional memories change over time. We investigated the evolution of memory for negative scenes across 30 min, 12 daytime hours spent awake, and 12 nighttime hours including sleep. After 30 min, negative objects were well remembered at the expense of information about their backgrounds. Time spent awake led to forgetting of the entire negative scene, with memories of objects and their backgrounds decaying at similar rates. Sleep, in contrast, led to a preservation of memories of negative objects, but not their backgrounds, a result suggesting that the two components undergo differential processing during sleep. Memory for a negative scene develops differentially across time delays containing sleep and wake, with sleep selectively consolidating those aspects of memory that are of greatest value to the organism.     

Developmental patterns in priming and familiarity in explicit recollection

Developmental trajectories of two classes of human memory, implicit and explicit memory, appear to diverge. We examined how developmental differences in perceptual and conceptual priming, two types of implicit memory, coincide with differences between familiarity and recollective responses on explicit memory tests that employ the Remember/Know paradigm ( Tulving, 1985 ). Both types of priming were characterized by developmental invariance in 52 children and adolescents ages 8-19 years. Contrary to Komatsu, Naito, and Fuke (1996) results, few age-group differences in perceptual priming were observed following a levels-of-processing encoding manipulation. In contrast, age group differences were found for "Remember" but not "Know" responses. Neither levels of awareness nor strategies influenced priming. Adult levels of performance appear earlier in development on perceptual and conceptual priming tests compared to explicit memory tests. Similar developmental dissociations exist between explicit and implicit memory performance as between "Remember" and "Know" recollective responses.     

The contribution of recollection and familiarity to recognition memory performance in chronic pain patients

This study examines the selective impact of chronic pain on memory functioning in a recognition task. Thirty chronic pain patients and 30 healthy control subjects performed a yes-no word recognition test. The contribution of recollection and familiarity to both groups' performance was compared by means of the Remember/Know (R/K) procedure, which distinguishes recognition based on the recollection of the encoding episode (R responses) and recognition accompanied by a feeling of familiarity (K responses). Chronic pain patients showed a decrease in recollection together with an increase in familiarity: indeed, they reported less R and more K responses than control subjects. This pattern of performance was not related to the overall recognition ability. These findings are consistent with the hypothesis of the attentional cost of chronic pain, suggesting a selective impact of chronic pain on the most attention-demanding cognitive processes, such as recollection. This study emphasises the relevance of specific procedures distinguishing the underlying components of memory functioning rather than solely global indicators.     

Conjoint recognition and phantom recollection

A new methodology for measuring illusory conscious experience of the "presentation" of unstudied material (phantom recollection) is evaluated that extracts measurements directly from recognition responses, rather than indirectly from introspective reports. Application of this methodology in the Deese-Roediger-McDermott (DRM) paradigm (Experiments 1 and 2) and in a more conventional paradigm (Experiment 3) showed that 2 processes (phantom recollection and familiarity) contribute to false recognition of semantically related distractors. Phantom recollection was the larger contributor to false recognition of critical distractors in the DRM paradigm, but surprisingly, it was also the larger contributor to false recognition of other types of distractors. Variability in false recognition was tied to variability in phantom recollection. Experimental control of phantom recollection was achieved with manipulations that were motivated by fuzzy-trace theory's hypothesis that the phenomenon is gist-based.     

Conjunction error rates on a continuous recognition memory test: little evidence for recollection

Two experiments examined conjunction memory errors on a continuous recognition task where the lag between parent words (e.g., blackmail, jailbird) and later conjunction lures (blackbird) was manipulated. In Experiment 1, contrary to expectations, the conjunction error rate was highest at the shortest lag (1 word) and decreased as the lag increased. In Experiment 2 the conjunction error rate increased significantly from a 0- to a 1-word lag, then decreased slightly from a 1- to a 5-word lag. The results provide mixed support for simple familiarity and dual-process accounts of recognition. Paradoxically, searching for an item in memory does not appear to be a good encoding task.     

ROC in animals: Uncovering the neural substrates of recollection and familiarity in episodic recognition memory

It is a consensus that familiarity and recollection contribute to episodic recognition memory. However, it remains controversial whether familiarity and recollection are qualitatively distinct processes supported by different brain regions, or whether they reflect different strengths of the same process and share the same support. In this review, I discuss how adapting standard human recognition memory paradigms to rats, performing circumscribed brain lesions and using receiver operating characteristic (ROC) methods contributed to solve this controversy. First, I describe the validation of the animal ROC paradigms and report evidence that familiarity and recollection are distinct processes in intact rats. Second, I report results from rats with hippocampal dysfunction which confirm this finding and lead to the conclusion that the hippocampus supports recollection but not familiarity. Finally, I describe a recent study focusing on the medial entorhinal cortex (MEC) that investigates the contribution of areas upstream of the hippocampus to recollection and familiarity.     

Dissociating familiarity from recollection in human recognition memory: Different rates of forgetting over short retention intervals

Two functionally distinct forms of recognition memory have been identified in human and nonhuman species—the ability to recollect qualitative information about previous events, and the ability to differentiate between familiar and novel stimuli. Separate dual-process theories have been developed in the animal and human literatures to account for these findings. However, it is not clear whether these theories describe the same two underlying memory processes. On the basis of animal studies of medial temporal lobe function, familiarity is expected to exhibit disproportionately fast forgetting compared with recollection over short retention intervals. We tested this prediction in healthy human subjects by examining recognition forgetting rates across a range of 8–32 intervening items and found significant forgetting in the accuracy of familiarity-based discriminations and no evidence of forgetting in the accuracy of recollection-based discriminations. In agreement with the results from nonhuman species, the present results indicate that item familiarity decreases more rapidly than recollection over short retention intervals.     

Familiarity and recollection in item and associative recognition

Recognition memory for item information (single words) and associative information (word pairs) was tested immediately and after retention intervals of 30 min and 1 day (Experiment 1) and 2 days and 7 days (Experiment 2) using Tulving's (1985) remember/know response procedure. Associative recognition decisions were accompanied by more "remember" responses and less "know" responses than item recognition decisions. Overall recognition performance and the proportion of remember responses declined at similar rates for item and associative information. The pattern of results for item recognition was consistent with Donaldson's (1996) single-factor signal detection model of remember/know responses, as comparisons based on A' between overall item recognition and remember item recognition showed no significant differences. For associative recognition, however, A' for remember responses was reliably greater than for overall recognition. The results show that recollection plays a significant role in associative recognition.     

Self-referencing enhances recollection in both young and older adults

Processing information in relation to the self enhances subsequent item recognition in both young and older adults and further enhances recollection at least in the young. Because older adults experience recollection memory deficits, it is unknown whether self-referencing improves recollection in older adults. We examined recollection benefits from self-referential encoding in older and younger adults and further examined the quality and quantity of episodic details facilitated by self-referencing. We further investigated the influence of valence on recollection, given prior findings of age group differences in emotional memory (i.e., “positivity effects”). Across the two experiments, young and older adults processed positive and negative adjectives either for self-relevance or for semantic meaning. We found that self-referencing, relative to semantic encoding, increased recollection memory in both age groups. In Experiment 1, both groups remembered proportionally more negative than positive items when adjectives were processed semantically; however, when adjectives were processed self-referentially, both groups exhibited evidence of better recollection for the positive items, inconsistent with a positivity effect in aging. In Experiment 2, both groups reported more episodic details associated with recollected items, as measured by a memory characteristic questionnaire, for the self-reference relative to the semantic condition. Overall, these data suggest that self-referencing leads to detail-rich memory representations reflected in higher rates of recollection across age.     

Robust recollection rejection in the memory conjunction paradigm

The present research provides compelling evidence for recollection rejection in the memory conjunction paradigm. In Experiment 1, warnings provided at time of test were shown to reduce memory conjunction errors. Moreover, the authors found substantial evidence of recollection rejection and phantom recollection. In Experiment 2, the authors manipulated how often study items were presented. Participants were told that they could earn a cash payoff for being accurate. Recognition of conjunction lures was lower in the multiple presentation condition. However, the payoff manipulation did not significantly interact with item type. The authors obtained evidence of robust recollection rejection from 3 different dependent measures. Consistent with Experiment 1, they also found evidence of phantom recollection. These findings provide evidence that recollection rejection can be quite robust in the memory conjunction paradigm.     

Familiarity and recollection in fictitious face recognition: implications for recognition models

Using the paradigm, participants were engaged in a fictitious face recognition experiment in which three between-subject conditions were manipulated by either adding or not adding wrinkles on the faces between the study and the recognition tasks (no change, single change, double change). Our hypothesis was that this procedure would maximize judgments based on familiarity, thus determining whether data provided better fit to the models based on the signal detection theory or to predictions of dual models. In global terms, our results support the signal detection model predictions, although we discuss whether these models better fit tasks based on familiarity or tasks based on recollection.     

Aging selectively impairs recollection in recognition memory for pictures: evidence from modeling and receiver operating characteristic curves

Young and older adults were tested on recognition memory for pictures. The Yonelinas high threshold (YHT) model, a formal implementation of 2-process theory, fit the response distribution data of both young and older adults significantly better than a normal unequal variance signal-detection model. Consistent with this finding, nonlinear z-transformed receiver operating characteristic curves were obtained for both groups. Estimates of recollection from the YHT model were significantly higher for young than for older adults. This deficit was not a consequence of a general decline in memory; older adults showed comparable overall accuracy and in fact a nonsignificant increase in their familiarity scores. Implications of these results for theories of recognition memory and the mnemonic deficit associated with aging are discussed.     

Post-training reversible inactivation of the hippocampus enhances novel object recognition memory

Research on the role of the hippocampus in object recognition memory has produced conflicting results. Previous studies have used permanent hippocampal lesions to assess the requirement for the hippocampus in the object recognition task. However, permanent hippocampal lesions may impact performance through effects on processes besides memory consolidation including acquisition, retrieval, and performance. To overcome this limitation, we used an intrahippocampal injection of the GABA agonist muscimol to reversibly inactivate the hippocampus immediately after training mice in two versions of an object recognition task. We found that the inactivation of the dorsal hippocampus after training impairs object-place recognition memory but enhances novel object recognition (NOR) memory. However, inactivation of the dorsal hippocampus after repeated exposure to the training context did not affect object recognition memory. Our findings suggest that object recognition memory formation does not require the hippocampus and, moreover, that activity in the hippocampus can interfere with the consolidation of object recognition memory when object information encoding occurs in an unfamiliar environment.The medial temporal lobe plays an important role in recognition memory formation, as damage to this brain structure in humans, monkeys, and rodents impairs performance in recognition memory tasks (for review, see Squire et al. 2007). Within the medial temporal lobe, studies have consistently demonstrated that the perirhinal cortex is involved in this form of memory (Brown and Aggleton 2001; Winters and Bussey 2005; Winters et al. 2007, 2008; Balderas et al. 2008). In contrast, the role of the hippocampus in object recognition memory remains a source of debate. Some studies have reported novel object recognition (NOR) impairments in animals with hippocampal lesions (Clark et al. 2000; Broadbent et al. 2004, 2010), yet others have reported no impairments (Winters et al. 2004; Good et al. 2007). Differences in hippocampal lesion size and behavioral procedures among the different studies have been implicated as the source of discrepancy in these findings (Ainge et al. 2006), but previous studies have not examined the consequences of environment familiarity on the hippocampus dependence of object recognition memory.Previous studies addressing the role of the hippocampus in recognition memory relied on permanent, pre-training lesions (Clark et al. 2000; Broadbent et al. 2004; Winters et al. 2004; Good et al. 2007). Permanent lesions inactivate the hippocampus not only during the consolidation phase, but also during habituation, acquisition, and memory retrieval, potentially confounding interpretation of the results. Furthermore, permanent lesion studies require long surgery recovery times during which extrahippocampal changes may emerge to mask or compensate for the loss of hippocampal function. To overcome these problems, we reversibly inactivated the dorsal hippocampus after training mice in two versions of the object recognition task. We infused muscimol, a γ-aminobutyric acid (GABA) receptor type A agonist, into the dorsal hippocampus immediately after training in an object-place recognition task or immediately following training in a NOR task. Consistent with previous studies (Save et al. 1992; Galani et al. 1998; Mumby et al. 2002; Stupien et al. 2003; Aggleton and Brown 2005), we observed that hippocampal inactivation impairs object-place recognition memory. Interestingly, we observed that the degree of contextual familiarity can influence NOR memory formation. We found that when shorter periods of habituation to the experimental environment were used, hippocampal inactivation enhances long-term NOR memory. In contrast, after extended periods of contextual habituation, long-term recognition memory was unaltered by hippocampal inactivation. Together these results suggest that if familiarization with objects occurs at a stage in which the contextual environment is relatively novel, the hippocampus plays an inhibitory role on the consolidation of object recognition memory. Supporting this view, we observed that object recognition memory is unaffected by hippocampal inactivation when initial exploration of the objects occurred in a familiar environment.