Recognition memory and the hippocampus: A test of the hippocampal contribution to recollection and familiarity

It has been suggested that the hippocampus selectively supports recollection and that adjacent cortex in the medial temporal lobe can support familiarity. Alternatively, it has been suggested that the hippocampus supports both recollection and familiarity. We tested these suggestions by assessing the performance of patients with hippocampal lesions on recognition memory tests that differ in the extent to which recollection and familiarity contribute to the recognition decision. When targets and foils are highly similar, prior evidence suggests that, on a forced-choice test in which targets are presented together with highly similar, corresponding foils (the FC-C format), performance is supported primarily by familiarity. By contrast, when targets are presented together with foils that are similar to other targets (the FC-NC format) or when memory is tested in a yes/no (Y/N) format, performance is based much more strongly on recollection. Accordingly, a finding that hippocampal damage impaired both Y/N recognition and FC-NC recognition but spared FC-C recognition would suggest that the hippocampus selectively supports recollection. We administered Y/N, FC-C, and FC-NC tests to five memory-impaired patients with circumscribed hippocampal lesions and 14 controls. The patients were impaired on all three types of recognition test, and there was no indication that the patients were disproportionately benefited or disproportionately impaired on any test. This pattern of performance suggests that the hippocampus supports both recollection and familiarity.The medial temporal lobe (the hippocampus plus the entorhinal, perirhinal, and parahippocampal cortices) is essential for the recognition of past experience. The capacity for recognition is widely thought to depend on two distinct processes, recollection and familiarity (Mandler 1980; Yonelinas et al. 2002; Wixted 2007). Recollection involves remembering specific details about the episode in which an item was encountered. Familiarity involves simply knowing that an item was presented, even when no additional information can be retrieved about the learning episode itself. This distinction has been prominent in recent discussions about memory, particularly in relation to its possible anatomical basis. One proposal is that recollection depends on the hippocampus and that familiarity depends on the adjacent medial temporal lobe cortex (Brown and Aggleton 2001; Mayes et al. 2002; Yonelinas et al. 2002). Alternatively, it has been suggested that the hippocampus is important for both recollection and familiarity and that the distinction between these two processes does not illuminate the functional differences between the hippocampus and adjacent cortex (Rutishauser et al. 2006; Wais et al. 2006; Squire et al. 2007; Wixted 2007).To clarify the role of the hippocampus in recognition memory, the performance of memory-impaired patients with hippocampal damage has often been compared to that of controls on tests that differ in the extent to which recollection and familiarity contribute to the recognition memory decision. One such approach involves the use of highly similar targets and foils tested using a yes/no (Y/N) format and a forced-choice corresponding (FC-C) format (Holdstock et al. 2002; Westerberg et al. 2006; Bayley et al. 2008). In the case of the Y/N format, participants see a list of targets intermixed with foils (each similar to one of the targets) and are asked to respond “yes” to the targets and “no” to the foils. In the FC-C format, participants see a target presented together with its corresponding, similar foil and are asked to identify the target. According to an idea advanced by Norman and O''Reilly (2003), familiarity can support FC-C recognition because one can make effective use of small but consistent differences between the familiarity signals triggered by the target and foil items. That is, when targets and foils are highly similar and are presented together in the FC-C format, familiarity for the target is likely to slightly and reliably exceed that of the similar foil, allowing the target to be correctly chosen on the basis of familiarity. By contrast, in the Y/N format, slight differences between the familiarity signals of target items and their corresponding foils no longer provide useful information, because the targets and their corresponding foils are not presented together at test. Accordingly, good performance with the Y/N format is more dependent on recollection than with the FC-C format.The same explanation may account for why performance on FC-C tests sometimes exceeds performance on forced-choice noncorresponding (FC-NC) tests (e.g., Hintzman 1988). In the FC-NC format, target items are presented together with a noncorresponding foil that is similar to another target item from the study list (Fig. 1). Thus, the FC-C and FC-NC tests differ only in that the similar targets and foils are presented together in the former but not in the latter. When the corresponding targets and foils are presented together (in the FC-C format), participants can make effective use of consistent differences in familiarity values (as discussed above). When the corresponding targets and foils are not presented together, participants cannot make use of the small differences that they might detect through a side-by-side comparison.Open in a separate windowFigure 1.Test format and materials for the three kinds of recognition test. For each test, 12 images, either objects (A) or silhouettes (B), were presented at study, and memory was tested in one of three ways. For the forced-choice corresponding test (FC-C), each target (a studied item) was presented together with a highly similar foil (a new item). For the forced-choice noncorresponding test (FC-NC), each target was presented together with a foil that was highly similar to a different target from the study list. Participants were asked to point to exactly the same image they had seen during study. For the yes/no test (Y/N), the 12 targets and the 12 foils (each similar to one of the targets) were intermixed and presented one at a time. Participants were asked to respond “yes” if they had seen exactly the same image before and “no” if they had not. Asterisks identify the target items.A recent study (Migo et al. 2009) provides empirical support for the suggestion that familiarity primarily contributes to the recognition decision in the FC-C format, whereas recollection contributes more strongly in the Y/N format and in the FC-NC format. In the Migo et al. (2009) study, healthy participants received FC-C, FC-NC, and Y/N tests after receiving either standard instructions to make their decisions based on familiarity or recollection or modified instructions to base their decisions on familiarity only. On the FC-NC test and on the Y/N test, performance using familiarity alone was significantly worse than under standard instructions. On the FC-C test, performance using familiarity alone was nearly as good as under standard instructions. This result supports the earlier suggestion that FC-C is primarily supported by familiarity, whereas recollection plays a larger role in FC-NC and Y/N recognition (Norman and O''Reilly 2003).If the hippocampus is critical for recollection but not for familiarity, and if good performance on the FC-C format can be achieved using familiarity alone, then patients with focal hippocampal lesions should be differentially impaired on the Y/N and FC-NC recognition test formats compared with the FC-C format. Three recent studies investigated this issue by assessing the effects of hippocampal damage (or presumed hippocampal damage) on Y/N and FC-C tests that used highly similar targets and foils (the FC-NC format was not used in these earlier studies). All three studies used black-and-white silhouette images of objects, and the FC-C test involved the target item and three similar foils (i.e., multiple-choice with four alternatives). In one study, a single patient with bilateral hippocampal damage (patient Y.R.) was impaired on the test of Y/N recognition but was unimpaired on the test of FC-C recognition (Holdstock et al. 2002). A similar result was reported in patients with a diagnosis of mild cognitive impairment (MCI) (Westerberg et al. 2006). These findings have been taken to support the suggestion that the hippocampus selectively supports recollection. However, the study by Holdstock and colleagues (2002) involved a single patient (Y.R.), and findings from a single patient need not agree with findings obtained from a group of patients (see Discussion). In addition, the Westerberg et al. (2006) study involved individuals with a diagnosis of MCI for whom anatomical data were not available. It is therefore not clear what the status of the hippocampus was in these patients. Moreover, a standard Y/N procedure involving 12 study items and 24 test items (as opposed to the 12 study test items and 60 test items used in previous studies [Holdstock et al. 2002; Westerberg et al. 2006; Bayley et al. 2008]) might be better suited to address the question of whether Y/N recognition is selectively impaired in hippocampal patients. Bayley et al. (2008) tested five patients with circumscribed hippocampal damage using the same test materials and procedure as in Holdstock et al. (2002). When all 60 test items of the Y/N test were scored, the patients were found to be more impaired on the Y/N test than on the FC-C test. However, when only the first 24 test items of the Y/N test were scored (according to the standard Y/N procedure), the patients were found to be impaired on both the Y/N and FC-C tests to a similar degree.The earlier studies (Holdstock et al. 2002; Westerberg et al. 2006; Bayley et al. 2008) compared Y/N recognition to four-alternative FC-C recognition in which each target was presented along with three corresponding foils. None of the earlier studies investigated how patients with hippocampal lesions performed on FC-NC recognition. As Migo et al. (2009) point out, FC-C and FC-NC tests are better matched than the FC-C and Y/N tests because they are both forced-choice tests, and both use the same number of test trials. As such, they argue, it would be more useful to compare FC-C recognition performance to FC-NC recognition performance to determine whether patients with hippocampal lesions are intact or impaired on familiarity-based tests.The present study assessed Y/N, two-alternative FC-C, and two-alternative FC-NC recognition, using highly similar targets and foils. The tests were given to five patients with circumscribed hippocampal damage and 14 matched controls. The Y/N test involved an equal number of targets and foils (unlike the design used in the prior studies), and a two-alternative format was used for the forced-choice tests to make them comparable to the Y/N test (i.e., all three tests involved the same number of targets and foils). The FC-C and FC-NC tests were identical except with respect to how the targets and their corresponding foils were paired on the recognition test.To extend our findings beyond the stimuli used in prior studies, we also used color photographs of objects in addition to black-and-white silhouettes. Using these three test formats, we asked the following questions: (1) Does hippocampal damage impair Y/N recognition memory but spare, or disproportionately benefit, FC-C recognition (as suggested by the view that the hippocampus supports recollection and not familiarity)? Or does hippocampal damage impair Y/N and FC-C recognition similarly (as suggested by the view that the hippocampus supports both recollection and familiarity)? (2) Does hippocampal damage disproportionately benefit FC-C recognition relative to FC-NC recognition, or does hippocampal damage impair FC-C and FC-NC recognition similarly?     

Making Sense of Suffering: A Preliminary Study of Changes in Religious Women Adjusting to Severe Adversity

This qualitative study examined interviews from 25 women who held theistic beliefs from Christian, Islamic, or Jewish traditions. All had recently experienced severe adversity but reported they were coping well. Analysis illustrated changes in religious beliefs and attitudes they made as a result of learning to cope. Differences were found among the 3 religious groups. Findings of this preliminary study suggest that religious meaning and experience may change because of the process of learning to cope with severe adversity. Recommendations are made for counseling theistically oriented women.     

Getting less than their fair share: Maltreated youth are hyper‐cooperative yet vulnerable to exploitation in a public goods game

Human cooperative behavior has long been thought to decline under adversity. However, studies have primarily examined perceived patterns of cooperation, with little eye to actual cooperative behavior embedded within social interaction. Game‐theoretical paradigms can help close this gap by unpacking subtle differences in how cooperation unfolds during initial encounters. This study is the first to use a child‐appropriate, virtual, public goods game to study actual cooperative behavior in 329 participants aged 9–16 years with histories of maltreatment (n = 99) and no maltreatment (n = 230) while controlling for psychiatric symptoms. Unlike work on perceived patterns of cooperation, we found that maltreated participants actually contribute more resources to a public good during peer interaction than their nonmaltreated counterparts. This effect was robust when controlling for psychiatric symptoms and peer problems as well as demographic variables. We conclude that maltreatment may engender a hyper‐cooperative strategy to minimize the odds of hostility and preserve positive interaction during initial encounters. This, however, comes at the cost of potential exploitation by others.     

The influence of reasons on interpretations of probability forecasts

When providing a probability estimate for an event, experts often supply reasons that they expect will clarify and support that estimate. We investigated the possible unintended influence that these reasons might have on a listener's intuitive interpretation of the event's likelihood. Experiments 1 and 2 demonstrated that people who read positive reasons for a doctor's probability estimate regarding a hypothetical surgery were more optimistic than those who read negative reasons for the identical estimate. Experiment 3 tested whether a doctor's failure forecast for a surgery would result in differing levels of pessimism when the potential risk was attributed to one complication that had a probability of 0.30 versus three complications that had a disjunctive probability of 0.30. Overall, the findings are consistent with the argument that a probability estimate, albeit numerically precise, can be flexibly interpreted at an intuitive level depending on the reasons that the forecaster provides as the basis for the estimate. Copyright © 2003 John Wiley & Sons, Ltd.     

Some Antiepileptic Compounds Impair Learning by Rats in a Morris Water Maze

In the present experiments, we investigated the effects of several commonly employed antiepileptic drugs on the performance of adult rats in a Morris water maze task. We found that phenytoin treatment produced the most deleterious performance impairments across all days of training, and that these performance deficits are not likely due to any general sensorimotor impairments. Carbamazepine had milder, but detectable negative effects, as carbamazepine-treated animals exhibited initial acquisition deficits, but rapidly achieved escape levels comparable to controls. In marked contrast, valproate and ethosuximide had no detectable effects on learning in the water maze. These results parallel previous findings in rats treated with these compounds and tested in an instrumental learning task, and are in general agreement with the human clinical literature. To the extent that one might wish to minimize learning deficits associated with maintenance on antiepileptic drugs, phenytoin is definitely not the treatment of choice, while valproate or ethosuximide are apparently much less disruptive.     

Student perceptions and motivation in the classroom: exploring relatedness and value

According to Self-Determination Theory, feelings of relatedness and value of a behavior are critical factors that affect internalization and integration. The purpose of the current study was to identify factors that influence relatedness and value in an academic setting. Specifically, the study investigated the effects of autonomy, mastery goals, performance-approach goals, and performance-avoidance goals, on two dependent variables: relatedness to the professor and value of the course. Participants were 222 undergraduate students (90 males) enrolled in introductory psychology classes. Linear regression analyses showed a statistically significant effect of mastery goals and autonomy on relatedness such that higher scores were associated with greater relatedness. A similar pattern emerged for value. Neither performance-approach nor performance-avoidance goals were significantly associated with relatedness or value. Theoretical and practical contributions are discussed.

Attention to adjacent and separate positions in space: An electrophysiological analysis

Some theories of visuospatial attention propose that attention can be divided between separated zones of space that exclude the intervening region, whereas other theories state that the focus of attention must encompass aunitary, continuous zone. These contrasting viewswere evaluated in an experiment 9n which subjects were required to monitor two of four stimulus locations for targets; the two relevant locations were adjacent in one condition and were separated by an intervening irrelevant location in a second condition . To assess the distribution of attention across the relevant and irrelevant locations, event-related brain potentials(ERPa)were recorded to taskirrelevant “probe” stimuli that were occasionally presented at the individual stimulus locations. When the relevant locations were adjacent, probes presented at irrelevant locations elicited smaller sensory-evoked electrophysiological responses than probes presented at relevant locations, consistent with an attentional suppression of inputs from the unattended locations. When the relevant locations were separated by an irrelevant location, however, the sensory responses evoked by probes presented at this intervening irrelevant location were not suppressed, and target detection performance became slower and less accurate. These results suggest that attentionforms a unitary zone that may expand to encompass multiple relevant locations but must also include the area between them; as a result, irrelevant information arising from intervening locations is not suppressed and perceptual processing is compromised.     

Logical searches of young children in hiding and finding tasks

Thirty-two 3 and 32 4-year-olds were tested on two tasks which required them to infer the location of a concealed object. In the hiding tusk the child watched while an object was hidden and then attempted to find it; in the finding tusk the child watched while one object was found and then attempted to find a duplicate of it in the same place. Each sequence of events that the child watched ruled out two of the four locations in a linear array as possible hiding places for the object, but did not specify which of the remaining two contained it. The children did use the information conveyed by the sequences of events to decide where to search. Older children generally did better than younger children both in their first choices and in their second choices when the first, although correct, did not locate the object. However, neither age group made the correct choice of a second location consistently. This suggested that the children encountered mnemonic or logical difficulties, or both, because of the fact that two locations were equally compatible with a given sequence of events.     

Television news and elderly persons.

Previous studies concerning elderly people have examined either use of all media by older adults or their depiction in television entertainment programs. What has been overlooked has been television news and its effects on elderly people. Careful research is needed to gauge this.     

Learned helplessness and the detection of contingency: A direct test

Two studies tested a basic hypothesis of the learned helplessness model: That performance deficits associated with exposure to uncontrollable outcomes are directly mediated by an individual's perception of response-outcome independence. In the first experiment 48 subjects were exposed to noise bursts. For one experimental group, the termination of the noise was response-contingent. For five other groups, noise-burst termination was independent of subjects' responses. These five groups varied in the number of trials on which they received positive feedback: As predicted, subjects overestimated the amount of control they had over noise termination as a positive linear function of the amount of noncontingent positive feedback they received. Although subjects exposed to either noncontingent positive or negative feedback showed subsequent performance deficits on an anagrams task, the expected relation between perceived control and subsequent performance failed to emerge. These findings were replicated in a second experiment. In addition, subjects' locus, stability, and globality attributions failed to predict subsequent performance. These results call into question the central premises of helplessness theory: That perceived uncontrollability and causal attributions mediate learned helplessness.