Two kinds of memory signals in neurons of the human hippocampus.

Prior studies of the neural representation of episodic memory in the human hippocampus have identified generic memory signals representing the categorical status of test items (novel vs. repeated), whereas other studies have identified item specific memory signals representing individual test items. Here, we report that both kinds of memory signals can be detected in hippocampal neurons in the same experiment. We recorded single-unit activity from four brain regions (hippocampus, amygdala, anterior cingulate, and prefrontal cortex) of epilepsy patients as they completed a continuous recognition task. The generic signal was found in all four brain regions, whereas the item-specific memory signal was detected only in the hippocampus and reflected sparse coding. That is, for the item-specific signal, each hippocampal neuron responded strongly to a small fraction of repeated words, and each repeated word elicited strong responding in a small fraction of neurons. The neural code was sparse, pattern-separated, and limited to the hippocampus, consistent with longstanding computational models. We suggest that the item-specific episodic memory signal in the hippocampus is fundamental, whereas the more widespread generic memory signal is derivative and is likely used by different areas of the brain to perform memory-related functions that do not require item-specific information.

Optimizing the selection of fillers in police lineups.

A typical police lineup contains a photo of one suspect (who is innocent in a target-absent lineup and guilty in a target-present lineup) plus photos of five or more fillers who are known to be innocent. To create a fair lineup in which the suspect does not stand out, two filler selection methods are commonly used. In the first, fillers are selected if they are similar in appearance to the suspect. In the second, fillers are selected if they possess facial features included in the witness's description of the culprit (e.g., "20-y-old white male"). The police sometimes use a combination of the two methods by selecting description-matched fillers whose appearance is also similar to that of the suspect in the lineup. Decades of research on which approach is better remains unsettled. Here, we tested a counterintuitive prediction made by a formal model based on signal detection theory: From a pool of acceptable description-matched photos, selecting fillers whose appearance is otherwise dissimilar to the suspect should increase the hit rate without affecting the false-alarm rate (increasing discriminability). In Experiment 1, we confirmed this prediction using a standard mock-crime paradigm. In Experiment 2, the effect on discriminability was reversed (as also predicted by the model) when fillers were matched on similarity to the perpetrator in both target-present and target-absent lineups. These findings suggest that signal-detection theory offers a useful theoretical framework for understanding eyewitness identification decisions made from a police lineup.

Science is not a signal detection problem.

The perceived replication crisis and the reforms designed to address it are grounded in the notion that science is a binary signal detection problem. However, contrary to null hypothesis significance testing (NHST) logic, the magnitude of the underlying effect size for a given experiment is best conceptualized as a random draw from a continuous distribution, not as a random draw from a dichotomous distribution (null vs. alternative). Moreover, because continuously distributed effects selected using a P < 0.05 filter must be inflated, the fact that they are smaller when replicated (reflecting regression to the mean) is no reason to sound the alarm. Considered from this perspective, recent replication efforts suggest that most published P < 0.05 scientific findings are "true" (i.e., in the correct direction), with observed effect sizes that are inflated to varying degrees. We propose that original science is a screening process, one that adopts NHST logic as a useful fiction for selecting true effects that are potentially large enough to be of interest to other scientists. Unlike original science, replication science seeks to precisely measure the underlying effect size associated with an experimental protocol via large-N direct replication, without regard for statistical significance. Registered reports are well suited to (often resource-intensive) direct replications, which should focus on influential findings and be published regardless of outcome. Conceptual replications play an important but separate role in validating theories. However, because they are part of NHST-based original science, conceptual replications cannot serve as the field's self-correction mechanism. Only direct replications can do that.

Spiking activity in the human hippocampus prior to encoding predicts subsequent memory.

Encoding activity in the medial temporal lobe, presumably evoked by the presentation of stimuli (postonset activity), is known to predict subsequent memory. However, several independent lines of research suggest that preonset activity also affects subsequent memory. We investigated the role of preonset and postonset single-unit and multiunit activity recorded from epilepsy patients as they completed a continuous recognition task. In this task, words were presented in a continuous series and eventually began to repeat. For each word, the patient's task was to decide whether it was novel or repeated. We found that preonset spiking activity in the hippocampus (when the word was novel) predicted subsequent memory (when the word was later repeated). Postonset activity during encoding also predicted subsequent memory, but was simply a continuation of preonset activity. The predictive effect of preonset spiking activity was much stronger in the hippocampus than in three other brain regions (amygdala, anterior cingulate, and prefrontal cortex). In addition, preonset and postonset activity around the encoding of novel words did not predict memory performance for novel words (i.e., correctly classifying the word as novel), and preonset and postonset activity around the time of retrieval did not predict memory performance for repeated words (i.e., correctly classifying the word as repeated). Thus, the only predictive effect was between preonset activity (along with its postonset continuation) at the time of encoding and subsequent memory. Taken together, these findings indicate that preonset hippocampal activity does not reflect general arousal/attention but instead reflects what we term "attention to encoding."

Eyewitness memory is reliable, but the criminal justice system is not.

The reliability of any type of forensic evidence (e.g., forensic DNA) is assessed by testing its information value when it is not contaminated and is properly tested. Assessing the reliability of forensic memory evidence should be no exception to that rule. Unfortunately, testing a witness's memory irretrievably contaminates it. Thus, only the first (properly conducted) test is relevant to the question of whether eyewitness memory is reliable. With few exceptions, the results of studies conducted in the lab and in the real world show that confidence is highly predictive of accuracy on the first test, and high-confidence often implies high accuracy. The fact that many eyewitnesses are known to have made high-confidence misidentifications in the courtroom has cemented the almost universal impression that eyewitness memory is unreliable. However, it is the criminal justice system that is guilty of unwittingly using contaminated memory evidence (relying on the last memory test, in court) in conjunction with an improper testing procedure (namely, a courtroom showup) to win convictions of the innocent. That mistake should no longer be blamed on the unreliability of eyewitness memory.

Doing right by the eyewitness evidence: a response to Berkowitz et al.

Berkowitz et al. (Berkowitz, S. R., Garrett, B. L., Fenn, K. M., & Loftus, E. F. (2020). Convicting with confidence? Why we should not over-rely on eyewitness confidence. Memory. https://doi.org/10.1080/09658211.2020.1849308) attribute to us the claim that "confidence trumps all", and the few out-of-context quotations they selected can certainly be used to create that false impression. However, it is easily disproved, and we do so here. The notion that "confidence trumps all" is the mistake that the jurors made in the DNA exoneration cases, not a position that we have ever advocated.

Order effects in bilingual recognition memory partially confirm predictions of the frequency-lag hypothesis.

The present study examined task order, language, and frequency effects on list memory to investigate how bilingualism affects recognition memory. In Experiment 1, 64 bilinguals completed a recognition memory task including intermixed high and medium frequency words in English and another list in Spanish. In Experiment 2, 64 bilinguals and 64 monolinguals studied lists with only high frequency English words and a separate list with only low frequency English words, in counterbalanced order followed by a recognition test. In Experiment 1, bilinguals who completed the task in the dominant language first outperformed bilinguals tested in the nondominant language first, and order effects were not stronger in the dominant language. In Experiment 2, participants who were tested with high frequency word lists first outperformed those tested with low frequency word lists first. Regardless of language and testing order, memory for English and high frequency words was lower than memory for Spanish and medium frequency (in Experiment 1) or low frequency (in Experiment 2) words. Order effects on recognition memory patterned differently from previously reported effects on picture naming in ways that do not suggest between language interference and instead invite an analogy between language dominance and frequency of use (i.e., dominant language = higher frequency) as the primary factor affecting bilingual recognition memory.

Coding of episodic memory in the human hippocampus.

Neurocomputational models have long posited that episodic memories in the human hippocampus are represented by sparse, stimulus-specific neural codes. A concomitant proposal is that when sparse-distributed neural assemblies become active, they suppress the activity of competing neurons (neural sharpening). We investigated episodic memory coding in the hippocampus and amygdala by measuring single-neuron responses from 20 epilepsy patients (12 female) undergoing intracranial monitoring while they completed a continuous recognition memory task. In the left hippocampus, the distribution of single-neuron activity indicated that only a small fraction of neurons exhibited strong responding to a given repeated word and that each repeated word elicited strong responding in a different small fraction of neurons. This finding reflects sparse distributed coding. The remaining large fraction of neurons exhibited a concurrent reduction in firing rates relative to novel words. The observed pattern accords with longstanding predictions that have previously received scant support from single-cell recordings from human hippocampus.

Identifying the guilty word: Simultaneous versus sequential lineups for DRM word lists.

Recent research in the eyewitness identification literature has investigated whether simultaneous or sequential lineups yield better discriminability. In standard eyewitness identification experiments, subjects view a mock-crime video and then are tested only once, requiring large samples for adequate power. However, there is no reason why theories of simultaneous versus sequential lineup performance cannot be tested using more traditional recognition memory tasks. In two experiments, subjects studied DRM (Deese-Roediger-McDermott) word lists (e.g., bed, rest, tired, ...) and were tested using "lineups" in which six words were presented either simultaneously or sequentially. A studied word (e.g., tired) served as the guilty suspect in target-present lineups, unstudied related words (e.g., nap) served as fillers in target-present and target-absent lineups, and critical lures (e.g., sleep) were included in some target-present and target-absent lineups as well, to serve as attractive alternatives to the target word (or suspect). ROC analyses showed that the simultaneous test format generally yielded superior discriminability performance compared to the sequential test format, whether or not the critical lure was present in the lineup.

Policy and procedure recommendations for the collection and preservation of eyewitness identification evidence.

OBJECTIVE: The Executive Committee of the American Psychology-Law Society (Division 41 of the American Psychological Association) appointed a subcommittee to update the influential 1998 scientific review paper on guidelines for eyewitness identification procedures. METHOD: This was a collaborative effort by six senior eyewitness researchers, who all participated in the writing process. Feedback from members of AP-LS and the legal communities was solicited over an 18-month period. RESULTS: The results yielded nine recommendations for planning, designing, and conducting eyewitness identification procedures. Four of the recommendations were from the 1998 article and concerned the selection of lineup fillers, prelineup instructions to witnesses, the use of double-blind procedures, and collection of a confidence statement. The additional five recommendations concern the need for law enforcement to conduct a prelineup interview of the witness, the need for evidence-based suspicion before conducting an identification procedure, video-recording of the entire procedure, avoiding repeated identification attempts with the same witness and same suspect, and avoiding the use of showups when possible and improving how showups are conducted when they are necessary. CONCLUSIONS: The reliability and integrity of eyewitness identification evidence is highly dependent on the procedures used by law enforcement for collecting and preserving the eyewitness evidence. These nine recommendations can advance the reliability and integrity of the evidence. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Recognition Memory in Marmoset and Macaque Monkeys: A Comparison of Active Vision.

The core functional organization of the primate brain is remarkably conserved across the order, but behavioral differences evident between species likely reflect derived modifications in the underlying neural processes. Here, we performed the first study to directly compare visual recognition memory in two primate species-rhesus macaques and marmoset monkeys-on the same visual preferential looking task as a first step toward identifying similarities and differences in this cognitive process across the primate phylogeny. Preferences in looking behavior on the task were broadly similar between the species, with greater looking times for novel images compared with repeated images as well as a similarly strong preference for faces compared with other categories. Unexpectedly, we found large behavioral differences among the two species in looking behavior independent of image familiarity. Marmosets exhibited longer looking times, with greater variability compared with macaques, regardless of image content or familiarity. Perhaps most strikingly, marmosets shifted their gaze across the images more quickly, suggesting a different behavioral strategy when viewing images. Although such differences limit the comparison of recognition memory across these closely related species, they point to interesting differences in the mechanisms underlying active vision that have significant implications for future neurobiological investigations with these two nonhuman primate species. Elucidating whether these patterns are reflective of species or broader phylogenetic differences (e.g., between New World and Old World monkeys) necessitates a broader sample of primate taxa from across the Order.

The cognitive neuroscience of human memory since H.M.

Work with patient H.M., beginning in the 1950s, established key principles about the organization of memory that inspired decades of experimental work. Since H.M., the study of human memory and its disorders has continued to yield new insights and to improve understanding of the structure and organization of memory. Here we review this work with emphasis on the neuroanatomy of medial temporal lobe and diencephalic structures important for memory, multiple memory systems, visual perception, immediate memory, memory consolidation, the locus of long-term memory storage, the concepts of recollection and familiarity, and the question of how different medial temporal lobe structures may contribute differently to memory functions.

Autobiographical memory, future imagining, and the medial temporal lobe.

In two experiments, patients with damage to the medial temporal lobe (MTL) and healthy controls produced detailed autobiographical narratives as they remembered past events (recent and remote) and imagined future events (near and distant). All recent events occurred after the onset of memory impairment. The first experiment aimed to replicate the methods of Race et al. [Race E, Keane MM, Verfaellie M (2011) J Neurosci 31(28):10262-10269]. Transcripts from that study were kindly made available for independent analysis, which largely reproduced the findings from that study. Our patients produced marginally fewer episodic details than controls. Patients from the earlier study were more impaired than our patients. Patients in both groups had difficulty in returning to their narratives after going on tangents, suggesting that anterograde memory impairment may have interfered with narrative construction. In experiment 2, the experimenter used supportive questioning to help keep participants on task and reduce the burden on anterograde memory. This procedure increased the number of details produced by all participants and rescued the performance of our patients for the distant past. Neither of the two patient groups had any special difficulty in producing spatial details. The findings suggest that constructing narratives about the remote past and the future does not depend on MTL structures, except to the extent that anterograde amnesia affects performance. The results further suggest that different findings about the status of autobiographical memory likely depend on differences in the location and extent of brain damage in different patient groups.

Learning and remembering real-world events after medial temporal lobe damage.

The hippocampus is important for autobiographical memory, but its role is unclear. In the study, patients with hippocampal damage and controls were taken on a 25-min walk on the University of California, San Diego, campus during which 11 planned events occurred. Memory was tested directly after the walk. In addition, a second group of controls took the same walk and were tested after 1 mo. Patients with hippocampal damage remembered fewer details than controls tested directly after the walk but remembered a similar number of details as controls tested after 1 mo. Notably, the details that were reported by patients had the characteristics of episodic recollection and included references to particular places and events. Patients exhibited no special difficulty remembering spatial details in comparison with nonspatial details. Last, whereas both control groups tended to recall the events of the walk in chronological order, the order in which patients recalled the events was unrelated to the order in which they occurred. The findings illuminate the role of the hippocampus in autobiographical memory and in the spatial and nonspatial aspects of episodic recollection.

Estimating the reliability of eyewitness identifications from police lineups.

Laboratory-based mock crime studies have often been interpreted to mean that (i) eyewitness confidence in an identification made from a lineup is a weak indicator of accuracy and (ii) sequential lineups are diagnostically superior to traditional simultaneous lineups. Largely as a result, juries are increasingly encouraged to disregard eyewitness confidence, and up to 30% of law enforcement agencies in the United States have adopted the sequential procedure. We conducted a field study of actual eyewitnesses who were assigned to simultaneous or sequential photo lineups in the Houston Police Department over a 1-y period. Identifications were made using a three-point confidence scale, and a signal detection model was used to analyze and interpret the results. Our findings suggest that (i) confidence in an eyewitness identification from a fair lineup is a highly reliable indicator of accuracy and (ii) if there is any difference in diagnostic accuracy between the two lineup formats, it likely favors the simultaneous procedure.

Models of lineup memory.

Face recognition memory is often tested by the police using a photo lineup, which consists of one suspect, who is either innocent or guilty, and five or more physically similar fillers, all of whom are known to be innocent. For many years, lineups were investigated in lab studies without guidance from standard models of recognition memory. More recently, signal detection theory has been used to conceptualize lineup memory and to motivate receiver operating characteristic (ROC) analysis of lineup performance. Here, we describe three competing signal-detection models of lineup memory, derive their likelihood functions, and fit them to empirical ROC data. We also introduce the notion that memory signals generated by the faces in a lineup are likely to be correlated because, by design, those faces share features. The models we investigate differ in their predictions about the effect that correlated memory signals should have on the ability to discriminate innocent from guilty suspects. A popular compound signal detection model known as the Integration model predicts that correlated memory signals should impair discriminability. Empirically, this model performed so poorly that, going forward, it should probably be abandoned. The best-fitting model incorporates a principle known as "ensemble coding," which predicts that correlated memory signals should enhance discriminability. The ensemble model aligns with a previously proposed theory of eyewitness identification according to which the simultaneous presentation of faces in a lineup enhances discriminability compared to when faces are presented in isolation because it permits eyewitnesses to detect and discount non-diagnostic facial features.

Sparse and distributed coding of episodic memory in neurons of the human hippocampus.

Neurocomputational models hold that sparse distributed coding is the most efficient way for hippocampal neurons to encode episodic memories rapidly. We investigated the representation of episodic memory in hippocampal neurons of nine epilepsy patients undergoing intracranial monitoring as they discriminated between recently studied words (targets) and new words (foils) on a recognition test. On average, single units and multiunits exhibited higher spike counts in response to targets relative to foils, and the size of this effect correlated with behavioral performance. Further analyses of the spike-count distributions revealed that (i) a small percentage of recorded neurons responded to any one target and (ii) a small percentage of targets elicited a strong response in any one neuron. These findings are consistent with the idea that in the human hippocampus episodic memory is supported by a sparse distributed neural code.

Hippocampal damage impairs recognition memory broadly, affecting both parameters in two prominent models of memory.

Declarative memory is thought to rely on two processes: recollection and familiarity. Recollection involves remembering specific details about the episode in which an item was encountered, and familiarity involves simply knowing that an item was presented even when no information can be recalled about the episode itself. There has been debate whether the hippocampus supports only recollection or whether it supports both processes. We approached this issue in a relatively theory-neutral way by fitting two prominent models that have been used to describe recognition memory: dual process signal detection and unequal variance signal detection. Both models yield two parameters of interest when fit to recognition memory data. The dual process signal detection model yields estimates of recollection (r) and familiarity (d'). The unequal variance signal detection model yields estimates of the ratio of the variance of target and foil memory strength distributions (σtarget/σfoil) and the difference in the means of the two distributions (d). We asked how the two parameters of each model were affected by hippocampal damage. We tested five patients with well-characterized bilateral lesions thought to be limited to the hippocampus and age-matched controls. The patients exhibited a broad memory deficit that markedly reduced the value of both parameters in both models. In addition, the pattern of results exhibited by the patients was recapitulated in healthy controls as the delay between learning and testing was extended. Thus, hippocampal damage impairs both component processes of recognition memory.