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.

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."

The Oddity Detection in Diverse Scenes (ODDS) database: Validated real-world scenes for studying anomaly detection.

Many applied screening tasks (e.g., medical image or baggage screening) involve challenging searches for which standard laboratory search is rarely equivalent. For example, whereas laboratory search frequently requires observers to look for precisely defined targets among isolated, non-overlapping images randomly arrayed on clean backgrounds, medical images present unspecified targets in noisy, yet spatially regular scenes. Those unspecified targets are typically oddities, elements that do not belong. To develop a closer laboratory analogue to this, we created a database of scenes containing subtle, ill-specified "oddity" targets. These scenes have similar perceptual densities and spatial regularities to those found in expert search tasks, and each includes 16 variants of the unedited scene wherein an oddity (a subtle deformation of the scene) is hidden. In Experiment 1, eight volunteers searched thousands of scene variants for an oddity. Regardless of their search accuracy, they were then shown the highlighted anomaly and rated its subtlety. Subtlety ratings reliably predicted search performance (accuracy and response times) and did so better than image statistics. In Experiment 2, we conducted a conceptual replication in which a larger group of naïve searchers scanned subsets of the scene variants. Prior subtlety ratings reliably predicted search outcomes. Whereas medical image targets are difficult for naïve searchers to detect, our database contains thousands of interior and exterior scenes that vary in difficulty, but are nevertheless searchable by novices. In this way, the stimuli will be useful for studying visual search as it typically occurs in expert domains: Ill-specified search for anomalies in noisy displays.

Flexible attention allocation dynamically impacts incidental encoding in prospective memory.

Remembering to fulfill an intention at a later time often requires people to monitor the environment for cues that it is time to act. This monitoring involves the strategic allocation of attentional resources, ramping attention up more in some contexts than others. In addition to interfering with ongoing task performance, flexibly shifting attention may affect whether task-irrelevant information is later remembered. In the present investigation, we manipulated contextual expectations in event-related prospective memory (PM) to examine the consequences of flexible attention allocation on incidental memory. Across two experiments, participants completed a color-matching task while monitoring for ill-defined (Experiment 1) or specific (Experiment 2) PM targets. To manipulate contextual expectations, some participants were explicitly told about the trial types in which PM targets could (or not) appear, while others were given less precise or no expectations. Across experiments, participants' color-matching decisions were slower in high-expectation trials, relative to trials when targets were not expected. Additionally, participants had better incidental memory for PM-irrelevant items from high-expectation trials, but only when they received explicit contextual expectations. These results confirm that participants flexibly allocate attention based on explicit trial-by-trial expectations. Furthermore, the present study indicates that greater attention to item identity yields better incidental memory even for PM-irrelevant items, irrespective of processing time.

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.

The detail is in the difficulty: Challenging search facilitates rich incidental object encoding.

When searching for objects in the environment, observers necessarily encounter other, nontarget, objects. Despite their irrelevance for search, observers often incidentally encode the details of these objects, an effect that is exaggerated as the search task becomes more challenging. Although it is well established that searchers create incidental memories for targets, less is known about the fidelity with which nontargets are remembered. Do observers store richly detailed representations of nontargets, or are these memories characterized by gist-level detail, containing only the information necessary to reject the item as a nontarget? We addressed this question across two experiments in which observers completed multiple-target (one to four potential targets) searches, followed by surprise alternative forced-choice (AFC) recognition tests for all encountered objects. To assess the detail of incidentally stored memories, we used similarity rankings derived from multidimensional scaling to manipulate the perceptual similarity across objects in 4-AFC (Experiment 1a) and 16-AFC (Experiments 1b and 2) tests. Replicating prior work, observers recognized more nontarget objects encountered during challenging, relative to easier, searches. More importantly, AFC results revealed that observers stored more than gist-level detail: When search objects were not recognized, observers systematically chose lures with higher perceptual similarity, reflecting partial encoding of the search object's perceptual features. Further, similarity effects increased with search difficulty, revealing that incidental memories for visual search objects are sharpened when the search task requires greater attentional processing.

Not all information in visual working memory is forgotten equally.

To improve maintenance of task-relevant information in visual working memory (VWM), previously encoded, but no longer relevant, information can be suppressed or forgotten. However, it is unclear whether a cue directing attention to a subset of stimuli leads to complete forgetting for non-cued stimuli. The current study utilized a novel method of testing to-be forgotten information to determine if the effectiveness of forgetting differs depending on the type of encoded stimuli. Participants performed a directed forgetting change detection task, and importantly, the changed stimulus could be a novel stimulus or a to-be-forgotten stimulus. Stimulus type (colors, objects, or shapes) was manipulated across two experiments. Results suggest that a cue benefits memory for to-be-remembered information, but performance is not equivalent to never encoding to-be-forgotten information. Furthermore, the type of encoded information impacts the extent of forgetting.

Response dynamics of event-based prospective memory retrieval in mouse tracking.

Prospective memory (PM) is typically measured using keypresses in laboratory paradigms, which therefore assess only discrete, stage-like processes. In the present study we manipulated focal and nonfocal PM cue conditions, as well as participants' focus on different aspects of the PM/ongoing task set, using the methodology to capture dynamic computer mouse movements. The software captured mouse trajectories during lexical decisions and PM responses. We replicated many findings typical in the PM literature, including the accuracy advantage for focal over nonfocal conditions and longer ongoing-task response times for nonfocal conditions. Participants' movement trajectories during PM responses revealed evidence for both spontaneous-retrieval and strategic-monitoring processes in focal and nonfocal PM retrieval conditions. During trials suggestive of spontaneous retrieval, mouse trajectories initially went toward the typical ongoing-task response but turned mid-trajectory toward the PM response field on the opposite side of the computer screen. In nonfocal conditions, these trajectory reversals had a wider arc and took longer to complete, reflecting the likely greater retrospective retrieval requirements of nonfocal conditions. Regarding what are more likely to be strategic-monitoring processes, a significant portion of responses traveled directly to the PM response field, as though people were prepared to make such a response.

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.

Modern Speed-Reading Apps Do Not Foster Reading Comprehension.

New computer apps are gaining popularity by suggesting that reading speeds can be drastically increased when eye movements that normally occur during reading are eliminated. This is done using rapid serial visual presentation (RSVP), where words are presented 1 at a time, thus preventing natural eye movements such as saccades, fixations, and regressions from occurring. Al- though the companies producing these apps suggest that RSVP reading does not yield comprehension deficits, research investigating the role of eye movements in reading documents shows the necessity of natural eye movements for accurate comprehension. The current study explored variables that may affect reading comprehension during RSVP reading, including text difficulty (6th grade and 12th grade), text presentation speed (static, 700 wpm, and 1,000 wpm), and working memory capacity (WMC). Consistent with recent work showing a tenuous relationship between comprehension and WMC, participants' WMC did not predict comprehension scores. Instead, comprehension was most affected by reading speed: Static text was associated with superior performance, relative to either RSVP reading condition. Furthermore, slower RSVP speeds yielded better verbatim comprehension, and faster speeds benefited inferential comprehension.

Distributed representation of visual objects by single neurons in the human brain.

It remains unclear how single neurons in the human brain represent whole-object visual stimuli. While recordings in both human and nonhuman primates have shown distributed representations of objects (many neurons encoding multiple objects), recordings of single neurons in the human medial temporal lobe, taken as subjects' discriminated objects during multiple presentations, have shown gnostic representations (single neurons encoding one object). Because some studies suggest that repeated viewing may enhance neural selectivity for objects, we had human subjects discriminate objects in a single, more naturalistic viewing session. We found that, across 432 well isolated neurons recorded in the hippocampus and amygdala, the average fraction of objects encoded was 26%. We also found that more neurons encoded several objects versus only one object in the hippocampus (28 vs 18%, p < 0.001) and in the amygdala (30 vs 19%, p < 0.001). Thus, during realistic viewing experiences, typical neurons in the human medial temporal lobe code for a considerable range of objects, across multiple semantic categories.

High target prevalence may reduce the spread of attention during search tasks.

Target prevalence influences many cognitive processes during visual search, including target detection, search efficiency, and item processing. The present research investigated whether target prevalence may also impact the spread of attention during search. Relative to low-prevalence searches, high-prevalence searches typically yield higher fixation counts, particularly during target-absent trials. This may emerge because the attention spread around each fixation may be smaller for high than low prevalence searches. To test this, observers searched for targets within object arrays in Experiments 1 (free-viewing) and 2 (gaze-contingent viewing). In Experiment 3, observers searched for targets in a Rapid Serial Visual Presentation (RSVP) stream at the center of the display while simultaneously processing occasional peripheral objects. Experiment 1 used fixation patterns to estimate attentional spread, and revealed that attention was narrowed during high, relative to low, prevalence searches. This effect was weakened during gaze-contingent search (Experiment 2) but emerged again when eye movements were unnecessary in RSVP search (Experiment 3). These results suggest that, although task demands impact how attention is allocated across displays, attention may also narrow when searching for frequent targets.

Spotting missing or wanted people: racial biases in prospective person memory.

Searching for missing or wanted people is a crucial task in our society. Previous work on prospective person memory (PPM) has demonstrated that performance on this type of search task is worse relative to standard prospective memory tasks. Importantly, this process may be further affected by the race of the missing person, yet this has never been tested in laboratory settings. To test the effects of race on PPM, a convenience sample consisting primarily of self-identified Caucasian participants was asked to search for either a Caucasian or an Indian target person while judging the orientation of different Caucasian and Indian faces. Although the tasks were otherwise identical, 89% of Caucasian PPM targets were found while only 53% of Indian targets were found. Furthermore, relative to a control group with no PPM requirements, participants were slower and more error-prone when judging Indian faces relative to White faces, particularly if they were searching for an Indian face. We interpret these results as revealing other-race effects in prospective person memory, highlighting race as a critical factor for finding missing people. Importantly, this also emphasizes the need for real-world search efforts to factor in difficulty differences when people monitor for missing/wanted people from their own or different racial backgrounds. For example, media coverage of missing persons cases could perhaps be distributed more equitably by considering whether the missing person is from a racial minority in that region.

Encoding of Race Categories by Single Neurons in the Human Brain.

Previous research has suggested that race-specific features are automatically processed during face perception, often with out-group faces treated categorically. Functional imaging has illuminated the hemodynamic correlates of this process, with fewer studies examining single-neuron responses. In the present experiment, epilepsy patients undergoing microwire recordings in preparation for surgical treatment were shown realistic computer-generated human faces, which they classified according to the emotional expression shown. Racial categories of the stimulus faces varied independently of the emotion shown, being irrelevant to the patients' primary task. Nevertheless, we observed race-driven changes in neural firing rates in the amygdala, anterior cingulate cortex, and hippocampus. These responses were broadly distributed, with the firing rates of 28% of recorded neurons in the amygdala and 45% in the anterior cingulate cortex predicting one or more racial categories. Nearly equal proportions of neurons responded to White and Black faces (24% vs. 22% in the amygdala and 26% vs. 28% in the anterior cingulate cortex). A smaller fraction (12%) of race-responsive neurons in the hippocampus predicted only White faces. Our results imply a distributed representation of race in brain areas involved in affective judgments, decision making, and memory. They also support the hypothesis that race-specific cues are perceptually coded even when those cues are task-irrelevant.

Eye movements reflect expertise development in hybrid search.

Domain-specific expertise changes the way people perceive, process, and remember information from that domain. This is often observed in visual domains involving skilled searches, such as athletics referees, or professional visual searchers (e.g., security and medical screeners). Although existing research has compared expert to novice performance in visual search, little work has directly documented how accumulating experiences change behavior. A longitudinal approach to studying visual search performance may permit a finer-grained understanding of experience-dependent changes in visual scanning, and the extent to which various cognitive processes are affected by experience. In this study, participants acquired experience by taking part in many experimental sessions over the course of an academic semester. Searchers looked for 20 categories of targets simultaneously (which appeared with unequal frequency), in displays with 0-3 targets present, while having their eye movements recorded. With experience, accuracy increased and response times decreased. Fixation probabilities and durations decreased with increasing experience, but saccade amplitudes and visual span increased. These findings suggest that the behavioral benefits endowed by expertise emerge from oculomotor behaviors that reflect enhanced reliance on memory to guide attention and the ability to process more of the visual field within individual fixations.

Deficits in cross-race face learning: insights from eye movements and pupillometry.

The own-race bias (ORB) is a well-known finding wherein people are better able to recognize and discriminate own-race faces, relative to cross-race faces. In 2 experiments, participants viewed Asian and Caucasian faces, in preparation for recognition memory tests, while their eye movements and pupil diameters were continuously monitored. In Experiment 1 (with Caucasian participants), systematic differences emerged in both measures as a function of depicted race: While encoding cross-race faces, participants made fewer (and longer) fixations, they preferentially attended to different sets of features, and their pupils were more dilated, all relative to own-race faces. Also, in both measures, a pattern emerged wherein some participants reduced their apparent encoding effort to cross-race faces over trials. In Experiment 2 (with Asian participants), the authors observed the same patterns, although the ORB favored the opposite set of faces. Taken together, the results suggest that the ORB appears during initial perceptual encoding. Relative to own-race face encoding, cross-race encoding requires greater effort, which may reduce vigilance in some participants.

Spotting rare items makes the brain "blink" harder: Evidence from pupillometry.

In many visual search tasks (e.g., cancer screening, airport baggage inspections), the most serious search targets occur infrequently. As an ironic side effect, when observers finally encounter important objects (e.g., a weapon in baggage), they often fail to notice them, a phenomenon known as the low-prevalence effect (LPE). Although many studies have investigated LPE search errors, we investigated the attentional consequences of successful rare target detection. Using an attentional blink paradigm, we manipulated how often observers encountered the first serial target (T1), then measured its effects on their ability to detect a following target (T2). Across two experiments, we show that the LPE is more than just an inflated miss rate: When observers successfully detected rare targets, they were less likely to spot subsequent targets. Using pupillometry to index locus-coeruleus (LC) mediated attentional engagement, Experiment 2 confirmed that an LC refractory period mediates the attentional blink (`Nieuwenhuis, Gilzenrat, Holmes, & Cohen, 2005, Journal of Experimental Psychology: General, 134[3], 291-307), and that these effects emerge relatively quickly following T1 onset. Moreover, in both behavioral and pupil analyses, we found that detecting low-prevalence targets exacerbates the LC refractory period. Consequences for theories of the LPE are discussed.

Incidental memory following rapid object processing: The role of attention allocation strategies.

When observers search for multiple (rather than singular) targets, they are slower and less accurate, yet have better incidental memory for nontarget items encountered during the task (Hout & Goldinger, 2010). One explanation for this may be that observers titrate their attention allocation based on the expected difficulty suggested by search cues. Difficult search cues may implicitly encourage observers to narrow their attention, simultaneously enhancing distractor encoding and hindering peripheral processing. Across three experiments, we manipulated the difficulty of search cues preceding passive visual search for real-world objects, using a Rapid Serial Visual Presentation (RSVP) task to equate item exposure durations. In all experiments, incidental memory was enhanced for distractors encountered while participants monitored for difficult targets. Moreover, in key trials, peripheral shapes appeared at varying eccentricities off center, allowing us to infer the spread and precision of participants' attentional windows. Peripheral item detection and identification decreased when search cues were difficult, even when the peripheral items appeared before targets. These results were not an artifact of sustained vigilance in miss trials, but instead reflect top-down modulation of attention allocation based on task demands. Implications for individual differences are discussed. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Retrieval dynamics of recognition and rejection.

Recognition memory is often viewed as the end-product of discrete cognitive events, involving the combination of latent operations such as the assessment of memory strength, the decision time, and the memory judgement. Recently, researchers have begun using the physical dynamics of memory retrieval to provide insight into the dynamic, possibly non-discrete, processes that underlie memory decisions. In this study, the underlying distributional properties of targets and lures were manipulated by populating lists with items drawn from either homogeneous or heterogeneous word frequency and context variability ranges. In all conditions, participants' x-, y-mouse coordinates were recorded as they processed test items, allowing estimates of response dynamics (e.g., initial deviation and area under the curve [AUC]), and eventual old/new responses. The stimulus manipulations affected the distribution shapes and, to a greater degree, the placements of subjective confidence thresholds. We observed tight correspondences between confidence and AUC for both hits and correct rejections. We interpret these results within dynamic models of recognition memory.

Photo ID verification remains challenging despite years of practice.

BACKGROUND: Matching unfamiliar faces to photographic identification (ID) documents occurs across many domains, including financial transactions (e.g., mortgage documents), controlling the purchase of age-restricted goods (e.g., alcohol sales), and airport security. Laboratory research has repeatedly documented the fallibility of this process in novice observers, but little research has assessed individual differences based on occupational expertise (cf. White et al., PLoS One 9:e103510, 2014; White et al., Proceedings of the Royal Society B 282(1814):20151292, 2015). In the present study, over 800 professional notaries (who routinely verify identity prior to witnessing signatures on legal documents), 70 bank tellers, and 35 undergraduate students completed an online unfamiliar face-matching test. In this test, observers made match/nonmatch decisions to 30 face ID pairs (half of which were matches), with no time constraints and no trial-by-trial feedback. RESULTS: Results showed that all groups performed similarly, although age was negatively correlated with accuracy. Critically, weekly and yearly experience with unfamiliar face matching did not impact performance. CONCLUSIONS: These results suggest that accumulated occupational experience has no bearing on unfamiliar face ID abilities and that cognitive declines associated with aging also manifest in unfamiliar face matching.