The emergence of all-or-none retrieval of chunks in verbal serial recall.

People often subdivide a list into smaller pieces, called chunks. Some theories of serial recall assume memories are stored hierarchically, with all-or-none retrieval of chunks, but most mathematical models avoid hierarchical assumptions. Johnson (Journal of Verbal Learning and Verbal Behavior, 8(6), 725-731, 1969) found steep drops in errors following correct recalls (transitional-error probabilities) within putative chunks during multi-trial letter-list learning, and viewed this as evidence for all-or-none retrieval. Here we test whether all-or-none retrieval occurs in lists studied only once. In serial recall of six-word lists (Experiment 1), transitional-error probabilities were inconsistent with all-or-none retrieval, both when participants were instructed to subdivide and when temporal grouping induced subdivision. Curiously, the same analysis of previous temporally grouped nine-letter lists produced compelling evidence for all-or-none retrieval, which may result from recoding rather than the formation of chunks. In Experiment 2, participants were pre-trained on three-word chunks. For nine-word lists constructed from those trained chunks, transitional-error probabilities exhibited more pronounced evidence of all-or-none retrieval. Nearly all effects reversed with post-cued backward recall, suggesting mechanisms that play out over the course of recall rather than encoding of the list. In sum, subdivided lists do not result in hierarchical memories after a single study trial, although they may emerge in lists formed from chunks that are previously learned as such. This suggests a continuous transition from non-hierarchical subdivision of lists to all-or-none retrieval over the course of chunk formation.

The relationship between interactive-imagery instructions and association memory.

Interactive imagery, one of the most effective strategies for remembering pairs of words, involves asking participants to form mental images during study. We tested the hypothesis that the visual image is, in fact, responsible for its memory benefit. Neither subjectively reported vividness (all experiments) nor objective imagery skill (experiments 1 and 3) could explain the benefit of interactive imagery for cued recall. Aphantasic participants, who self-identified little to no mental imagery, benefited from interactive-imagery instructions as much as controls (experiment 3). Imagery instructions did not improve memory for the constituent order of associations (AB versus BA), even when participants were told how to incorporate order within their images (experiments 1 and 2). Taken together, our results suggest that the visual format of images may not be responsible for the effectiveness of the interactive-imagery instruction and moreover, interactive imagery may not result in qualitatively different associative memories.

Competition between Associations in Memory.

If two associations share an item, one may be remembered at the expense of the other (BC recalled but not AB). Here, we identify the neural processes by which this competition materializes and is resolved. We analyzed fMRI signal while participants studied sets of pairs that reliably induced pair-to-pair associative interference, but which participants could not fully resolve. Precuneus activity tracked retrieval of previous pairs during study of later overlapping pairs. This retrieval apparently produced interference by diverting study resources from the currently displayed pair. However, when activity in ventromedial prefrontal cortex, as well as anterior subregions of the hippocampus, was present while the earlier pair had been studied, interference was reversed, and both pairs were likely to be recalled. Angular gyrus and mid-frontal activity were related to interference resolution once the participant had seen both pairs. Taken together, associations compete via precuneus-mediated competitive retrieval, but ventromedial prefrontal cortex may neutralize this by ensuring that when the earlier association is remembered while studying the later pair, memories of the two pairs can overcome interference likely via activity in mid-frontal cortex and angular gyrus.

Mnemonic scaffolds vary in effectiveness for serial recall.

Memory champions remember vast amounts of information in order and at first encounter by associating each study item to an anchor within a scaffold - a pre-learned, structured memory. The scaffold provides direct-access retrieval cues. Dominated by the familiar-route scaffold (Method of Loci), researchers have little insight into what characteristics of scaffolds make them effective, nor whether individual differences might play a role. We compared participant-generated mnemonic scaffolds: (a) familiar routes (Loci), (b) autobiographical stories (Story), (c) parts of the human body (Body), and (d) routine activities (Routine Activity). Loci, Body, and Story Scaffolds benefited serial recall over Control (no scaffold). The Body and Loci Scaffold were equally superior to the other scaffolds. Measures of visual imagery aptitude and vividness and body responsiveness did not predict accuracy. A second experiment tested whether embodiment could be responsible for the high level of effectiveness of the Body Scaffold; this was not supported. In short, mnemonic scaffolds are not equally effective and embodied cognition may not directly contribute to memory success. The Body Scaffold may be a strong alternative to the Method of Loci and may enhance learning for most learners, including those who do not find the Method of Loci useful.

Emotional arousal impairs association memory: roles of prefrontal cortex regions.

The brain processes underlying impairing effects of emotional arousal on associative memory were previously attributed to two dissociable routes using high-resolution fMRI of the MTL (Madan et al. 2017). Extrahippocampal MTL regions supporting associative encoding of neutral pairs suggested unitization; conversely, associative encoding of negative pairs involved compensatory hippocampal activity. Here, whole-brain fMRI revealed prefrontal contributions: dmPFC was more involved in hippocampal-dependent negative pair learning and vmPFC in extrahippocampal neutral pair learning. Successful encoding of emotional memory associations may require emotion regulation/conflict resolution (dmPFC), while neutral memory associations may be accomplished by anchoring new information to prior knowledge (vmPFC).

Imagery-based strategies for memory for associations.

Cued recall of word pairs is improved by asking participants to combine items in an interactive image. Meanwhile, interactive images facilitate serial-recall (Link Method), but even better when each item is imagined alongside a previously learned peg-word (Peg List Method). We asked if a peg system could support memory for pairs, hypothesising it would outperform interactive imagery. Tested with cued recall, five study strategies were manipulated between-subjects, across two experiments: (1) Both words linked to one peg; (2) Each word linked to a different peg; (3) Peg list method but studying as a serial list; (4) Interactive imagery (within-pairs); (5) Link Method. Participants were able to apply peg-list strategies to pairs, as anticipated by mathematical modelling. Error-patterns spoke to mathematical models; peg lists exhibited distance-based confusability, characteristic of positional-coding models, and errors tended to preserve within-pair position, even for inter-item associative strategies, suggesting models of association should incorporate position. However, the peg list strategies came with a speed-accuracy tradeoff and did not challenge the superiority of the interactive imagery strategy. Without extensive practice with peg list strategies, interactive imagery remains superior for associations. Peg strategies may excel instead in tasks that primarily test serial order or with extensive training.

Predicting memory from study-related brain activity.

To isolate brain activity that may reflect effective cognitive processes during the study phase of a memory task, cognitive neuroscientists commonly contrast brain activity during study of later-remembered versus later-forgotten items. This "subsequent memory effect" method has been described as identifying brain activity "predictive" of memory outcome. However, the modern field of machine learning distinguishes between descriptive analysis, subject to overfitting, and true prediction, that can classify untrained data. First, we tested whether classic event-related potential signals were, in fact, predictive of later old/new recognition memory (N = 62, 225 items/participant); this produced significant but small predictive success. Next, pattern classification of the multivariate spatiotemporal features of the single-trial EEG waveform also succeeded in predicting memory. However, the prediction was still small in magnitude. In addition, topographic maps suggested individual differences in sources of predictive activity. These findings suggest that, on average, brain activity, measured by EEG, during the study phase is only marginally predictive of subsequent memory. It is possible that this predictive approach will succeed better when other experimental factors known to influence memory outcome are also integrated into the models.NEW & NOTEWORTHY For both basic and applied reasons, an important goal is to identify brain activity present while people study materials that enable us to predict whether they will remember those materials. We show that this is possible with the conventional event-related potential "subsequent-memory-effect" signals as well as with machine learning classifiers, but only to a small degree. This is in line with behavioral research, which supports many determinants of memory apart from the cognitive processes during study.

Temporal grouping and direction of serial recall.

When lists are presented with temporal pauses between groups of items, participants' response times reiterate those pauses. Accuracy is also increased, especially at particular serial positions. By comparing forward with backward serial recall, we tested whether the influence of temporal grouping is primarily a function of serial position or output position. Results favored the latter, both when recall direction was known to participants prior to (Experiment 2) or only after (Experiment 2) studying each list. Alongside fits of variants of a temporal distinctiveness-based model, our findings suggest that the influence of temporal grouping is not just a consequence of grouping information stored during the study phase. Rather, it critically depends on participants cueing with within-chunk position during recall, combined with response suppression.

Performance on an Associative Memory Test Decreases 8 hr After Cardiovascular Exercise.

This study was designed to assess the effects of acute exercise on performance of a paired associate learning (PAL) test, an operationalization of hippocampal-dependent associative memory. Participants performed a PAL test and then ran on a treadmill (exercise group, n = 52) or solved Sudoku puzzles (control group, n = 54). Participants returned 2, 5, or 8 hr later to perform a second, different, PAL test. PAL scores for the control group did not change over time. Similarly, scores on tests taken 2 and 5 hr after exercise were not different from baseline or control data. Scores on tests taken 8 hr after exercise, however, fell significantly below baseline (by 8.6%) and control (by 9.8%) scores. These data demonstrate that acute exercise can negatively affect the encoding and retrieval of new information even hours after the exercise bout, which should be a consideration when designing exercise programs to enhance, and not hinder, learning.

A hexagonal Fourier model of grid cells.

Grid cells in rat medial entorhinal cortex are widely thought to play a major role in spatial behavior. However, the exact computational role of the population of grid cells is not known. Here we provide a descriptive model, which nonetheless considers biologically feasible mechanisms, whereby the grid cells are viewed as a two-dimensional Fourier basis set, in hexagonal coordinates, with restricted availability of basis functions. With known properties imposed in the model parameters, we demonstrate how various empirical benchmark findings are straight-forward to understand in this model. We also explain how complex computations, inherent in a Fourier model, are feasible in the medial entorhinal cortex with simple mechanisms. We further suggest, based on model experiments, that grid cells may support a form of lossy compression of contextual information, enabling its representation in an efficient manner. In sum, this hexagonal Fourier model suggests how the entire population of grid cells may be modeled in a principled way, incorporates biologically feasible mechanisms and provides a potentially powerful interpretation of the relationship between grid-cell activity and contextual information beyond spatial knowledge. This enables various phenomena to be modeled with relatively simple mechanisms, and leads to novel and testable predictions.

Reduced associative memory for negative information: impact of confidence and interactive imagery during study.

Although item-memory for emotional information is enhanced, memory for associations between items is often impaired for negative, emotionally arousing compared to neutral information. We tested two possible mechanisms underlying this impairment, using picture pairs: 1) higher confidence in one's own ability to memorise negative information may cause participants to under-study negative pairs; 2) better interactive imagery for neutral pairs could facilitate associative memory for neutral pairs more than for negative pairs. Tested with associative recognition, we replicated the impairment of associative memory for negative pairs. We also replicated the result that confidence in future memory (judgments of learning) was higher for negative than neutral pairs. Inflated confidence could not explain the impairment of associative recognition memory: Judgements of learning were positively correlated with associative memory success for both negative and neutral pairs. However, neutral pairs were rated higher in their conduciveness to interactive imagery than negative pairs, and this difference in interactive imagery showed a robust relationship to the associative memory difference. Thus, associative memory reductions for negative information are not due to differences in encoding effort. Instead, interactive imagery may be less effective for encoding of negative than neutral pairs.

Intrusions in episodic memory: reconsolidation or interference?

It would be profoundly important if reconsolidation research in animals and other memory domains generalized to human episodic memory. A 3-d-list-discrimination procedure, based on free recall of objects, with a contextual reminder cue (the testing room), has been thought to demonstrate reconsolidation of human episodic memory (as noted in a previous study). Our goal was to replicate the central result, a high intrusion rate during recall of the target list, and evaluate the reconsolidation account relative to an alternative account, based on state-dependent learning and interference. First, replication was not straightforward (Experiment 1). Second, using a very unique, highly salient context (Experiment 2), the method produced a qualitative replication, but it was small in magnitude. A critical assumption of the reconsolidation account, that the target list is reactivated and destabilized during re-exposure to the study context, was not supported (Experiment 3). Although troubling for the reconsolidation account, the findings can be easily accommodated by an alternative account that does not assume additional neurobiological processes underlying the destabilization of consolidated memories, instead explaining intrusion rates simply in terms of well-established cognitive effects, such as item-to-context binding and interference during retrieval.

Rhythmic Activity and Individual Variability in Recognition Memory: Theta Oscillations Correlate with Performance whereas Alpha Oscillations Correlate with ERPs.

During study trials of a recognition memory task, alpha (∼10 Hz) oscillations decrease, and concurrently, theta (4-8 Hz) oscillations increase when later memory is successful versus unsuccessful (subsequent memory effect). Likewise, at test, reduced alpha and increased theta activity are associated with successful memory (retrieval success effect). Here we take an individual-differences approach to test three hypotheses about theta and alpha oscillations in verbal, old/new recognition, measuring the difference in oscillations between hit trials and miss trials. First, we test the hypothesis that theta and alpha oscillations have a moderately mutually exclusive relationship; but no support for this hypothesis was found. Second, we test the hypothesis that theta oscillations explain not only memory effects within participants, but also individual differences. Supporting this prediction, durations of theta (but not alpha) oscillations at study and at test correlated significantly with d' across participants. Third, we test the hypothesis that theta and alpha oscillations reflect familiarity and recollection processes by comparing oscillation measures to ERPs that are implicated in familiarity and recollection. The alpha-oscillation effects correlated with some ERP measures, but inversely, suggesting that the actions of alpha oscillations on memory processes are distinct from the roles of familiarity- and recollection-linked ERP signals. The theta-oscillation measures, despite differentiating hits from misses, did not correlate with any ERP measure; thus, theta oscillations may reflect elaborative processes not tapped by recollection-related ERPs. Our findings are consistent with alpha oscillations reflecting visual inattention, which can modulate memory, and with theta oscillations supporting recognition memory in ways that complement the most commonly studied ERPs.

Emotional arousal impairs association-memory: Roles of amygdala and hippocampus.

Emotional arousal is well-known to enhance memory for individual items or events, whereas it can impair association memory. The neural mechanism of this association memory impairment by emotion is not known: In response to emotionally arousing information, amygdala activity may interfere with hippocampal associative encoding (e.g., via prefrontal cortex). Alternatively, emotional information may be harder to unitize, resulting in reduced availability of extra-hippocampal medial temporal lobe support for emotional than neutral associations. To test these opposing hypotheses, we compared neural processes underlying successful and unsuccessful encoding of emotional and neutral associations. Participants intentionally studied pairs of neutral and negative pictures (Experiments 1-3). We found reduced association-memory for negative pictures in all experiments, accompanied by item-memory increases in Experiment 2. High-resolution fMRI (Experiment 3) indicated that reductions in associative encoding of emotional information are localizable to an area in ventral-lateral amygdala, driven by attentional/salience effects in the central amygdala. Hippocampal activity was similar during both pair types, but a left hippocampal cluster related to successful encoding was observed only for negative pairs. Extra-hippocampal associative memory processes (e.g., unitization) were more effective for neutral than emotional materials. Our findings suggest that reduced emotional association memory is accompanied by increases in activity and functional coupling within the amygdala. This did not disrupt hippocampal association-memory processes, which indeed were critical for successful emotional association memory formation.

Word Imageability Enhances Association-memory by Increasing Hippocampal Engagement.

The hippocampus is thought to support association-memory, particularly when tested with cued recall. One of the most well-known and studied factors that influences accuracy of verbal association-memory is imageability; participants remember pairs of high-imageability words better than pairs of low-imageability words. High-imageability words are also remembered better in tests of item-memory. However, we previously found that item-memory effects could not explain the enhancement in cued recall, suggesting that imageability enhances association-memory strength. Here we report an fMRI study designed to ask, what is the role of the hippocampus in the memory advantage for associations due to imageability? We tested two alternative hypotheses: (1) Recruitment Hypothesis: High-imageability pairs are remembered better because they recruit the underlying hippocampal association-memory function more effectively. Alternatively, (2) Bypassing Hypothesis: Imageability functions by making the association-forming process easier, enhancing memory in a way that bypasses the hippocampus, as has been found, for example, with explicit unitization imagery strategies. Results found, first, hippocampal BOLD signal was greater during study and recall of high- than low-imageability word pairs. Second, the difference in activity between recalled and forgotten pairs showed a main effect, but no significant interaction with imageability, challenging the bypassing hypothesis, but consistent with the predictions derived from the recruitment hypothesis. Our findings suggest that certain stimulus properties, like imageability, may leverage, rather than avoid, the associative function of the hippocampus to support superior association-memory.

Distinguishing rhythmic from non-rhythmic brain activity during rest in healthy neurocognitive aging.

Rhythmic brain activity at low frequencies (<12Hz) during rest are thought to increase in neurodegenerative disease, but findings in healthy neurocognitive aging are mixed. Here we address two reasons conventional spectral analyses may have led to inconsistent results. First, spectral-power measures are compared to a baseline condition; when resting activity is the signal of interest, it is unclear what the baseline should be. Second, conventional methods do not clearly differentiate power due to rhythmic versus non-rhythmic activity. The Better OSCillation detection method (BOSC; Caplan et al., 2001; Whitten et al., 2011) avoids these problems by using the signal's own spectral characteristics as a reference to detect elevations in power lasting a few cycles. We recorded electroencephalographic (EEG) signal during rest, alternating eyes open and closed, in healthy younger (18-25 years) and older (60-74 years) participants. Topographic plots suggested the conventional and BOSC analyses measured different sources of activity, particularly at frequencies, like delta (1-4Hz), at which rhythms are sporadic; topographies were more similar in the 8-12Hz alpha band. There was little theta-band activity meeting the BOSC method's criteria, suggesting prior findings of theta power in healthy aging may reflect non-rhythmic signal. In contrast, delta oscillations were present at higher levels than theta in both age groups. In summary, applying strict and standardized criteria for rhythmicity, slow rhythms appear present in the resting brain at delta and alpha, but not theta frequencies, and appear unchanged in healthy aging.

A perception-based ERP reveals that the magnitude of delay matters for memory-guided reaching.

Delayed action research has suggested that perceptual information about a visual stimulus decays over several seconds. With event-related potential (ERP) methodology, one should be able to track the time course of the electrophysiological processes associated with this decay. Recently, Cruikshank et al. (J Vis 12:29, 2012) found that the N170 ERP component reflected ventral stream processes linked to motor planning and perception for action. Specifically, the N170 was larger for actions that relied on perceptual-based information. However, the delay interval was very short (tens of ms). Behavioral and neuroimaging studies suggest that when longer delays are employed, reactivation of ventral areas is necessary in order to access a stored representation of the target's characteristics. Therefore, the N170 may reflect not only the perception-for-action processes, but also the accuracy of the representation. In order to test this, we traced the time course of the N170 in memory-guided reaching when 1-, 2-, and 3-s delays separated target occlusion and response initiation. During reach initiation, the N170 was more negative and peaked earlier for the 1 s than the 2- and 3-s delays and correlated significantly with performance at the longest delay. These results suggest that the neural mechanisms involved in movement planning change for delays beyond 1 s. The smaller N170 may reflect an impoverished visual perceptual representation in the ventral stream. To our knowledge, these are the first electrophysiological results to suggest that there is decay of visual perceptual information that occurs with increasing time.

Is what goes in what comes out? Encoding and retrieval event-related potentials together determine memory outcome.

Understanding memory function amounts to identifying how events (cognitive and neural) at study eventually influence events at test. Many of the proposed cognitive correlates of memory-related event-related potentials (ERPs) at study resemble proposed cognitive correlates of other memory-related ERPs, recorded at test. We wondered whether a given known ERP feature at study might in fact reflect an effective-encoding process that is, in turn, tapped by another specific ERP feature, recorded at test. To this end, we asked which pairs of known memory-related ERP features explain common variance across a large sample of participants, while they perform a word-recognition task. Two early ERP features, the Late Positive Component (study) and the FN400 (test), covaried significantly. These features also correlated with memory success (d' and response time). Two later ERP features, the Slow Wave (study) and the Late Parietal Positivity (test), also covaried when lures were incorporated into the analysis. Interestingly, these later features were uncorrelated with memory outcome. This novel approach, exploiting naturally occurring subject variability (in strategy and ERP amplitudes), informs our understanding of the memory functions of ERP features in several ways. Specifically, they strengthen the argument that the earlier ERP features may drive old/new recognition (but perhaps not the later features). Our findings suggest the Late Positive Component at study, in some degree, may cause the FN400 to increase at test, together producing effective recognition memory. The Slow Wave at study appears to relate the Left Parietal Positivity at test, but these may play roles in more complex memory judgments and may be less critical for simple old/new recognition.

Generality of a congruity effect in judgements of relative order.

The judgement of relative order (JOR) procedure is used to investigate serial-order memory. Measuring response times, the wording of the instructions (whether the earlier or the later item was designated as the target) reversed the direction of search in subspan lists (Chan, Ross, Earle, & Caplan Psychonomic Bulletin & Review, 16(5), 945-951, 2009). If a similar congruity effect applied to above-span lists and, furthermore, with error rate as the measure, this could suggest how to model order memory across scales. Participants performed JORs on lists of nouns (Experiment 1: list lengths = 4, 6, 8, 10) or consonants (Experiment 2: list lengths = 4, 8). In addition to the usual distance, primacy, and recency effects, instructions interacted with serial position of the later probe in both experiments, not only in response time, but also in error rate, suggesting that availability, not just accessibility, is affected by instructions. The congruity effect challenges current memory models. We fitted Hacker's (Journal of Experimental Psychology: Human Learning and Memory, 6(6), 651-675, 1980) self-terminating search model to our data and found that a switch in search direction could explain the congruity effect for short lists, but not longer lists. This suggests that JORs may need to be understood via direct-access models, adapted to produce a congruity effect, or a mix of mechanisms.

Lack of effects of acute exercise intensity on mnemonic discrimination.

The hippocampus is thought to support episodic memory by pattern separation, thereby supporting the ability to discriminate high similarity items. Past research evaluating whether acute exercise can improve mnemonic discrimination of high similarity items is mixed. The present experiment attempts to extend these prior mixed findings by evaluating the effects of multiple exercise intensities on hippocampal-dependent, mnemonic discrimination and memory performance. Fifty-seven young adults completed a three-condition (control, moderate-intensity, and vigorous-intensity), within-subjects crossover pretest-posttest comparison. We observed no effects of acute exercise on recognition memory or mnemonic discrimination. We discuss the implications of these null findings with the broader literature by discussing the complexity of this potential exercise-mnemonic discrimination relationship, including the unique role of exercise intensity, differences in the level of processing (e.g., conceptual vs. perceptual), and unique brain regions involved in mnemonic discrimination.