Memory for drawings in locations: Spatial source memory and event‐related potentials

ABSTRACTResearch showed that source memory functioning declines with ageing. Evidence suggests that encoding visual stimuli with manual pointing in addition to visual observation can have a positive effect on spatial memory compared with visual observation only. The present study investigated whether pointing at picture locations during encoding would lead to better spatial source memory than naming (Experiment 1) and visual observation only (Experiment 2) in young and older adults. Experiment 3 investigated whether response modality during the test phase would influence spatial source memory performance. Experiments 1 and 2 supported the hypothesis that pointing during encoding led to better source memory for picture locations than naming or observation only. Young adults outperformed older adults on the source memory but not the item memory task in both Experiments 1 and 2. In Experiments 1 and 2, participants manually responded in the test phase. Experiment 3 showed that if participants had to verbally respond in the test phase, the positive effect of pointing compared with naming during encoding disappeared. The results suggest that pointing at picture locations during encoding can enhance spatial source memory in both young and older adults, but only if the response modality is congruent in the test phase.

Introduction Remembering relationships between items (information) and the contexts (sources) in which they are framed is crucial for everyday functioning. Total sleep deprivation (TSD) impairs this ability, with evidence suggesting that TSD affects source memory even when items are remembered. Source memory deficits imply problems with associative memory, which relies on hippocampal functioning, known to be altered by TSD. Serotonin is highly expressed in the hippocampus, is influenced by TSD, and may be part of a mechanism by which TSD degrades source memory. We investigated the association between 5-HTTLPR, a functional length polymorphism of the human serotonin transporter gene (SLC6A4), and item and source memory during TSD. Methods N=34 healthy adults (ages 27.3±4.9y; 18 female) participated in a 4-day/3-night laboratory TSD study. Participants underwent 38h TSD, preceded and followed by 10h sleep opportunities. At baseline and 24h later during TSD, they completed an item/source memory task. Participants listened to a list of 60 words each presented by a male or female speaker (study phase). They were then tested for recognition of the words (items) out of 60 old and 60 new words presented visually, and were asked to identify the corresponding speakers (sources, male or female). Results The genotype distribution was in Hardy-Weinberg equilibrium (P=0.34), with 35.3% long/long, 41.2% long/short, 23.5% short/short. Mixed-effects ANOVA showed a significant adverse effect of TSD for both item recognition (P< 0.001) and source recognition (P< 0.001), where TSD degraded source memory even when item recognition was accurate. There were no 5-HTTLPR genotype effects on item memory. However, there was a significant main effect for genotype on source memory (P=0.019), and a genotype by TSD interaction (P=0.018). For accurately recognized items, source memory was largely preserved for the short/short genotype but impaired for carriers of the long allele, and especially the long/long genotype. Conclusion 5-HTTLPR genotype predicted source memory deficits from TSD, distinct from item memory deficits unaffected by genotype, which confirms that item and source memory deficits due to TSD are dissociable. Furthermore, TSD’s impact on binding of items and sources in memory may be mediated by hippocampal serotonin. Support (if any) NIH R21CA167691, WSU Anthony Marchionne and Foundry10 Bridge fellowships

The existence of a functional-anatomic dissociation for retrieving item versus contextual information within subregions of the medial temporal lobe (MTL) is currently under debate. We used a spatial source memory paradigm during event-related functional magnetic resonance imaging to investigate this issue. At study, abstract shapes were presented to the left or right of fixation. During test, old and new shapes were presented at fixation. Participants responded whether each shape had been previously presented on the “left,” the “right,” or was “new.” Activity associated with contextual memory (i.e., source memory) was isolated by contrasting accurate versus inaccurate memory for spatial location. Item-memory-related activity was isolated by contrasting accurate item recognition without contextual memory with forgotten items. Source memory was associated with activity in the hippocampus and parahippocampal cortex. Although item memory was not associated with unique MTL activity at our original threshold, a region-of-interest (ROI) analysis revealed item-memory-related activity in the perirhinal cortex. Furthermore, a functional-anatomic dissociation within the parietal cortex for retrieving item and contextual information was not found in any of three ROIs. These results support the hypothesis that specific subregions in the MTL are associated with item memory and memory for context.

Episodic memory is accounted for with two processes: ‘familiarity’ when generally recognizing an item and ‘recollection’ when retrieving the full contextual details bound with the item. Paradoxically, people sometimes report contextual information as familiar but without recollecting details, which is not easily accounted for by existing theories. We tested a combination of item recognition confidence and source memory, focusing upon ‘item-only hits with source unknown’ (‘item familiarity’), ‘low-confidence hits with correct source memory’ (‘context familiarity’), and ‘high-confidence hits with correct source memory’ (‘recollection’). Results across multiple within-subjects (trial-wise) and between subjects (individual variability) levels indicated these were behaviorally and physiologically distinct. Behaviorally, a crossover interaction was evident in response times, with context familiarity being slower than each condition during item recognition, but faster during source memory. Electrophysiologically, a Condition × Time × Location triple dissociation was evident in event-related potentials (ERPs), which was then independently replicated. Context familiarity exhibited an independent negative central effect from 800–1200 ms, differentiated from positive ERPs for item-familiarity (400 to 600 ms) and recollection (600 to 900 ms). These three conditions thus reflect mutually exclusive, fundamentally different processes of episodic memory. Context familiarity is a third distinct process of episodic memory.

Given the importance of memory to our daily functioning, humans have made use of many strategies to improve their encoding and later retrieval. Recently, drawing has emerged as a particularly effective strategy that robustly improves memory compared with traditional encoding strategies, and in the current study, we investigate the cognitive features that underlie this effect. Participants (N = 60) engaged in four distinct encoding tasks-Drawing, No Ink Drawing, Tracing, and Visualizing-each designed to engage one or more of the multisensory 'components' thought to underlie the impact of drawing on memory. We evaluated memory performance using both a classic old/new recognition task and source memory judgment, providing insights into both general recognition performance, and memory for specific encoding contexts. Consistent with prior work, we found Drawing led to the best memory performance in both recognition and source memory. Notably however, the No Ink Drawing condition, which lacked the visual component offered by Drawing, produced the second best old/new recognition performance, but the worst source memory. Unpacking this result, we found participants were frequently confusing No Ink Drawing with Drawing during source memory judgments, perhaps reflecting a hierarchy to the components that enhance memory, which seems to favor motoric engagement and elaboration over visual information. Together, our results extend our current understanding of the cognitive processes underlying successful encoding and provide new insights into how various memory tests can provide information about the specific information encoded alongside memories.

A circular analogue of the diffusion model adapted for continuous response tasks is applied to a continuous-outcome source memory task. In contrast to existing models of source retrieval that attribute all of the variability in responding to memory, the circular diffusion model decomposes noise into variability arising from memory and from decision processes. We compared three models: (1) a single diffusion process with trial-to-trial variability in drift rate, (2) a mixture of two diffusion processes, one with positive drift that does not vary from trial-to-trial, and a second zero-drift process that represents discrete guessing, and (3) a hybrid model that mixed positive and zero-drift processes with trial-to-trial variability in the positive drift process. Comparison of model fits to joint response error and response-time (RT) data suggest that a memory strength threshold under which no information is retrieved appears to underlie responding in a continuous-report source memory task. Additionally, we also conditioned participants' source responding on their confidence in an old/new recognition task, ruling out the possibility that participant guessing was only due to unrecognized items. Overall, our findings support an all-or-none or some-or none view of source memory retrieval and pose a challenge to continuous models of source memory.

A boost of confidence: The role of the ventromedial prefrontal cortex in memory, decision-making, and schemas

The Role of Medial Prefrontal Cortex in Memory and Decision Making

Event-related potentials (ERPs) were recorded during recognition tasks for spoken words alone (items) or for both words and the voice of the speaker (sources). Neither performance nor ERP measures suggested that voice information was retrieved automatically during the item-recognition task. In both tasks, correctly recognized old words elicited more positive ERPs than new words, beginning around 400 ms poststimulus onset. In the source task only, old words also elicited a focal prefrontal positivity beginning about 700 ms. The prefrontal task effect did not distinguish trials with accurate and inaccurate voice judgments and is interpreted as reflecting the search for voice information in memory. More posterior recording sites were sensitive to the successful recovery of voice or source information. The results indicate that word and voice information were retrieved hierarchically and distinguish retrieval attempt from retrieval success.

fMRI subsequent source memory effects in young, middle-aged and old adults

Children and adolescents with Williams-Beuren syndrome (WBS) have been described as having specific memory abilities and emotional reactivity. Although it is well established in the literature that emotion can enhance memory, no such studies have been undertaken in individuals with WBS. In three experiments, the present study tested whether the negative or positive emotional valence of stimuli can influence verbal, visual and visuo-spatial memory by specifically evaluating two memory components: item and associative memory. Sixteen 8- to 18-year-old individuals with WBS performed the first two experiments and, among them, twelve participated in the third. They were compared to equivalent groups of typically developing control children. Participants completed intentional-encoding tasks followed by immediate item recognition, associative recall or item recall tasks. Event-related potential measures during encoding and recognition of pictures were also added in the third experiment. Results demonstrated, for the first time, effects of emotions on visual item memory and visuo-spatial associative memory in individuals with WBS, that were similar to those observed in typically developing children. By combining behavioral and neural measures, our study provides new knowledge of the interaction between emotion and memory in WBS individuals, which seems to be unaffected by their atypical development.

Deletion of the GluA1 AMPA receptor subunit impairs short-term spatial recognition memory. It has been suggested that short-term recognition depends upon memory caused by the recent presentation of a stimulus that is independent of contextual–retrieval processes. The aim of the present set of experiments was to test whether the role of GluA1 extends to nonspatial recognition memory. Wild-type and GluA1 knockout mice were tested on the standard object recognition task and a context-independent recognition task that required recency-dependent memory. In a first set of experiments it was found that GluA1 deletion failed to impair performance on either of the object recognition or recency-dependent tasks. However, GluA1 knockout mice displayed increased levels of exploration of the objects in both the sample and test phases compared to controls. In contrast, when the time that GluA1 knockout mice spent exploring the objects was yoked to control mice during the sample phase, it was found that GluA1 deletion now impaired performance on both the object recognition and the recency-dependent tasks. GluA1 deletion failed to impair performance on a context-dependent recognition task regardless of whether object exposure in knockout mice was yoked to controls or not. These results demonstrate that GluA1 is necessary for nonspatial as well as spatial recognition memory and plays an important role in recency-dependent memory processes.

Chinese character unitization enhances item memory in addition to associative memory: Evidence from ERP and TFR

Episodic memory comprises memory for individual information units (item memory) and for the connections among them (associative memory). In two experiments using an object pair learning task, we examined the effect of visual stimulus complexity on memory encoding and retrieval mechanisms and on item and associative memory performance. Subjects encoded pairs of black monochrome object images (low complexity, LC condition) or color photographs of objects (high complexity, HC condition) via interactive imagery, and subsequently item and associative recognition were tested. In Experiment 1, event-related potentials (ERPs) revealed an enhanced frontal N2 during encoding and an enhanced late posterior negativity (LPN) during item recognition in the HC condition, suggesting that memory traces containing visually more complex objects elicited a stronger effort in reconstructing the past episode. Item memory was consistently superior in the HC compared to the LC condition. Associative memory was either statistically unaffected by complexity (Experiment 1) or improved (Experiment 2) in the HC condition, speaking against a tradeoff between resources allocated to item versus associative memory, and hence contradicting results of some prior studies. In Experiment 2, in both young and older adults, both item and associative memory benefitted from stimulus complexity, such that the magnitude of the age-related associative deficit was not influenced by stimulus complexity. Together, these results suggest that if familiar objects are presented in a form that exhibits a higher visual complexity, which may support semantic processing, complexity can benefit both item and associative memory. Stimulus properties that enhance item memory can scaffold associative memory in this situation.

Auditory beat stimulation is an upcoming technique for non-invasive brain stimulation. Its influence on mediotemporal regions and memory processes has not yet been thoroughly investigated. A recent study suggests that auditory beats are able to alter intracranial EEG (iEEG) power and phase synchronization. 5 Hz binaural beat stimulation increased temporo-lateral phase synchronization, while 5 Hz monaural beat stimulation decreased mediotemporal synchronization. Based on the relevance of phase synchronization for memory operations, we hypothesized that 5 Hz binaural beat stimulation enhances, while 5 Hz monaural beat stimulation decreases long-term memory performance. We analyzed data from presurgical epilepsy patients with implanted depth electrodes in the hippocampus and rhinal cortex. 5 Hz monaural and binaural beat vs. control stimulation was applied while patients performed an associative learning task involving item and source recognition. We evaluated behavioral effects for item (hits minus false alarms) and source memory (correct minus incorrect) and the impact of auditory beats on iEEG power, rhinal-hippocampal phase synchronization and inter-trial phase locking. A three-way repeated measures ANOVA (encoding/retrieval, item/source, monaural/binaural/control) revealed a main effect of stimulation (p = 0.03) and a linear effect in the expected direction: binaural > control > monaural (p = 0.036). Both monaural and binaural stimulation were associated with increased phase locking of 5 Hz oscillations within rhinal cortex. These phase locking increases, however, corresponded to reverse phase shifts. Our data suggest that binaural vs. monaural 5 Hz stimulation increases vs. decreases long-term memory performance. These behavioral effects appear to be related to reverse phase shifts within rhinal cortex.