Ask how they did it: untangling the relationships between task-specific strategy use, everyday strategy use, and associative memory.

OBJECTIVE: Past research has shown that self-reported everyday strategy use and task-specific strategy use are related to associative memory performance in aging. Understudied is the relationship between these types of strategy use, whether they predict associative memory performance, and how this may differ across genders. METHOD: A sample of older adults (N = 566, 53% female, ages 60-80) completed this online study. Study measures included 1. Multifactorial Memory Questionnaire (MMQ) Strategy Use subscale, a self-report measure of everyday strategy use, 2. Face-Name Task (FNT), a measure of associative memory, and 3. self-initiated number and types of strategies used on the FNT. Analyses examined the interrelationships among all study measures and their relative contributions to FNT performance while accounting for intraindividual factors. RESULTS: Participants who reported using more strategies on the FNT performed better than those who used fewer or no strategies; those who reported using at least three strategies and relating FNT to past experience performed best. Women outperformed men on the FNT but did not differ in task-specific strategy use. Participants who reported using no strategies on the FNT had lower MMQ Strategy Use scores. A multiple regression analysis indicated that female gender and using at least two task strategies were significant predictors of greater FNT performance. CONCLUSIONS: The results indicate that task-specific strategy use relates more to associative memory performance than to everyday strategy use, but neither accounts for the female advantage in FNT performance. Findings encourage querying task-specific strategy use to contextualize age-related associative memory decline.

Organization of pRF size along the AP axis of the hippocampus and adjacent medial temporal cortex is related to specialization for scenes versus faces.

The hippocampus is largely recognized for its integral contributions to memory processing. By contrast, its role in perceptual processing remains less clear. Hippocampal properties vary along the anterior-posterior (AP) axis. Based on past research suggesting a gradient in the scale of features processed along the AP extent of the hippocampus, the representations have been proposed to vary as a function of granularity along this axis. One way to quantify such granularity is with population receptive field (pRF) size measured during visual processing, which has so far received little attention. In this study, we compare the pRF sizes within the hippocampus to its activation for images of scenes versus faces. We also measure these functional properties in surrounding medial temporal lobe (MTL) structures. Consistent with past research, we find pRFs to be larger in the anterior than in the posterior hippocampus. Critically, our analysis of surrounding MTL regions, the perirhinal cortex, entorhinal cortex, and parahippocampal cortex shows a similar correlation between scene sensitivity and larger pRF size. These findings provide conclusive evidence for a tight relationship between the pRF size and the sensitivity to image content in the hippocampus and adjacent medial temporal cortex.

Retrieval of temporal structure at recall can occur automatically.

Temporal-structure, namely, the order in which events unfold over time, is one of the fundamental principles of episodic memory organization. A seminal empirical demonstration of the prominence of temporal structure in memory organization is the Temporal Contiguity Effect (TCE), whereby the proximity between two items at encoding predicts the likelihood of those two items being retrieved consecutively during recall. Recent studies have found that TCE occurs under a wide variety of conditions in which strategic control processes at encoding are reduced or even eliminated. This suggests that the encoding of temporal structure occurs automatically. Extending these findings, in the current study we asked whether the retrieval of temporal structure, as reflected by indices of the TCE, is influenced by strategic control processes at retrieval. To manipulate participants' ability to rely on strategic control processes, we compared standard recall performance (Full Attention condition) to a condition in which attention was divided between recall and a concurrent task (Divided Attention condition), which has been shown to disrupt such control processes. Across two experiments-one with standard encoding conditions and one with continual distraction during encoding-we found no differences in any index of the TCE between the two conditions. These results are all the more striking considering that in both experiments, dividing attention negatively affected overall recall performance compared to the Full Attention condition. Thus, while recall performance is reduced when disrupting strategic processes, the ability to use temporal structure to drive recall is not affected.

Sex and menstrual cycle influence human spatial navigation strategies and performance.

Which facets of human spatial navigation do sex and menstrual cycle influence? To answer this question, a cross-sectional online study of reproductive age women and men was conducted in which participants were asked to demonstrate and self-report their spatial navigation skills and strategies. Participants self-reported their sex and current menstrual phase [early follicular (EF), late follicular/periovulatory (PO), and mid/late luteal (ML)], and completed a series of questionnaires and tasks measuring self-reported navigation strategy use, topographical memory, cognitive map formation, face recognition, and path integration. We found that sex influenced self-reported use of cognitive map- and scene-based strategies, face recognition, and path integration. Menstrual phase moderated the influence of sex: compared to men, women had better face recognition and worse path integration, but only during the PO phase; PO women were also better at path integration in the presence of a landmark compared to EF + ML women and men. These findings provide evidence that human spatial navigation varies with the menstrual cycle and suggest that sensitivity of the entorhinal cortex and longitudinal axis of the hippocampus to differential hormonal effects may account for this variation.

Ready for action! When the brain learns, yet memory-biased action does not follow.

Does memory prepare us to act? Long-term memory can facilitate signal detection, though the degree of benefit varies and can even be absent. To dissociate between learning and behavioral expression of learning, we used high-density electroencephalography (EEG) to assess memory retrieval and response processing. At learning, participants heard everyday sounds. Half of these sound clips were paired with an above-threshold lateralized tone, such that it was possible to form incidental associations between the sound clip and the location of the tone. Importantly, attention was directed to either the sound clip (Experiment 1) or the tone (Experiment 2). Participants then completed a novel detection task that separated cued retrieval from response processing. At retrieval, we observed a striking brain-behavior dissociation. Learning was observed neurally in both experiments. Behaviorally, however, signal detection was only facilitated in Experiment 2, for which there was an accompanying explicit memory for tone presence. Further, implicit neural memory for tone location correlated with the degree of response preparation, but not response execution. Together, the findings suggest 1) that attention at learning affects memory-biased action and 2) that memory prepared action via both explicit and implicit associative memory, with the latter triggering response preparation.

Differential involvement of the anterior and posterior hippocampus, parahippocampus, and retrosplenial cortex in making precise judgments of spatial distance and object size for remotely acquired memories of environments and objects.

The hippocampus is known to support processing of precise spatial information in recently learned environments. It is less clear, but crucial for theories of systems consolidation, to know whether it also supports processing of precise spatial information in familiar environments learned long ago and whether such precision extends to objects and numbers. In this fMRI study, we asked participants to make progressively more refined spatial distance judgments among well-known Toronto landmarks (whether landmark A is closer to landmark B or C) to examine hippocampal involvement. We also tested whether the hippocampus was similarly engaged in estimating magnitude regarding sizes of familiar animals and numbers. We found that the hippocampus was only engaged in spatial judgment. Activation was greater and lasted longer in the posterior than anterior hippocampus, which instead showed greater modulation as discrimination between spatial distances became more fine grained. These findings suggest that the anterior and posterior hippocampus have different functions which are influenced differently by estimation of differential distance. Similarly, parahippocampal-place-area and retrosplenial cortex were involved only in the spatial condition. By contrast, activation of the intraparietal sulcus was modulated by precision in all conditions. Therefore, our study supports the idea that the hippocampus and related structures are implicated in retrieving and operating even on remote spatial memories whenever precision is required, as posted by some theories of systems consolidation.

Neurocognitive Model of Schema-Congruent and -Incongruent Learning in Clinical Disorders: Application to Social Anxiety and Beyond.

Negative schemas lie at the core of many common and debilitating mental disorders. Thus, intervention scientists and clinicians have long recognized the importance of designing effective interventions that target schema change. Here, we suggest that the optimal development and administration of such interventions can benefit from a framework outlining how schema change occurs in the brain. Guided by basic neuroscientific findings, we provide a memory-based neurocognitive framework for conceptualizing how schemas emerge and change over time and how they can be modified during psychological treatment of clinical disorders. We highlight the critical roles of the hippocampus, ventromedial prefrontal cortex, amygdala, and posterior neocortex in directing schema-congruent and -incongruent learning (SCIL) in the interactive neural network that comprises the autobiographical memory system. We then use this framework, which we call the SCIL model, to derive new insights about the optimal design features of clinical interventions that aim to strengthen or weaken schema-based knowledge through the core processes of episodic mental simulation and prediction error. Finally, we examine clinical applications of the SCIL model to schema-change interventions in psychotherapy and provide cognitive-behavior therapy for social anxiety disorder as an illustrative example.

From cognitive maps to spatial schemas.

A schema refers to a structured body of prior knowledge that captures common patterns across related experiences. Schemas have been studied separately in the realms of episodic memory and spatial navigation across different species and have been grounded in theories of memory consolidation, but there has been little attempt to integrate our understanding across domains, particularly in humans. We propose that experiences during navigation with many similarly structured environments give rise to the formation of spatial schemas (for example, the expected layout of modern cities) that share properties with but are distinct from cognitive maps (for example, the memory of a modern city) and event schemas (such as expected events in a modern city) at both cognitive and neural levels. We describe earlier theoretical frameworks and empirical findings relevant to spatial schemas, along with more targeted investigations of spatial schemas in human and non-human animals. Consideration of architecture and urban analytics, including the influence of scale and regionalization, on different properties of spatial schemas may provide a powerful approach to advance our understanding of spatial schemas.

Recollection and prior knowledge recruit the left angular gyrus during recognition.

The human angular gyrus (AG) is implicated in recollection, or the ability to retrieve detailed memory content from a specific episode. A separate line of research examining the neural bases of more general mnemonic representations, extracted over multiple episodes, also highlights the AG as a core region of interest. To reconcile these separate views of AG function, the present fMRI experiment used a Remember-Know paradigm with famous (prior knowledge) and non-famous (no prior knowledge) faces to test whether AG activity could be modulated by both task-specific recollection and general prior knowledge within the same individuals. Increased BOLD activity in the left AG was observed during both recollection in the absence of prior knowledge (recollected > non-recollected or correctly rejected non-famous faces) and when prior knowledge was accessed in the absence of experiment-specific recollection (famous > non-famous correct rejections). This pattern was most prominent for the left AG as compared to the broader inferior parietal lobe. Recollection-related responses in the left AG increased with encoding duration and prior knowledge, despite prior knowledge being incidental to the recognition decision. Overall, the left AG appears sensitive to both task-specific recollection and the incidental access of general prior knowledge, thus broadening our notions of the kinds of mnemonic representations that drive activity in this region.

Single voxel autocorrelation uncovers gradients of temporal dynamics in the hippocampus and entorhinal cortex during rest and navigation.

During navigation, information at multiple scales needs to be integrated. Single-unit recordings in rodents suggest that gradients of temporal dynamics in the hippocampus and entorhinal cortex support this integration. In humans, gradients of representation are observed, such that granularity of information represented increases along the long axis of the hippocampus. The neural underpinnings of this gradient in humans, however, are still unknown. Current research is limited by coarse fMRI analysis techniques that obscure the activity of individual voxels, preventing investigation of how moment-to-moment changes in brain signal are organized and how they are related to behavior. Here, we measured the signal stability of single voxels over time to uncover previously unappreciated gradients of temporal dynamics in the hippocampus and entorhinal cortex. Using our novel, single voxel autocorrelation technique, we show a medial-lateral hippocampal gradient, as well as a continuous autocorrelation gradient along the anterolateral-posteromedial entorhinal extent. Importantly, we show that autocorrelation in the anterior-medial hippocampus was modulated by navigational difficulty, providing the first evidence that changes in signal stability in single voxels are relevant for behavior. This work opens the door for future research on how temporal gradients within these structures support the integration of information for goal-directed behavior.

Transcranial magnetic stimulation to the angular gyrus modulates the temporal dynamics of the hippocampus and entorhinal cortex.

Transcranial magnetic stimulation (TMS) delivered to the angular gyrus (AG) affects hippocampal function and associated behaviors (Thakral PP, Madore KP, Kalinowski SE, Schacter DL. Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking. 2020a. Proc Natl Acad Sci U S A. 117:12729-12740). Here, we examine if functional magnetic resonance imaging (fMRI)-guided TMS disrupts the gradient organization of temporal signal properties, known as the temporal organization, in the hippocampus (HPC) and entorhinal cortex (ERC). For each of 2 TMS sessions, TMS was applied to either a control site (vertex) or to a left AG target region (N = 18; 14 females). Behavioral measures were then administered, and resting-state scans were acquired. Temporal dynamics were measured by tracking change in the fMRI signal (i) "within" single voxels over time, termed single-voxel autocorrelation and (ii) "between" different voxels over time, termed intervoxel similarity. TMS reduced AG connectivity with the hippocampal target and induced more rapid shifting of activity in single voxels between successive time points, lowering the single-voxel autocorrelation, within the left anteromedial HPC and posteromedial ERC. Intervoxel similarity was only marginally affected by TMS. Our findings suggest that hippocampal-targeted TMS disrupts the functional properties of the target site along the anterior/posterior axis. Further studies should examine the consequences of altering the temporal dynamics of these medial temporal areas to the successful processing of episodic information under task demand.

Early mobile app training proficiency predicts how well memory-impaired individuals learn to use digital memory aids in the real world.

Functional memory impairment following acquired brain injury can lead to decreased independence. External memory aids such as smartphones can be highly effective compensation tools, but cognitive deficits may create barriers to implementation in daily life. The present study examined predictors of real-world use of mobile calendar applications for memory compensation in an acquired brain injury sample. A retrospective chart review was completed from an outpatient rehabilitation program, extending 15 years into the past, yielding data from 34 eligible participants. All participants demonstrated skill learning of the calendar function in their digital device and subsequently completed the generalization phase of training, which is focused on real-world implementation (measured through prospective memory tasks). The results showed that the length of time required for skill learning of mobile calendars (event entry or responding to alerts) was not predictive of the duration of generalization training. Initial training performance for responding to alerts, but not event entry, was a significant predictor of the duration of generalization training needed to complete the program. A secondary analysis with a subset of the data revealed that individuals with additional executive deficits took significantly longer to complete generalization training compared to those with a more focal memory impairment.

Has the concept of systems consolidation outlived its usefulness? Identification and evaluation of premises underlying systems consolidation.

Systems consolidation has mostly been treated as a neural construct defined by the time-dependent change in memory representation from the hippocampus (HPC) to other structures, primarily the neocortex. Here, we identify and evaluate the explicit and implicit premises that underlie traditional or standard models and theories of systems consolidation based on evidence from research on humans and other animals. We use the principle that changes in neural representation over time and experience are accompanied by corresponding changes in psychological representations, and vice versa, to argue that each of the premises underlying traditional or standard models and theories of systems consolidation is found wanting. One solution is to modify or abandon the premises or theories and models. This is reflected in moderated models of systems consolidation that emphasize the early role of the HPC in training neocortical memories until they stabilize. The fault, however, may lie in the very concept of systems consolidation and its defining feature. We propose that the concept be replaced by one of memory systems reorganization, which does not carry the theoretical baggage of systems consolidation and is flexible enough to capture the dynamic nature of memory from inception to very long-term retention and retrieval at a psychological and neural level. The term "memory system reorganization" implies that memory traces are not fixed, even after they are presumably consolidated. Memories can continue to change as a result of experience and interactions among memory systems across the lifetime. As will become clear, hippocampal training of neocortical memories is only one type of such interaction, and not always the most important one, even at inception. We end by suggesting some principles of memory reorganization that can help guide research on dynamic memory processes that capture corresponding changes in memory at the psychological and neural levels.

Sex differences in item and associative memory among older adults with amnestic mild cognitive impairment.

In older adults without cognitive impairment, women have an advantage over men in verbal memory tests; however, whether women with amnestic mild cognitive impairment (aMCI) exhibit this advantage remains controversial. We evaluated sex-specific differences in older adults with and without aMCI in item and associative verbal memory by using an associative memory task with immediate and delayed recognition conditions. The associations between memory task performances and medial temporal morphometric measures were examined. The study included 49 individuals with aMCI and 55 healthy older adults (HOs). The results revealed that a female advantage in immediate item and delayed associative memory was evident in HOs, and the female advantage in associative memory persisted even after item memory performance was controlled. By contrast, the female advantage was absent in individuals with aMCI; such women had more associative false alarms than men with aMCI. Furthermore, decreases in item memory, associative memory, and cortical thickness in the perirhinal and entorhinal regions in individuals with aMCI versus their sex-matched controls were more prominent in women than in men. The relation between brain structure and associative memory function was evident only for women, indicating that women and men may have different cognitive and neural mechanisms for processing associative memory. These findings support the concept of cognitive reserve in women during normal aging. Accounting for sex differences in verbal memory performance is crucial to improve aMCI identification, particularly for women.

I remember therefore I am: Episodic memory retrieval and self-reported trait empathy judgments in young and older adults and individuals with medial temporal lobe excisions.

How do we know what sort of people we are? Do we reflect on specific past instances of our own behaviour, or do we just have a general idea? Previous work has emphasized the role of personal semantic memory (general autobiographical knowledge) in how we assess our own personality traits. Using a standardized trait empathy questionnaire, we show in four experiments that episodic autobiographical memory (memory for specific personal events) is associated with people's judgments of their own trait empathy. Specifically, neurologically healthy young adults rated themselves as more empathic on questionnaire items that cued episodic memories of events in which they behaved empathically. This effect, however, was diminished in people who are known to have poor episodic memory: older adults and individuals who have undergone unilateral excision of medial temporal lobe tissue (as treatment for epilepsy). Further, self-report ratings on individual questionnaire items were generally predicted by subjectively rated phenomenological qualities of the memories cued by those items, such as sensory detail, scene coherence, and overall vividness. We argue that episodic and semantic memory play different roles with respect to self-knowledge depending on life experience, the integrity of the medial temporal lobes, and whether one is assessing general abstract traits versus more concrete behaviours that embody these traits. Future research should examine different types of self-knowledge as well as personality traits other than empathy.

Mobile app learning in memory intervention for acquired brain injury: Neuropsychological associations of training duration.

Memory impairment is a common consequence of acquired brain injury, often leading to functional difficulties day-to-day and decreased independence. Memory Link is a theory-driven training programme for individuals with moderate-to-severe memory dysfunction, which enables the acquisition of digital device skills for functional compensation. The present study examined how neuropsychological functioning and initial training performance contribute to training duration in our outpatient memory rehabilitation programme. A retrospective chart review was conducted, extending 12 years into the past, yielding data from 37 eligible participants. All participants demonstrated skill learning of the calendar function in their digital device to the criterion point. The results showed that performance on neuropsychological tests of explicit memory (e.g., CVLT-II, BVMT-R), processing speed (e.g., Digit Symbol Coding, Trail Making sequencing), executive functioning (e.g., Trail Making switching), and perceptual ability (i.e., Block Design) were significantly associated with training duration to learn the core steps of calendar use. Furthermore, linear regression revealed that initial training performance was a significant predictor of training duration. Lastly, profile of cognitive impairment, with regard to severity of memory functioning and the presence of additional deficits, was found to be a significant factor contributing to how many training trials were required to learn application skills.

Differential Influence of Ventromedial Prefrontal Cortex Lesions on Neural Representations of Schema and Semantic Category Knowledge.

Prior knowledge, such as schemas or semantic categories, influences our interpretation of stimulus information. For this to transpire, prior knowledge must first be reinstated and then instantiated by being applied to incoming stimuli. Previous neuropsychological models implicate the ventromedial prefrontal cortex (vmPFC) in mediating these functions for schemas and the anterior/lateral temporal lobes and related structures for categories. vmPFC, however, may also affect processing of semantic category information. Here, the putative differential role of the vmPFC in the reinstatement and instantiation of schemas and semantic categories was examined by probing network-level oscillatory dynamics. Patients with vmPFC damage (n = 11) and healthy controls (n = 13) were instructed to classify words according to a given schema or category, while electroencephalography was recorded. As reinstatement is a preparatory process, we focused on oscillations occurring 500 msec prior to stimulus presentation. As instantiation occurs at stimulus presentation, we focused on oscillations occurring between stimulus presentation and 1000 msec poststimulus. We found that reinstatement was associated with prestimulus, theta and alpha desynchrony between vmPFC and the posterior parietal cortex for schemas, and between lateral temporal lobe and inferotemporal cortex for categories. Damage to the vmPFC influenced both schemas and categories, but patients with damage to the subcallosal vmPFC showed schema-specific deficits. Instantiation showed similar oscillatory patterns in the poststimulus time frame, but in the alpha and beta frequency bands. Taken together, these findings highlight distinct but partially overlapping neural mechanisms implicated in schema- and category-mediated processing.

Aging, pattern separation, and categorical perception of faces.

Categorical perception (CP) is the phenomenon by which observers view linear changes that occur across a continuum as distinct categories. Although categorical perception is a perceptual phenomenon, it may be subserved by mnemonic processes such as pattern separation. To examine this hypothesis, following standard CP tasks, we assessed younger and older participants' abilities to identify and discriminate between members of pairs of famous or non-famous faces. We hypothesized that if CP is dependent upon neural pattern separation, which declines with aging, discrimination ability as indexed by CP would be compromised in older adults, as was found in our study. Since familiarity promotes pattern separation, CP should be enhanced for famous, as compared to non-famous faces, even in older adults. We found that all participants benefited from familiarity, but younger adults outperformed older adults overall. We next examined the effects of face inversion on CP for both famous and non-famous faces. If pattern separation, and CP, is determined solely by the similarity across physical features, then CP should be similar for upright and inverted faces since these features are perceptually invariant across orientation. If, however, pattern separation, and CP, depends on how stimuli are represented, then orientation may matter as upright and inverted faces are represented holistically or part-based, respectively. We found that inversion disrupted CP in younger adults whereas older adults performed similarly across both conditions, suggesting that face-representation is more part-based in older adults.

No consolidation without representation: Correspondence between neural and psychological representations in recent and remote memory.

Memory systems consolidation is often conceived as the linear, time-dependent, neurobiological shift of memory from hippocampal-cortical to cortico-cortical dependency. We argue that contrary to this unidirectional view of memory reorganization, information about events may be retained in multiple forms (e.g., event-specific sensory-near episodic memory, event-specific gist information, event-general schematic information, or abstract semantic memory). These representations can all form at the time of the event and may continue to coexist for long durations. Their relative strength, composition, and dominance of expression change with time and experience, with task demands, and through their dynamic interaction with one another. These different psychological mnemonic representations depend on distinct functional and structural neurobiological substrates such that there is a neural-psychological representation correspondence (NPRC) among them. We discuss how the dynamics of psychological memory representations are reflected in multiple levels of neurobiological markers and their interactions. By this view, there are only variations of synaptic consolidation and memory dynamics without assuming a distinct systems consolidation process.