Affective music during episodic memory recollection modulates subsequent false emotional memory traces: an fMRI study.

Music is a powerful medium that influences our emotions and memories. Neuroscience research has demonstrated music's ability to engage brain regions associated with emotion, reward, motivation, and autobiographical memory. While music's role in modulating emotions has been explored extensively, our study investigates whether music can alter the emotional content of memories. Building on the theory that memories can be updated upon retrieval, we tested whether introducing emotional music during memory recollection might introduce false emotional elements into the original memory trace. We developed a 3-day episodic memory task with separate encoding, recollection, and retrieval phases. Our primary hypothesis was that emotional music played during memory recollection would increase the likelihood of introducing novel emotional components into the original memory. Behavioral findings revealed two key outcomes: 1) participants exposed to music during memory recollection were more likely to incorporate novel emotional components congruent with the paired music valence, and 2) memories retrieved 1 day later exhibited a stronger emotional tone than the original memory, congruent with the valence of the music paired during the previous day's recollection. Furthermore, fMRI results revealed altered neural engagement during story recollection with music, including the amygdala, anterior hippocampus, and inferior parietal lobule. Enhanced connectivity between the amygdala and other brain regions, including the frontal and visual cortex, was observed during recollection with music, potentially contributing to more emotionally charged story reconstructions. These findings illuminate the interplay between music, emotion, and memory, offering insights into the consequences of infusing emotional music into memory recollection processes.

The neural correlates of memory integration in value-based decision-making during human spatial navigation.

In daily life, we often make decisions based on relative value of the options, and we often derive these values from segmenting or integrating the outcomes of past episodes in memory. The neural correlates involved in value-based decision-making have been extensively studied in the literature, but few studies have investigated this topic in decisions that require segmenting or integrating episodic memory from related sources, and even fewer studies examine it in the context of spatial navigation. Building on the computational models from our previous studies, the current study investigates the neural substrates involved in decisions that require people either segment or integrate wayfinding outcomes involving different goals, across virtual spatial navigation tasks with differing demands. We find that when decisions require computation of spatial distances for navigation options, but also evaluation of one's prior spatial navigation ability with the task, the estimated value of navigational choices (EV) modulates neural activity in the dorsomedial prefrontal (dmPFC) cortex and ventrolateral prefrontal (vlFPC) cortex. However, superior parietal cortex tracked EV when decision-making tasks only require spatial distance memory but not evaluation of spatial navigation ability. Our findings reveal divergent neural substrates of memory integration in value-based decision-making under different spatial processing demands.

Beyond the ears: A review exploring the interconnected brain behind the hierarchical memory of music.

Music is a ubiquitous element of daily life. Understanding how music memory is represented and expressed in the brain is key to understanding how music can influence human daily cognitive tasks. Current music-memory literature is built on data from very heterogeneous tasks for measuring memory, and the neural correlates appear to differ depending on different forms of memory function targeted. Such heterogeneity leaves many exceptions and conflicts in the data underexplained (e.g., hippocampal involvement in music memory is debated). This review provides an overview of existing neuroimaging results from music-memory related studies and concludes that although music is a special class of event in our lives, the memory systems behind it do in fact share neural mechanisms with memories from other modalities. We suggest that dividing music memory into different levels of a hierarchy (structural level and semantic level) helps understand overlap and divergence in neural networks involved. This is grounded in the fact that memorizing a piece of music recruits brain clusters that separately support functions including-but not limited to-syntax storage and retrieval, temporal processing, prediction versus reality comparison, stimulus feature integration, personal memory associations, and emotion perception. The cross-talk between frontal-parietal music structural processing centers and the subcortical emotion and context encoding areas explains why music is not only so easily memorable but can also serve as strong contextual information for encoding and retrieving nonmusic information in our lives.

Visual Sequence Encoding is Enhanced by Predictable Music Pairing via Modulating Medial Temporal Lobe and Its Connectivity with Frontostriatal Loops.

Listening to music during cognitive activities, such as reading and studying, is very common in human daily life. Therefore, it is important to understand how music interacts with concurrent cognitive functions, particularly memory. Current literature has presented mixed results for whether music can benefit learning in other modalities. Evidence is needed for what neural mechanisms music can tap into to enhance concurrent memory processing. This fMRI study aimed to begin filling this gap by investigating how music of varying predictability levels influences parallel visual sequence encoding performance. Behavioral results suggest that overall, predictable music enhances visual sequential encoding, and this effect increases with the structural regularity and familiarity of music. fMRI results indicate that during visual sequence encoding, music activates traditional music-processing and motor-related areas, but decreases parahippocampal and striatal engagement. This deactivation may indicate a more efficient encoding of visual information when music is present. By comparing music conditions of different structural predictability and familiarity, we probed how this occurs. We demonstrate improved encoding with increased syntactical regularity, which was associated with decreased activity in default mode network and increased activity in inferior temporal gyrus. Furthermore, the temporal schema provided by music familiarity may influence encoding through altered functional connectivity between the prefrontal cortex, medial temporal lobe and striatum. Overall, we propose that pairing music with learning might facilitate memory by reducing neural demands for visual encoding and simultaneously strengthening the connectivity between the medial temporal lobe and frontostriatal loops important for sequencing information. Significance Statement: There is considerable interest in what mechanisms can be tapped to improve human memory. Music provides a potential modulator, but few studies have investigated music effects on encoding episodic memory. This study used a novel design to examine how music can influence concurrent visual item sequence encoding. We provided neural data to better understand mechanisms behind potential benefits of music for learning. Our results demonstrated predictable music may help guide parallel learning of sequences in another modality. We found that music might facilitate processing in neural systems associated with visual declarative long-term and working memory, and familiar music might modulate reward circuits and provide a temporal schema which facilitates better encoding of the temporal structure of new non-music information.

Effects of Acute Stress on Rigid Learning, Flexible Learning, and Value-Based Decision-Making in Spatial Navigation.

The current study investigated how stress affects value-based decision-making during spatial navigation and different types of learning underlying decisions. Eighty-two adult participants (42 females) first learned to find object locations in a virtual environment from a fixed starting location (rigid learning) and then to find the same objects from unpredictable starting locations (flexible learning). Participants then decided whether to reach goal objects from the fixed or unpredictable starting location. We found that stress impairs rigid learning in females, and it does not impair, and even improves, flexible learning when performance with rigid learning is controlled for. Critically, examining how earlier learning influences subsequent decision-making using computational models, we found that stress reduces memory integration, making participants more likely to focus on recent memory and less likely to integrate information from other sources. Collectively, our results show how stress impacts different memory systems and the communication between memory and decision-making.

Toward an Understanding of Cognitive Mapping Ability Through Manipulations and Measurement of Schemas and Stress.

Daily function depends on an ability to mentally map our environment. Environmental factors such as visibility and layout, and internal factors such as psychological stress, can challenge spatial memory and efficient navigation. Importantly, people vary dramatically in their ability to navigate flexibly and overcome such challenges. In this paper, we present an overview of "schema theory" and our view of its relevance to navigational memory research. We review several studies from our group and others, that integrate manipulations of environmental complexity and affective state in order to gain a richer understanding of the mechanisms that underlie individual differences in navigational memory. Our most recent data explicitly link such individual differences to ideas rooted in schema theory, and we discuss the potential for this work to advance our understanding of cognitive decline with aging. The data from this body of work highlight the powerful impacts of individual cognitive traits and affective states on the way people take advantage of environmental features and adopt navigational strategies.

A comparison of reinforcement learning models of human spatial navigation.

Reinforcement learning (RL) models have been influential in characterizing human learning and decision making, but few studies apply them to characterizing human spatial navigation and even fewer systematically compare RL models under different navigation requirements. Because RL can characterize one's learning strategies quantitatively and in a continuous manner, and one's consistency of using such strategies, it can provide a novel and important perspective for understanding the marked individual differences in human navigation and disentangle navigation strategies from navigation performance. One-hundred and fourteen participants completed wayfinding tasks in a virtual environment where different phases manipulated navigation requirements. We compared performance of five RL models (3 model-free, 1 model-based and 1 "hybrid") at fitting navigation behaviors in different phases. Supporting implications from prior literature, the hybrid model provided the best fit regardless of navigation requirements, suggesting the majority of participants rely on a blend of model-free (route-following) and model-based (cognitive mapping) learning in such navigation scenarios. Furthermore, consistent with a key prediction, there was a correlation in the hybrid model between the weight on model-based learning (i.e., navigation strategy) and the navigator's exploration vs. exploitation tendency (i.e., consistency of using such navigation strategy), which was modulated by navigation task requirements. Together, we not only show how computational findings from RL align with the spatial navigation literature, but also reveal how the relationship between navigation strategy and a person's consistency using such strategies changes as navigation requirements change.

Episodic memory integration shapes value-based decision-making in spatial navigation.

Valued-based decision-making has been studied for decades in myriad topics such as consumer spending and gambling, but very rarely in spatial navigation despite the link between the two being highly relevant to survival. Furthermore, how people integrate episodic memories, and what factors are related to the extent of memory integration in value-based decision-making, remain largely unknown. In the current study, participants learned locations of various objects in a virtual environment and then decided whether to reach goal objects from familiar starting locations or unpredictable ones, with different penalties associated with each option. We developed computational models to test whether, when given an object to find, participants' starting location decisions reflected their past performance specific to that goal (Target-specific model) or integrated memory from performance with all goals in the environment (Target-common model). Because participants' wayfinding performance improved throughout the experiment, we were able to examine what factors related to the generalization of past experience. We found that most participants' decisions were better fit by the Target-common model, and for the people whose decisions were better fit by the Target-common model this integrative tendency may be tied to their concurrently greater performance variability with individual targets. Moreover, greater success on our task was predicted by an interaction between the ability to estimate probabilities relevant to decision-making and self-report general task ability. Collectively, our results show how related navigational episodic memories can be reflected in decision-making, and uncover individual differences contributing to such processes. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Environmental overlap influences goal-oriented coding of spatial sequences differently along the long-axis of hippocampus.

When navigating our world we often first plan or retrieve a route to our goal, avoiding alternative paths to other destinations. Inspired by computational and animal models, we have recently demonstrated evidence that the human hippocampus supports prospective spatial coding, mediated by interactions with the prefrontal cortex. But the relationship between such signals and the need to discriminate possible routes based on their goal remains unclear. In the current study, we combined human fMRI, multi-voxel pattern analysis, and an established paradigm for contrasting memories of nonoverlapping routes with those of routes that cross paths and must be disambiguated. By classifying goal-oriented representations at the initiation of a navigational route, we demonstrate that environmental overlap modulates goal-oriented representations in the hippocampus. This modulation manifest through representational shifts from posterior to anterior components of the right hippocampus. Moreover, declines in goal-oriented decoding due to overlapping memories were predicted by the strength of the alternative memory, suggesting co-expression and competition between alternatives in the hippocampus during prospective thought. Moreover, exploratory whole-brain analyses revealed that a region of frontopolar cortex, which we have previously tied to prospective route planning, represented goal-states in new overlapping routes. Together, our findings provide insight into the influences of contextual overlap on the long-axis of the hippocampus and a broader memory and planning network that we have long-associated with such navigation tasks.

Evidence for a gradient within the medial temporal lobes for flexible retrieval under hierarchical task rules.

A fundamental question in memory research is how the hippocampus processes contextual cues to retrieve distinct mnemonic associations. Prior research has emphasized the importance of hippocampal-prefrontal interactions for context-dependent memory. Our fMRI study examined the human medial temporal lobes (MTL) and their prefrontal interactions when retrieving memories associated with hierarchically organized task contexts. Participants learned virtual object-location associations governed by subordinate and superordinate task rules, which could be independently cued to change. On each fMRI trial, participants retrieved the correct object for convergent rule and location contextual information. Results demonstrated that hippocampal activity and hippocampal-prefrontal functional interconnectivity distinguished retrieval under different levels of hierarchically organized task rules. In explicit contrast to the hippocampal tail, anterior (body and head) regions were recruited specifically for superordinate changes in the contextual hierarchy. The hippocampal body also differed in its functional connectivity with the prefrontal cortex for superordinate versus subordinate changes. Our findings demonstrate a gradient in MTL for associative retrieval under changing task rules, and advance understanding of hippocampal-prefrontal interactions that support flexible contextual memory.

Cognitive mapping: Anchoring our brain's sense of space in a dynamic world.

In complex environments, we rely on knowing our current location and pathways to others in order to flexibly navigate. But viable routes often change. New research suggests how the brain tracks where we are regardless of paths available to us.

The role of working memory capacity in spatial learning depends on spatial information integration difficulty in the environment.

A substantial amount of research has been conducted to uncover factors underlying the pronounced individual differences in spatial navigation. Spatial working memory capacity (SWM) is shown to be one important factor. In other domains such as reading comprehension, the role of working memory capacity in task performance differences depends on the difficulty of other task demands. In the current study, we investigated whether, similarly, the relationship between SWM and spatial performance was dependent on the difficulty of spatial information integration in the environment. Based on our prior work, spatial information integration difficulty depends on (a) difficulty in observing spatial relationships between locations of interest in the environment and (b) the individual's ability to integrate such relationships. Leveraging virtual reality, we manipulated the difficulty in observing the spatial relationships during learning by changing the visibility of the buildings, and measured individual's self-report sense of direction (SOD) which modulates the ability to integrate such relationships under different degrees of visibility. We consistently found that in the "easy" spatial integration condition (high SOD with high visibility), high SWM did not significantly improve spatial learning. The same pattern was observed in the difficult condition (low SOD with low visibility). On the other hand, high SWM improved spatial learning for medium difficulty (high SOD with low visibility, or vice versa). Together, our results reveal that the role of SWM in spatial learning differences depends on spatial integration difficulty. Our results also have significant applied implications for using virtual reality to target and facilitate spatial learning. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Environmental overlap and individual encoding strategy modulate memory interference in spatial navigation.

There has been great interest in how previously acquired knowledge interacts with newly learned knowledge and how prior knowledge facilitates semantic and "schema" learning. In studies of episodic memory, it is broadly associated with interference. Very few studies have examined the balance between interference and facilitation over the course of temporally-extended events and its individual differences. In the present study, we recruited 120 participants for a two-day spatial navigation experiment, wherein participants on Day 2 navigated virtual routes that were learned from Day 1 while also learning new routes. Critically, half of the new mazes overlapped with the old mazes, while the other half did not, enabling us to examine interference and facilitation in the context of spatial episodic learning. Overall, we found that navigation performance in new mazes that overlapped with previously-learned routes was significantly worse than the new non-overlapping mazes, suggesting proactive interference. Interestingly, we found memory facilitation for new routes in familiar environments in locations where there was no direct overlap with the previously-learned routes. Cognitive map accuracy positively correlated with proactive interference. Moreover, participants with high self-report spatial ability and/or a preference for place-based learning experienced more proactive interference. Taken together, our results show that 1) both memory interference and facilitation can co-occur as a function of prior learning, 2) proactive interference within a route varied as a function of the degree of overlap with old knowledge, and 3) individual differences in spatial ability and strategy can modulate proactive interference.

Stress Disrupts Human Hippocampal-Prefrontal Function during Prospective Spatial Navigation and Hinders Flexible Behavior.

The ability to anticipate and flexibly plan for the future is critical for achieving goal-directed outcomes. Extant data suggest that neural and cognitive stress mechanisms may disrupt memory retrieval and restrict prospective planning, with deleterious impacts on behavior. Here, we examined whether and how acute psychological stress influences goal-directed navigational planning and efficient, flexible behavior. Our methods combined fMRI, neuroendocrinology, and machine learning with a virtual navigation planning task. Human participants were trained to navigate familiar paths in virtual environments and then (concurrent with fMRI) performed a planning and navigation task that could be most efficiently solved by taking novel shortcut paths. Strikingly, relative to non-stressed control participants, participants who performed the planning task under experimentally induced acute psychological stress demonstrated (1) disrupted neural activity critical for mnemonic retrieval and mental simulation and (2) reduced traversal of shortcuts and greater reliance on familiar paths. These neural and behavioral changes under psychological stress were tied to evidence for disrupted neural replay of memory for future locations in the spatial environment, providing mechanistic insight into why and how stress can alter planning and foster inefficient behavior.

Heterogeneous correlations between hippocampus volume and cognitive map accuracy among healthy young adults.

Marked individual differences in the ability to mentally map our environment are pronounced not only among people of different ages or clinical conditions, but also within healthy young adults. Previous studies have shown that hippocampus size positively correlated with spatial navigation ability in healthy young adults, navigation experts, and patients with hippocampus lesions. However, a recent pre-registered study (Weisberg, Newcombe, & Chatterjee, 2019) with a large sample size (n = 90) did not observe this correlation in healthy young adults. Motivated by evidence that self-report sense of direction (SOD) could have a profound impact on how individuals utilize environmental cues, and that different navigation strategies could have opposite impacts on wayfinding performance in individuals with different cognitive map formation (CMF) abilities, we reanalyzed the publicly available dataset from Weisberg et al.'s study. We tested the influence of participants' SOD and CMF abilities on hippocampal volume-performance relationships. We find evidence that the non-significant correlation could envelop heterogeneous correlations among subgroups of individuals: the correlation between the right posterior hippocampal volume and spatial learning performance is significantly higher among individuals with high spatial ability than individuals with low spatial ability. This pattern of performance was observed for both SOD and CMF moderations of the relationship between hippocampal volume and spatial learning. While our re-analyses are fundamentally exploratory in nature, the new results imply that the relationship between hippocampal volume and spatial learning performance might be more complicated than previously thought.

Manipulating the visibility of barriers to improve spatial navigation efficiency and cognitive mapping.

Previous studies from psychology, neuroscience and geography showed that environmental barriers fragment the representation of the environment, reduce spatial navigation efficiency, distort distance estimation and make spatial updating difficult. Despite these negative effects, limited research has examined how to overcome barriers and if individual differences mediate their causes and potential interventions. We hypothesize that the reduced visibility caused by barriers plays a major role in accumulating error in spatial updating and encoding spatial relationships. We tested this using virtual navigation to grant participants 'X-ray' vision during environment encoding (i.e., barriers become translucent) and quantifying cognitive mapping benefits of counteracting fragmented visibility. We found that compared to the participants trained with naturalistic environment visibility, participants trained in the translucent environment had better performance in wayfinding and pointing tasks, which are theorized to measure navigation efficiency and cognitive mapping. Interestingly, these benefits were only observed in participants with high self-report sense of direction. Together, our results provide important insight into (1) how perceptual barrier effects manifest, even when physical fragmentation of space is held constant, (2) establish a novel intervention that can improve spatial learning, and (3) provide evidence that individual differences modulate perceptual barrier effects and the efficacy of such interventions.

Environmental Barriers Disrupt Grid-like Representations in Humans during Navigation.

Environmental barriers fundamentally shape our behavior and conceptualization of space [1-5]. Evidence from rodents suggests that, in contrast to an open-field environment, where grid cells exhibit firing patterns with a 6-fold rotational symmetry [5, 6], barriers within the field abolish the 6-fold symmetry and fragment the grid firing fields into compartmentalized repeating "submaps" [5]. These results suggest that barriers may exert their influence on the cognitive map through organization of the metric representation of space provided by entorhinal neurons. We directly tested this hypothesis in humans, combining functional MRI with a virtual navigation paradigm in which we manipulated the local barrier structure. When participants performed a fixed-route foraging task in an open field, the functional MRI signal in right entorhinal cortex exhibited a 6-fold periodic modulation by movement direction associated with conjunctive grid cell firing [7]. However, when environments were compartmentalized by barriers, the grid-like 6-fold spatial metric was abolished. Instead, a 4-fold modulation of the entorhinal signal was observed, consistent with a vectorized organization of spatial metrics predicted by rodent models of navigation [5]. Collectively, these results provide mechanistic insight into why barriers compartmentalize our cognitive map, indicating that boundaries exert a powerful influence on the way environments are represented in human entorhinal cortex. Given that our daily environments are rarely wide open and are often segmented by barriers (e.g., the buildings of our home city), our findings have implications for applying models of cognitive mapping based on grid-like metrics [8] to naturalistic circumstances.

Stress Impairs Episodic Retrieval by Disrupting Hippocampal and Cortical Mechanisms of Remembering.

Despite decades of science investigating the neural underpinnings of episodic memory retrieval, a critical question remains: how does stress influence remembering and the neural mechanisms of recollection in humans? Here, we used functional magnetic resonance imaging and multivariate pattern analyses to examine the effects of acute stress during retrieval. We report that stress reduced the probability of recollecting the details of past experience, and that this impairment was driven, in part, by a disruption of the relationship between hippocampal activation, cortical reinstatement, and memory performance. Moreover, even memories expressed with high confidence were less accurate under stress, and this stress-induced decline in accuracy was explained by reduced posterior hippocampal engagement despite similar levels of category-level cortical reinstatement. Finally, stress degraded the relationship between the engagement of frontoparietal control networks and retrieval decision uncertainty. Collectively, these findings demonstrate the widespread consequences of acute stress on the neural systems of remembering.

Learned Spatial Schemas and Prospective Hippocampal Activity Support Navigation After One-Shot Learning.

Prior knowledge structures (or schemas) confer multiple behavioral benefits. First, when we encounter information that fits with prior knowledge structures, this information is generally better learned and remembered. Second, prior knowledge can support prospective planning. In humans, memory enhancements related to prior knowledge have been suggested to be supported, in part, by computations in prefrontal and medial temporal lobe (MTL) cortex. Moreover, animal studies further implicate a role for the hippocampus in schema-based facilitation and in the emergence of prospective planning signals following new learning. To date, convergence across the schema-enhanced learning and memory literature may be constrained by the predominant use of hippocampally dependent spatial navigation paradigms in rodents, and non-spatial list-based learning paradigms in humans. Here, we targeted this missing link by examining the effects of prior knowledge on human navigational learning in a hippocampally dependent virtual navigation paradigm that closely relates to foundational studies in rodents. Outside the scanner, participants overlearned Old Paired Associates (OPA- item-location associations) in multiple spatial environments, and they subsequently learned New Paired Associates (NPA-new item-location associations) in the environments while undergoing fMRI. We hypothesized that greater OPA knowledge precision would positively affect NPA learning, and that the hippocampus would be instrumental in translating this new learning into prospective planning of navigational paths to NPA locations. Behavioral results revealed that OPA knowledge predicted one-shot learning of NPA locations, and neural results indicated that one-shot learning was predicted by the rapid emergence of performance-predictive prospective planning signals in hippocampus. Prospective memory relationships were not significant in parahippocampal cortex and were marginally dissociable from the primary hippocampal effect. Collectively, these results extend understanding of how schemas impact learning and performance, showing that the precision of prior spatial knowledge is important for future learning in humans, and that the hippocampus is involved in translating this knowledge into new goal-directed behaviors.