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.

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.

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.

Structural differences in hippocampal and prefrontal gray matter volume support flexible context-dependent navigation ability.

Spatial navigation is a fundamental part of daily life. Humans differ in their individual abilities to flexibly navigate their world, and a critical question is how this variability relates to differences in underlying brain structure. Our experiment examined individual differences in the ability to flexibly navigate routes that overlap with, and must be distinguished from, previously learned trajectories. We related differences in flexible navigation performance to differences in brain morphology in healthy young adults using voxel-based morphometry. Our findings provide novel evidence that individual differences in gray matter volume in the hippocampus and dorsolateral prefrontal cortex correlate with our ability rapidly to learn and flexibly navigate routes through our world.

Contributions of medial temporal lobe and striatal memory systems to learning and retrieving overlapping spatial memories.

Many life experiences share information with other memories. In order to make decisions based on overlapping memories, we need to distinguish between experiences to determine the appropriate behavior for the current situation. Previous work suggests that the medial temporal lobe (MTL) and medial caudate interact to support the retrieval of overlapping navigational memories in different contexts. The present study used functional magnetic resonance imaging (fMRI) in humans to test the prediction that the MTL and medial caudate play complementary roles in learning novel mazes that cross paths with, and must be distinguished from, previously learned routes. During fMRI scanning, participants navigated virtual routes that were well learned from prior training while also learning new mazes. Critically, some routes learned during scanning shared hallways with those learned during pre-scan training. Overlap between mazes required participants to use contextual cues to select between alternative behaviors. Results demonstrated parahippocampal cortex activity specific for novel spatial cues that distinguish between overlapping routes. The hippocampus and medial caudate were active for learning overlapping spatial memories, and increased their activity for previously learned routes when they became context dependent. Our findings provide novel evidence that the MTL and medial caudate play complementary roles in the learning, updating, and execution of context-dependent navigational behaviors.

Hippocampus and retrosplenial cortex combine path integration signals for successful navigation.

The current study used fMRI in humans to examine goal-directed navigation in an open field environment. We designed a task that required participants to encode survey-level spatial information and subsequently navigate to a goal location in either first person, third person, or survey perspectives. Critically, no distinguishing landmarks or goal location markers were present in the environment, thereby requiring participants to rely on path integration mechanisms for successful navigation. We focused our analysis on mechanisms related to navigation and mechanisms tracking linear distance to the goal location. Successful navigation required translation of encoded survey-level map information for orientation and implementation of a planned route to the goal. Our results demonstrate that successful first and third person navigation trials recruited the anterior hippocampus more than trials when the goal location was not successfully reached. When examining only successful trials, the retrosplenial and posterior parietal cortices were recruited for goal-directed navigation in both first person and third person perspectives. Unique to first person perspective navigation, the hippocampus was recruited to path integrate self-motion cues with location computations toward the goal location. Last, our results demonstrate that the hippocampus supports goal-directed navigation by actively tracking proximity to the goal throughout navigation. When using path integration mechanisms in first person and third person perspective navigation, the posterior hippocampus was more strongly recruited as participants approach the goal. These findings provide critical insight into the neural mechanisms by which we are able to use map-level representations of our environment to reach our navigational goals.

A high-resolution study of hippocampal and medial temporal lobe correlates of spatial context and prospective overlapping route memory.

When navigating our world we often first plan or retrieve an ideal route to our goal, avoiding alternative paths that lead to other destinations. The medial temporal lobe (MTL) has been implicated in processing contextual information, sequence memory, and uniquely retrieving routes that overlap or "cross paths." However, the identity of subregions of the hippocampus and neighboring cortex that support these functions in humans remains unclear. The present study used high-resolution functional magnetic resonance imaging (hr-fMRI) in humans to test whether the CA3/DG hippocampal subfield and parahippocampal cortex are important for processing spatial context and route retrieval, and whether the CA1 subfield facilitates prospective planning of mazes that must be distinguished from alternative overlapping routes. During hr-fMRI scanning, participants navigated virtual mazes that were well-learned from prior training while also learning new mazes. Some routes learned during scanning shared hallways with those learned during pre-scan training, requiring participants to select between alternative paths. Critically, each maze began with a distinct spatial contextual Cue period. Our analysis targeted activity from the Cue period, during which participants identified the current navigational episode, facilitating retrieval of upcoming route components and distinguishing mazes that overlap. Results demonstrated that multiple MTL regions were predominantly active for the contextual Cue period of the task, with specific regions of CA3/DG, parahippocampal cortex, and perirhinal cortex being consistently recruited across trials for Cue periods of both novel and familiar mazes. During early trials of the task, both CA3/DG and CA1 were more active for overlapping than non-overlapping Cue periods. Trial-by-trial Cue period responses in CA1 tracked subsequent overlapping maze performance across runs. Together, our findings provide novel insight into the contributions of MTL subfields to processing spatial context and route retrieval, and support a prominent role for CA1 in distinguishing overlapping episodes during navigational "look-ahead" periods.

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.

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.

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.

Cooperative interactions between hippocampal and striatal systems support flexible navigation.

Research in animals and humans has demonstrated that the hippocampus is critical for retrieving distinct representations of overlapping sequences of information. There is recent evidence that the caudate nucleus and orbitofrontal cortex are also involved in disambiguation of overlapping spatial representations. The hippocampus and caudate are functionally distinct regions, but both have anatomical links with the orbitofrontal cortex. The present study used an fMRI-based functional connectivity analysis in humans to examine the functional relationship between the hippocampus, caudate, and orbitofrontal cortex when participants use contextual information to navigate well-learned spatial routes which share common elements. Participants were trained outside the scanner to navigate virtual mazes from a first-person perspective. Overlapping condition mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping condition mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required contextual information identifying the current navigational route to guide the appropriate response for a given trial. Results revealed greater functional connectivity between the hippocampus, caudate, and orbitofrontal cortex for overlapping mazes compared to non-overlapping mazes. The current findings suggest that the hippocampus and caudate interact with prefrontal structures cooperatively for successful contextually dependent navigation.

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).

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.

Which way was I going? Contextual retrieval supports the disambiguation of well learned overlapping navigational routes.

Groundbreaking research in animals has demonstrated that the hippocampus contains neurons that distinguish between overlapping navigational trajectories. These hippocampal neurons respond selectively to the context of specific episodes despite interference from overlapping memory representations. The present study used functional magnetic resonance imaging in humans to examine the role of the hippocampus and related structures when participants need to retrieve contextual information to navigate well learned spatial sequences that share common elements. Participants were trained outside the scanner to navigate through 12 virtual mazes from a ground-level first-person perspective. Six of the 12 mazes shared overlapping components. Overlapping mazes began and ended at distinct locations, but converged in the middle to share some hallways with another maze. Non-overlapping mazes did not share any hallways with any other maze. Successful navigation through the overlapping hallways required the retrieval of contextual information relevant to the current navigational episode. Results revealed greater activation during the successful navigation of the overlapping mazes compared with the non-overlapping mazes in regions typically associated with spatial and episodic memory, including the hippocampus, parahippocampal cortex, and orbitofrontal cortex. When combined with previous research, the current findings suggest that an anatomically integrated system including the hippocampus, parahippocampal cortex, and orbitofrontal cortex is critical for the contextually dependent retrieval of well learned overlapping navigational routes.

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.

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.