Spatial Memory Representations Research Articles

Investigating the effect of real-world background images on spatial working memory representations

Investigating the effect of real-world background images on spatial working memory representations

Impaired Dynamics of Positional and Contextual Neural Coding in an Alzheimer's Disease Rat Model.

The hippocampal representation of space, formed by the collective activity of populations of place cells, is considered as a substrate of spatial memory. Alzheimer's disease (AD), a widespread severe neurodegenerative condition of multifactorial origin, typically exhibits spatial memory deficits among its early clinical signs before more severe cognitive impacts develop. To investigate mechanisms of spatial memory impairment in a double transgenic rat model of AD. In this study, we utilized 9-12-month-old double-transgenic TgF344-AD rats and age-matched controls to analyze the spatial coding properties of CA1 place cells. We characterized the spatial memory representation, assessed cells' spatial information content and direction-specific activity, and compared their population coding in familiar and novel conditions. Our findings revealed that TgF344-AD animals exhibited lower precision in coding, as evidenced by reduced spatial information and larger receptive zones. This impairment was evident in maps representing novel environments. While controls instantly encoded directional context during their initial exposure to a novel environment, transgenics struggled to incorporate this information into the newly developed hippocampal spatial representation. This resulted in impairment in orthogonalization of stored activity patterns, an important feature directly related to episodic memory encoding capacity. Overall, the results shed light on the nature of impairment at both the single-cell and population levels in the transgenic AD model. In addition to the observed spatial coding inaccuracy, the findings reveal a significantly impaired ability to adaptively modify and refine newly stored hippocampal memory patterns.

Individual differences in spatial working memory strategies differentially reflected in the engagement of control and default brain networks.

Spatial locations can be encoded and maintained in working memory using different representations and strategies. Fine-grained representations provide detailed stimulus information, but are cognitively demanding and prone to inexactness. The uncertainty in fine-grained representations can be compensated by the use of coarse, but robust categorical representations. In this study, we employed an individual differences approach to identify brain activity correlates of the use of fine-grained and categorical representations in spatial working memory. We combined data from six functional magnetic resonance imaging studies, resulting in a sample of $155$ ($77$ women, $25 \pm 5$ years) healthy participants performing a spatial working memory task. Our results showed that individual differences in the use of spatial representations in working memory were associated with distinct patterns of brain activity. Higher precision of fine-grained representations was related to greater engagement of attentional and control brain systems throughout the task trial, and the stronger deactivation of the default network at the time of stimulus encoding. In contrast, the use of categorical representations was associated with lower default network activity during encoding and higher frontoparietal network activation during maintenance. These results may indicate a greater need for attentional resources and protection against interference for fine-grained compared with categorical representations.

Individual differences in spatial working memory strategies differentially reflected in the engagement of control and default brain networks.

Spatial locations can be encoded and maintained in working memory using different representations and strategies. Fine-grained representations provide detailed stimulus information, but are cognitively demanding and prone to inexactness. The uncertainty in fine-grained representations can be compensated by the use of coarse, but robust categorical representations. In this study, we employed an individual differences approach to identify brain activity correlates of the use of fine-grained and categorical representations in spatial working memory. We combined data from six fMRI studies, resulting in a sample of 155 (77 women, 25 ± 5 years) healthy participants performing a spatial working memory task. Our results showed that individual differences in the use of spatial representations in working memory were associated with distinct patterns of brain activity. Higher precision of fine-grained representations was related to greater engagement of attentional and control brain systems throughout the task trial, and the stronger deactivation of the default network at the time of stimulus encoding. In contrast, the use of categorical representations was associated with lower default network activity during encoding and higher frontoparietal network activation during maintenance. These results may indicate a greater need for attentional resources and protection against interference for fine-grained compared to categorical representations.

Forming cognitive maps for abstract spaces: the roles of the human hippocampus and orbitofrontal cortex.

How does the human brain construct cognitive maps for decision-making and inference? Here, we conduct an fMRI study on a navigation task in multidimensional abstract spaces. Using a deep neural network model, we assess learning levels and categorized paths into exploration and exploitation stages. Univariate analyses show higher activation in the bilateral hippocampus and lateral prefrontal cortex during exploration, positively associated with learning level and response accuracy. Conversely, the bilateral orbitofrontal cortex (OFC) and retrosplenial cortex show higher activation during exploitation, negatively associated with learning level and response accuracy. Representational similarity analysis show that the hippocampus, entorhinal cortex, and OFC more accurately represent destinations in exploitation than exploration stages. These findings highlight the collaboration between the medial temporal lobe and prefrontal cortex in learning abstract space structures. The hippocampus may be involved in spatial memory formation and representation, while the OFC integrates sensory information for decision-making in multidimensional abstract spaces.

Real and virtual environments have comparable spatial memory distortions after scale and geometric transformations

ABSTRACT Boundaries define space, impacting spatial memory and neural representations. Unlike rodents, impact in humans is often tested using desktop virtual-reality (VR). This lacks self-motion cues, diminishing path-integration input. We replicated a desktop-VR study testing boundary impact on spatial memory for object locations using a physical, desktop-VR, and head-mounted-display-VR environment. Performance was measured by comparing participant responses to seven spatial distribution models using geometric or walking-path metrics. A weighted-linear combination of geometric models and a “place-cell-firing” model performed best, with identical fits across environments. Spatial representation appears differentially influenced by different boundary changes, but similarly across virtual and physical environments.

Multisensory input modulates memory-guided spatial navigation in humans

Efficient navigation is supported by a cognitive map of space. The hippocampus plays a key role for this map by linking multimodal sensory information with spatial memory representations. However, in human navigation studies, the full range of sensory information is often unavailable due to the stationarity of experimental setups. We investigated the contribution of multisensory information to memory-guided spatial navigation by presenting a virtual version of the Morris water maze on a screen and in an immersive mobile virtual reality setup. Patients with hippocampal lesions and matched controls navigated to memorized object locations in relation to surrounding landmarks. Our results show that availability of multisensory input improves memory-guided spatial navigation in both groups. It has distinct effects on navigational behaviour, with greater improvement in spatial memory performance in patients. We conclude that congruent multisensory information shifts computations to extrahippocampal areas that support spatial navigation and compensates for spatial navigation deficits.

Awareness of the relative quality of spatial working memory representations.

Working memory (WM) is the ability to maintain and manipulate information no longer accessible in the environment. The brain maintains WM representations over delay periods in noisy population-level activation patterns, resulting in variability in WM representations across items and trials. It is established that participants can introspect aspects of the quality of WM representations, and that they can accurately compare which of several WM representations of stimulus features like orientation or color is better on each trial. However, whether this ability to evaluate and compare the quality of multiple WM representations extends to spatial WM tasks remains unknown. Here, we employed a memory-guided saccade task to test recall errors for remembered spatial locations when participants were allowed to choose the most precise representation to report. Participants remembered either one or two spatial locations over a delay and reported one item's location with a saccade. On trials with two spatial locations, participants reported either the spatial location of a randomly cued item, or the location of the stimulus they remembered best. We found a significant improvement in recall error and increase in response time(RT) when participants reported their best-remembered item compared with trials in which they were randomly cued. These results demonstrate that participants can accurately introspect the relative quality of neural WM representations for spatial position, consistent with previous observations for other stimulus features, and support a model of WM coding involving noisy representations across items and trials.

Oculomotor rehearsal in visuospatial working memory

The neural and cognitive mechanisms of spatial working memory are tightly coupled with the systems that control eye movements, but the precise nature of this coupling is not well understood. It has been argued that the oculomotor system is selectively involved in rehearsal of spatial but not visual material in visuospatial working memory. However, few studies have directly compared the effect of saccadic interference on visual and spatial memory, and there is little consensus on how the underlying working memory representation is affected by saccadic interference. In this study we aimed to examine how working memory for visual and spatial features is affected by overt and covert attentional interference across two experiments. Participants were shown a memory array, then asked to either maintain fixation or to overtly or covertly shift attention in a detection task during the delay period. Using the continuous report task we directly examined the precision of visual and spatial working memory representations and fit psychophysical functions to investigate the sources of recall error associated with different types of interference. These data were interpreted in terms of embodied theories of attention and memory and provide new insights into the nature of the interactions between cognitive and motor systems.

Zn2+ inhibits spatial memory and hippocampal place cell representation through high-affinity binding to the NMDA receptor GluN2A subunit

A subset of glutamatergic neurons in the forebrain uses labile Zn2+ as a co-transmitter alongside glutamate. Synaptic Zn2+ plays a key role in learning and memory processes, but its mechanisms of action remain poorly understood. Here, we used a knock-in (KI) mouse line carrying a point mutation at the GluN2A Zn2+ binding site that selectively eliminates zinc inhibition of NMDA receptors. Ablation of Zn2+-GluN2A binding improves spatial memory retention and contextual fear memory formation. Electrophysiological recording of hippocampal neurons in the CA1 area revealed a greater proportion of place cells and substantial place field remapping in KI mice compared to wildtype littermates. Persistent place cell remapping was also seen in KI mice upon repeated testing suggesting an enhanced ability to maintain a distinct representation across multiple overlapping experiences. Together, these findings reveal an original molecular mechanism through which synaptic Zn2+ negatively modulates spatial cognition by dampening GluN2A-containing NMDA receptor signaling.

To Drive or to Be Driven? The Impact of Autopilot, Navigation System, and Printed Maps on Driver’s Cognitive Workload and Spatial Knowledge

The technical advances in navigation systems should enhance the driving experience, supporting drivers’ spatial decision making and learning in less familiar or unfamiliar environments. Furthermore, autonomous driving systems are expected to take over navigation and driving in the near future. Yet, previous studies pointed at a still unresolved gap between environmental exploration using topographical maps and technical navigation means. Less is known about the impact of the autonomous system on the driver’s spatial learning. The present study investigates the development of spatial knowledge and cognitive workload by comparing printed maps, navigation systems, and autopilot in an unfamiliar virtual environment. Learning of a new route with printed maps was associated with a higher cognitive demand compared to the navigation system and autopilot. In contrast, driving a route by memory resulted in an increased level of cognitive workload if the route had been previously learned with the navigation system or autopilot. Way-finding performance was found to be less prone to errors when learning a route from a printed map. The exploration of the environment with the autopilot was not found to provide any compelling advantages for landmark knowledge. Our findings suggest long-term disadvantages of self-driving vehicles for spatial memory representations.

Testing the precision of spatial memory representations using a change-detection task: effects of viewpoint change

ABSTRACT The brain encodes spatial information in at least two distinct ways: egocentric representations encode locations relative to the observer, whereas allocentric representations encode locations relative to the environment. Both inform spatial memory, but the extent to which they influence behaviour varies depending on the task. In two preregistered experiments we used a psychophysical approach to measure the precision of spatial memory while varying ego- and allocentric task demands. Participants attempted to detect the changed location of one of four objects when seen from a new viewpoint. In both experiments (one using a Same/Different task, the other a 2AFC task), psychophysically-determined change detection thresholds showed a monotonic but non-linear increase as the degree of viewpoint change increased. Our findings were consistent with a preregistered model which shows how, governed by distinct ego- and allocentric contributions, the precision of spatial memory changes lawfully as a function of viewpoint shift.

Hippocampal spatial memory representations in mice are heterogeneously stable.

The population of hippocampal neurons actively coding space continually changes across days as mice repeatedly perform tasks. Many hippocampal place cells become inactive while other previously silent neurons become active, challenging the idea that stable behaviors and memory representations are supported by stable patterns of neural activity. Active cell replacement may disambiguate unique episodes that contain overlapping memory cues, and could contribute to reorganization of memory representations. How active cell replacement affects the evolution of representations of different behaviors within a single task is unknown. We trained mice to perform a delayed nonmatching to place task over multiple weeks, and performed calcium imaging in area CA1 of the dorsal hippocampus using head-mounted miniature microscopes. Cells active on the central stem of the maze "split" their calcium activity according to the animal's upcoming turn direction (left or right), the current task phase (study or test), or both task dimensions, even while spatial cues remained unchanged. We found that, among reliably active cells, different splitter neuron populations were replaced at unequal rates, resulting in an increasing number of cells modulated by turn direction and a decreasing number of cells with combined modulation by both turn direction and task phase. Despite continual reorganization, the ensemble code stably segregated these task dimensions. These results show that hippocampal memories can heterogeneously reorganize even while behavior is unchanging.

Tracking spatial and non-spatial working memory representations coded in human oscillatory brain activity

Tracking spatial and non-spatial working memory representations coded in human oscillatory brain activity

Spatial working memory representations are resistant to an intervening stimulus and behavioral task

Spatial working memory representations are resistant to an intervening stimulus and behavioral task

Long-term spatial memory representations in human visual cortex

Long-term spatial memory representations in human visual cortex

Hippocampal CA1 gamma power predicts the precision of spatial memory judgments

The hippocampus plays a critical role in spatial memory. However, the exact neural mechanisms underlying high-fidelity spatial memory representations are unknown. We report findings from presurgical epilepsy patients with bilateral hippocampal depth electrodes performing an object-location memory task that provided a broad range of spatial memory precision. During encoding, patients were shown a series of objects along the circumference of an invisible circle. At test, the same objects were shown at the top of the circle (0°), and patients used a dial to move the object to its location shown during encoding. Angular error between the correct location and the indicated location was recorded as a continuous measure of performance. By registering pre- and postimplantation MRI scans, we were able to localize the electrodes to specific hippocampal subfields. We found a correlation between increased gamma power, thought to reflect local excitatory activity, and the precision of spatial memory retrieval in hippocampal CA1 electrodes. Additionally, we found a similar relationship between gamma power and memory precision in the dorsolateral prefrontal cortex and a directional relationship between activity in this region and in the CA1, suggesting that the dorsolateral prefrontal cortex is involved in postretrieval processing. These results indicate that local processing in hippocampal CA1 and dorsolateral prefrontal cortex supports high-fidelity spatial memory representations.

Intuitive physics ability in systemizers relies on differential use of the internalizing system and long-term spatial representations

According to the Empathizing-Systemizing theory (E-S Theory), individual differences in how people understand the physical world (systemizing) and the social world (empathizing), are two continuums in the general population with several implications, from vocational interests to skills in the social and physical domains. The underlying mechanisms of intuitive physics performance among individuals with strong systemizing and weak empathizing (systemizers) are, however, unknown. Our results affirm higher intuitive physics skills in healthy adult systemizers (N=36), and further reveal the brain mechanisms that are characteristic for those individuals in carrying out such tasks. When the participants performed intuitive physics tasks during functional magnetic resonance imaging, combined higher systemizing and lower empathizing was associated with stronger activations in parts of the default mode network (DMN, cuneus and posterior cingulate gyrus), middle occipital gyrus, and parahippocampal region. The posterior cingulate gyrus and parahippocampal gyrus were specifically associated with systemizing “brain type” even after controlling for task performance, while especially in the parietal cortex, the activation changes were simply explained by higher task performance. We therefore suggest that utilization of DMN-parahippocampal complex, suggested to play a role in internalizing and activating long-term spatial memory representations, is the factor that distinguishes systemizers from empathizers with the opposite “brain type” in intuitive physics tasks.

Fine-grained versus categorical: Pupil size differentiates between strategies for spatial working memory performance.

Pupillometry provides an accessible option to track working memory processes with high temporal resolution. Several studies showed that pupil size increases with the number of items held in working memory; however, no study has explored whether pupil size also reflects the quality of working memory representations. To address this question, we used a spatial working memory task to investigate the relationship of pupil size with spatial precision of responses and indicators of reliance on generalized spatial categories. We asked 30 participants (15 female, aged 19-31) to remember the position of targets presented at various locations along a hidden radial grid. After a delay, participants indicated the remembered location with a high-precision joystick providing a parametric measure of trial-to-trial accuracy. We recorded participants' pupil dilations continuously during task performance. Results showed a significant relation between pupil dilation during preparation/early encoding and the precision of responses, possibly reflecting the attentional resources devoted to memory encoding. In contrast, pupil dilation at late maintenance and response predicted larger shifts of responses toward prototypical locations, possibly reflecting larger reliance on categorical representation. On an intraindividual level, smaller pupil dilations during encoding predicted larger dilations during late maintenance and response. On an interindividual level, participants relying more on categorical representation also produced larger precision errors. The results confirm the link between pupil size and the quality of spatial working memory representation. They suggest compensatory strategies of spatial working memory performance-loss of precise spatial representation likely increases reliance on generalized spatial categories.

Association between COMT genotype and the control of memory guided saccades: Individual differences in healthy adults reveal a detrimental role of dopamine

The neural circuits involved in oculomotor control are well described; however, neuromodulation of eye movements is still hardly understood. Memory guided saccades have been extensively studied and in particular neurophysiological evidence from monkey studies points to a crucial functional role of prefrontal dopamine activity. We exploited individual differences in dopamine regulation due to the well established COMT (catechol-O-methyltransferase) Val158Met polymorphism to explore the link between prefrontal dopamine activity and memory guided saccades in healthy subjects. The COMT genotype is thought to modulate dopamine metabolism in prefrontal cortex producing differences in dopamine availability. We investigated memory guided saccades in 111 healthy subjects and determined individual genotypes. Accuracy and precision were reduced in subjects with putatively higher prefrontal dopamine levels. In contrast, we found no modulation of saccade parameters by genotype in a visually guided control task. Our results suggest that increased dopamine activity can have a detrimental effect on saccades that rely on spatial memory representations. Although these findings await replication in larger and more diverse sample sizes, they provide persuasive support that specific oculomotor parameters are sensitive to dopaminergic variation in healthy subjects and add to a better understanding of how dopamine modulates saccadic control.