The relationship between object-based spatial ability and virtual navigation performance.

Spatial navigation is a multi-faceted behaviour drawing on many different aspects of cognition. Visuospatial abilities, such as mental rotation and visuospatial working memory, in particular, may be key factors. A range of tests have been developed to assess visuospatial processing and memory, but how such tests relate to navigation ability remains unclear. This understanding is important to advance tests of navigation for disease monitoring in various disorders (e.g., Alzheimer's disease) where spatial impairment is an early symptom. Here, we report the use of an established mobile gaming app, Sea Hero Quest (SHQ), as a measure of navigation ability in a sample of young, predominantly female university students (N = 78; 20; female = 74.3%; mean age = 20.33 years). We used three separate tests of navigation embedded in SHQ: wayfinding, path integration and spatial memory in a radial arm maze. In the same participants, we also collected measures of mental rotation (Mental Rotation Test), visuospatial processing (Design Organization Test) and visuospatial working memory (Digital Corsi). We found few strong correlations across our measures. Being good at wayfinding in a virtual navigation test does not mean an individual will also be good at path integration, have a superior memory in a radial arm maze, or rate themself as having a strong sense of direction. However, we observed that participants who were good in the wayfinding task of SHQ tended to perform well on the three visuospatial tasks examined here, and to also use a landmark strategy in the radial maze task. These findings help clarify the associations between different abilities involved in spatial navigation.

The Versatile Wayfinder: Prefrontal Contributions to Spatial Navigation.

The prefrontal cortex (PFC) supports decision-making, goal tracking, and planning. Spatial navigation is a behavior that taxes these cognitive processes, yet the role of the PFC in models of navigation has been largely overlooked. In humans, activity in dorsolateral PFC (dlPFC) and ventrolateral PFC (vlPFC) during detours, reveal a role in inhibition and replanning. Dorsal anterior cingulate cortex (dACC) is implicated in planning and spontaneous internally-generated changes of route. Orbitofrontal cortex (OFC) integrates representations of the environment with the value of actions, providing a 'map' of possible decisions. In rodents, medial frontal areas interact with hippocampus during spatial decisions and switching between navigation strategies. In reviewing these advances, we provide a framework for how different prefrontal regions may contribute to different stages of navigation.

Backtracking during navigation is correlated with enhanced anterior cingulate activity and suppression of alpha oscillations and the 'default-mode' network.

Successful navigation can require realizing the current path choice was a mistake and the best strategy is to retreat along the recent path: 'back-track'. Despite the wealth of studies on the neural correlates of navigation little is known about backtracking. To explore the neural underpinnings of backtracking we tested humans during functional magnetic resonance imaging on their ability to navigate to a set of goal locations in a virtual desert island riven by lava which constrained the paths that could be taken. We found that on a subset of trials, participants spontaneously chose to backtrack and that the majority of these choices were optimal. During backtracking, activity increased in frontal regions and the dorsal anterior cingulate cortex, while activity was suppressed in regions associated with the core default-mode network. Using the same task, magnetoencephalography and a separate group of participants, we found that power in the alpha band was significantly decreased immediately prior to such backtracking events. These results highlight the importance for navigation of brain networks previously identified in processing internally-generated errors and that such error-detection responses may involve shifting the brain from default-mode states to aid successful spatial orientation.

Prefrontal Dynamics Associated with Efficient Detours and Shortcuts: A Combined Functional Magnetic Resonance Imaging and Magnetoencenphalography Study.

Central to the concept of the "cognitive map" is that it confers behavioral flexibility, allowing animals to take efficient detours, exploit shortcuts, and avoid alluring, but unhelpful, paths. The neural underpinnings of such naturalistic and flexible behavior remain unclear. In two neuroimaging experiments, we tested human participants on their ability to navigate to a set of goal locations in a virtual desert island riven by lava, which occasionally spread to block selected paths (necessitating detours) or receded to open new paths (affording real shortcuts or false shortcuts to be avoided). Detours activated a network of frontal regions compared with shortcuts. Activity in the right dorsolateral PFC specifically increased when participants encountered tempting false shortcuts that led along suboptimal paths that needed to be differentiated from real shortcuts. We also report modulation in event-related fields and theta power in these situations, providing insight to the temporal evolution of response to encountering detours and shortcuts. These results help inform current models as to how the brain supports navigation and planning in dynamic environments.

Cognitive mapping style relates to posterior-anterior hippocampal volume ratio.

As London taxi drivers acquire "the knowledge" and develop a detailed cognitive map of London, their posterior hippocampi (pHPC) gradually increase in volume, reflecting an increasing pHPC/aHPC volume ratio. In the mnemonic domain, greater pHPC/aHPC volume ratios in young adults have been found to relate to better recollection ability, indicating that the balance between pHPC and aHPC volumes might be reflective of cross-domain individual differences. Here, we examined participants' self-reported use of cognitive map-based navigational strategies in relation to their pHPC/aHPC hippocampal volume ratio. We find that greater reported cognitive map use was related to significantly greater posterior, relative to anterior, hippocampal volume in two separate samples of young adults. Further, greater reported cognitive map usage correlated with better performance on a self-initiated navigation task. Together, these data help to advance our understanding of differences between aHPC and pHPC and the greater role of pHPC in spatial mapping.

The Functional Consequences of Social Attention for Memory-guided Attention Orienting and Anticipatory Neural Dynamics.

Social attention when viewing natural social (compared with nonsocial) images has functional consequences on contextual memory in healthy human adults. In addition to attention affecting memory performance, strong evidence suggests that memory, in turn, affects attentional orienting. Here, we ask whether the effects of social processing on memory alter subsequent memory-guided attention orienting and corresponding anticipatory dynamics of 8-12 Hz alpha-band oscillations as measured with EEG. Eighteen young adults searched for targets in scenes that contained either social or nonsocial distracters and their memory precision tested. Subsequently, RT was measured as participants oriented to targets appearing in those scenes at either valid (previously learned) locations or invalid (different) locations. Memory precision was poorer for target locations in social scenes. In addition, distractor type moderated the validity effect during memory-guided attentional orienting, with a larger cost in RT when targets appeared at invalid (different) locations within scenes with social distractors. The poorer memory performance was also marked by reduced anticipatory dynamics of spatially lateralized 8-12 Hz alpha-band oscillations for scenes with social distractors. The functional consequences of a social attention bias therefore extend from memory to memory-guided attention orienting, a bidirectional chain that may further reinforce attentional biases.

Emotional distraction in the context of memory-based orienting of attention.

Attention can be guided by expectations stemming from long-term memories. In addition to such endogenous cues, exogenous salient stimuli capture attention, such as those conveying threat. This study examined the extent to which threatening distractors affect the employment of memories in guiding attention, and whether this is affected by trait anxiety. Emotional distractors were incorporated into a speeded target detection task, in which memory cues were presented simultaneously with task irrelevant emotional faces. Fearful face distractors disrupted target detection significantly more than neutral faces and the additional disruption to task performance from fearful compared with neutral faces was positively correlated with trait anxiety scores. The current findings of attentional capture by threat in the context of a second, powerful endogenous driver of attention underscore the magnitude of anxiety-related attention to threat. That is, threatening stimuli are sufficiently salient to induce prolonged disruption to goal directed behavior in anxious individuals. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

The cognitive map in humans: spatial navigation and beyond.

The 'cognitive map' hypothesis proposes that brain builds a unified representation of the spatial environment to support memory and guide future action. Forty years of electrophysiological research in rodents suggest that cognitive maps are neurally instantiated by place, grid, border and head direction cells in the hippocampal formation and related structures. Here we review recent work that suggests a similar functional organization in the human brain and yields insights into how cognitive maps are used during spatial navigation. Specifically, these studies indicate that (i) the human hippocampus and entorhinal cortex support map-like spatial codes, (ii) posterior brain regions such as parahippocampal and retrosplenial cortices provide critical inputs that allow cognitive maps to be anchored to fixed environmental landmarks, and (iii) hippocampal and entorhinal spatial codes are used in conjunction with frontal lobe mechanisms to plan routes during navigation. We also discuss how these three basic elements of cognitive map based navigation-spatial coding, landmark anchoring and route planning-might be applied to nonspatial domains to provide the building blocks for many core elements of human thought.

The functional consequences of social distraction: Attention and memory for complex scenes.

Cognitive scientists have long proposed that social stimuli attract visual attention even when task irrelevant, but the consequences of this privileged status for memory are unknown. To address this, we combined computational approaches, eye-tracking methodology, and individual-differences measures. Participants searched for targets in scenes containing social or non-social distractors equated for low-level visual salience. Subsequent memory precision for target locations was tested. Individual differences in autistic traits and social anxiety were also measured. Eye-tracking revealed significantly more attentional capture to social compared to non-social distractors. Critically, memory precision for target locations was poorer for social scenes. This effect was moderated by social anxiety, with anxious individuals remembering target locations better under conditions of social distraction. These findings shed further light onto the privileged attentional status of social stimuli and its functional consequences on memory across individuals.

Cognitive Training in the Elderly: Bottlenecks and New Avenues.

Development of measures to preserve cognitive function or even reverse cognitive decline in the ever-growing elderly population is the focus of many research and commercial efforts. One such measure gaining in popularity is the development of computer-based interventions that "exercise" cognitive functions. Computer-based cognitive training has the potential to be specific and flexible, accommodates feedback, and is highly accessible. As in most budding fields, there are still considerable inconsistencies across methodologies and results, as well as a lack of consensus on a comprehensive assessment protocol. We propose that the success of training-based therapeutics will rely on targeting specific cognitive functions, informed by comprehensive and sensitive batteries that can provide a "fingerprint" of an individual's abilities. Instead of expecting a panacea from training regimens, focused and personalized training interventions that accommodate individual differences should be developed to redress specific patterns of deficits in cognitive rehabilitation, both in healthy aging and in disease.

Extent of hippocampal atrophy predicts degree of deficit in recall.

Which specific memory functions are dependent on the hippocampus is still debated. The availability of a large cohort of patients who had sustained relatively selective hippocampal damage early in life enabled us to determine which type of mnemonic deficit showed a correlation with extent of hippocampal injury. We assessed our patient cohort on a test that provides measures of recognition and recall that are equated for difficulty and found that the patients' performance on the recall tests correlated significantly with their hippocampal volumes, whereas their performance on the equally difficult recognition tests did not and, indeed, was largely unaffected regardless of extent of hippocampal atrophy. The results provide new evidence in favor of the view that the hippocampus is essential for recall but not for recognition.

Is attention based on spatial contextual memory preferentially guided by low spatial frequency signals?

A popular model of visual perception states that coarse information (carried by low spatial frequencies) along the dorsal stream is rapidly transmitted to prefrontal and medial temporal areas, activating contextual information from memory, which can in turn constrain detailed input carried by high spatial frequencies arriving at a slower rate along the ventral visual stream, thus facilitating the processing of ambiguous visual stimuli. We were interested in testing whether this model contributes to memory-guided orienting of attention. In particular, we asked whether global, low-spatial frequency (LSF) inputs play a dominant role in triggering contextual memories in order to facilitate the processing of the upcoming target stimulus. We explored this question over four experiments. The first experiment replicated the LSF advantage reported in perceptual discrimination tasks by showing that participants were faster and more accurate at matching a low spatial frequency version of a scene, compared to a high spatial frequency version, to its original counterpart in a forced-choice task. The subsequent three experiments tested the relative contributions of low versus high spatial frequencies during memory-guided covert spatial attention orienting tasks. Replicating the effects of memory-guided attention, pre-exposure to scenes associated with specific spatial memories for target locations (memory cues) led to higher perceptual discrimination and faster response times to identify targets embedded in the scenes. However, either high or low spatial frequency cues were equally effective; LSF signals did not selectively or preferentially contribute to the memory-driven attention benefits to performance. Our results challenge a generalized model that LSFs activate contextual memories, which in turn bias attention and facilitate perception.

Distinct response components indicate that binding is the primary cause of response repetition effects.

Humans must constantly react to their environments. In many cases, repeating a response results in performance benefits, but sometimes it results in performance costs. This dichotomy is referred to as response repetition effects (RR effects). To understand these effects, we dissociated 2 components of a response: response categories (response meaning) and motor responses (response execution). By doing so, we were able to examine 2 proposed explanations of RR effects. One, the response inhibition account, explains that RR effects are the product of an inhibitory mechanism meant to prevent accidental reexecution of responses and stimulus category repetition priming. The response inhibition account predicts additive effects of response inhibition and stimulus category priming. Another, the binding account, explains that RR effects are the product of interference from automatically retrieved memories of previous events. The binding account predicts an interactive relationship between the transitions of task, response category, and motor response; a partial repetition of trial components (i.e., the task, the response category, and the motor response) will result in interference when compared with repeating all or switching all components. In Experiments 1 and 2, response components were dissociated by using a verification procedure. In Experiment 3, the response components were dissociated by varying the motor response used to indicate each response category. We found an interactive relationship between the transitions of task, response category, and motor response, demonstrating the role of binding in RR effects. In combination with previous results, our results suggest that binding and response inhibition are separable components of RR effects.

Reward associations magnify memory-based biases on perception.

Long-term spatial contextual memories are a rich source of predictions about the likely locations of relevant objects in the environment and should enable tuning of neural processing of unfolding events to optimize perception and action. Of particular importance is whether and how the reward outcome of past events can impact perception. We combined behavioral measures with recordings of brain activity with high temporal resolution to test whether the previous reward outcome associated with a memory could modulate the impact of memory-based biases on perception, and if so, the level(s) at which visual neural processing is biased by reward-associated memory-guided attention. Data showed that past rewards potentiate the effects of spatial memories upon the discrimination of target objects embedded within complex scenes starting from early perceptual stages. We show that a single reward outcome of learning impacts on how we perceive events in our complex environments.

Long-term memories bias sensitivity and target selection in complex scenes.

In everyday situations, we often rely on our memories to find what we are looking for in our cluttered environment. Recently, we developed a new experimental paradigm to investigate how long-term memory (LTM) can guide attention and showed how the pre-exposure to a complex scene in which a target location had been learned facilitated the detection of the transient appearance of the target at the remembered location [Summerfield, J. J., Rao, A., Garside, N., & Nobre, A. C. Biasing perception by spatial long-term memory. The Journal of Neuroscience, 31, 14952-14960, 2011; Summerfield, J. J., Lepsien, J., Gitelman, D. R., Mesulam, M. M., & Nobre, A. C. Orienting attention based on long-term memory experience. Neuron, 49, 905-916, 2006]. This study extends these findings by investigating whether and how LTM can enhance perceptual sensitivity to identify targets occurring within their complex scene context. Behavioral measures showed superior perceptual sensitivity (d') for targets located in remembered spatial contexts. We used the N2pc ERP to test whether LTM modulated the process of selecting the target from its scene context. Surprisingly, in contrast to effects of visual spatial cues or implicit contextual cueing, LTM for target locations significantly attenuated the N2pc potential. We propose that the mechanism by which these explicitly available LTMs facilitate perceptual identification of targets may differ from mechanisms triggered by other types of top-down sources of information.

Long-term memory prepares neural activity for perception.

Past experience provides a rich source of predictive information about the world that could be used to guide and optimize ongoing perception. However, the neural mechanisms that integrate information coded in long-term memory (LTM) with ongoing perceptual processing remain unknown. Here, we explore how the contents of LTM optimize perception by modulating anticipatory brain states. By using a paradigm that integrates LTM and attentional orienting, we first demonstrate that the contents of LTM sharpen perceptual sensitivity for targets presented at memory-predicted spatial locations. Next, we examine oscillations in EEG to show that memory-guided attention is associated with spatially specific desynchronization of alpha-band activity over visual cortex. Additionally, we use functional MRI to confirm that target-predictive spatial information stored in LTM triggers spatiotopic modulation of preparatory activity in extrastriate visual cortex. Finally, functional MRI results also implicate an integrated cortical network, including the hippocampus and a dorsal frontoparietal circuit, as a likely candidate for organizing preparatory states in visual cortex according to the contents of LTM.