Neuropsychology of Environmental Navigation in Humans: Review and Meta-Analysis of fMRI Studies in Healthy Participants

In the past 20 years, many studies in the cognitive neurosciences have analyzed human ability to navigate in recently learned and familiar environments by investigating the cognitive processes involved in successful navigation. In this study, we reviewed the main experimental paradigms and made a cognitive-oriented meta-analysis of fMRI studies of human navigation to underline the importance of the experimental designs and cognitive tasks used to assess navigational skills. We performed a general activation likelihood estimation (ALE) meta-analysis of 66 fMRI experiments to identify the neural substrates underpinning general aspects of human navigation. Four individual ALE analyses were performed to identify the neural substrates of different experimental paradigms (i.e., familiar vs. recently learned environments) and different navigational strategies (allocentric vs. egocentric). Results of the general ALE analysis highlighted a wide network of areas with clusters in the occipital, parietal, frontal and temporal lobes, especially in the parahippocampal cortex. Familiar environments seem to be processed by an extended temporal-frontal network, whereas recently learned environments require activation in the parahippocampal cortex and the parietal and occipital lobes. Allocentric strategy is subtended by the same areas as egocentric strategy, but the latter elicits greater activation in the right precuneus, middle occipital lobe and angular gyrus. Our results suggest that different neural correlates are involved in recalling a well-learned or recently acquired environment and that different networks of areas subtend egocentric and allocentric strategies.     

Eye tracking, strategies, and sex differences in virtual navigation

Reports of sex differences in wayfinding have typically used paradigms sensitive to the female advantage (navigation by landmarks) or sensitive to the male advantage (navigation by cardinal directions, Euclidian coordinates, environmental geometry, and absolute distances). The current virtual navigation paradigm allowed both men and women an equal advantage. We studied sex differences by systematically varying the number of landmarks. Eye tracking was used to quantify sex differences in landmark utilisation as participants solved an eight-arm radial maze task within different virtual environments. To solve the task, participants were required to remember the locations of target objects within environments containing 0, 2, 4, 6, or 8 landmarks. We found that, as the number of landmarks available in the environment increases, the proportion of time men and women spend looking at landmarks and the number of landmarks they use to find their way increases. Eye tracking confirmed that women rely more on landmarks to navigate, although landmark fixations were also associated with an increase in task completion time. Sex differences in navigational behaviour occurred only in environments devoid of landmarks and disappeared in environments containing multiple landmarks. Moreover, women showed sustained landmark-oriented gaze, while men's decreased over time. Finally, we found that men and women use spatial and response strategies to the same extent. Together, these results shed new light on the discrepancy in landmark utilisation between men and women and help explain the differences in navigational behaviour previously reported.     

Orientation dependent mental representations following real-world navigation

The purpose of this study was to examine whether the mental representations acquired from real-world navigation are encoded in a single, specific orientation. Previous research has revealed an inconsistent pattern of results. In the present study, participants explored a university campus. In two reaction-time tasks, spatial judgments were then made relative to four imagined headings within the explored environment. The main result was that one of the headings was encoded in a distinct manner: When making left-right judgments performance on this heading was generally superior by comparison with the other orientations, and when making front-back judgments the same heading was the only one in which an advantage of front over back responses was observed. The finding that the headings were not encoded equally indicates that real-world navigation can lead to orientation specific representations.     

Parahippocampal and retrosplenial contributions to human spatial navigation

Spatial navigation is a core cognitive ability in humans and animals. Neuroimaging studies have identified two functionally defined brain regions that activate during navigational tasks and also during passive viewing of navigationally relevant stimuli such as environmental scenes: the parahippocampal place area (PPA) and the retrosplenial complex (RSC). Recent findings indicate that the PPA and RSC have distinct and complementary roles in spatial navigation, with the PPA more concerned with representation of the local visual scene and RSC more concerned with situating the scene within the broader spatial environment. These findings are a first step towards understanding the separate components of the cortical network that mediates spatial navigation in humans.     

Active steering along corrugated surfaces

A study is reported of the effect of dynamic occlusion that arises during locomotion over corrugated surfaces and its facilitating role on the control of locomotion, especially in cluttered environments. Surfaces varied in degree of corrugation and type of texture. Heading accuracy was assessed by having participants perform an active steering task. Results demonstrated the advantage of texture-mapped image surfaces over discrete element surfaces in the corrugated conditions. Observers appear to exploit accretion and deletion of optical texture at the occluding edge to extract and use information about heading direction for the control of movements in cluttered environments.     

Switching from reaching to navigation: differential cognitive strategies for spatial memory in children and adults

Navigational and reaching spaces are known to involve different cognitive strategies and brain networks, whose development in humans is still debated. In fact, high‐level spatial processing, including allocentric location encoding, is already available to very young children, but navigational strategies are not mature until late childhood. The Magic Carpet (MC) is a new electronic device translating the traditional Corsi Block‐tapping Test (CBT) to navigational space. In this study, the MC and the CBT were used to assess spatial memory for navigation and for reaching, respectively. Our hypothesis was that school‐age children would not treat MC stimuli as navigational paths, assimilating them to reaching sequences. Ninety‐one healthy children aged 6 to 11 years and 18 adults were enrolled. Overall short‐term memory performance (span) on both tests, effects of sequence geometry, and error patterns according to a new classification were studied. Span increased with age on both tests, but relatively more in navigational than in reaching space, particularly in males. Sequence geometry specifically influenced navigation, not reaching. The number of body rotations along the path affected MC performance in children more than in adults, and in women more than in men. Error patterns indicated that navigational sequences were increasingly retained as global paths across development, in contrast to separately stored reaching locations. A sequence of spatial locations can be coded as a navigational path only if a cognitive switch from a reaching mode to a navigation mode occurs. This implies the integration of egocentric and allocentric reference frames, of visual and idiothetic cues, and access to long‐term memory. This switch is not yet fulfilled at school age due to immature executive functions.     

Aging and Spatial Navigation: What Do We Know and Where Do We Go?

Spatial navigation is a complex cognitive skill that is necessary for everyday functioning in the environment. However, navigational skills are not typically measured in most test batteries assessing cognitive aging. The present paper reviews what we know about behavioral differences between older and younger adults in navigational skill and reviews the putative neural mechanisms that may underlie these behavioral differences. Empirical studies to date clearly identify navigation as an aspect of cognitive function that is vulnerable to the aging process. The few functional and structural neuroimaging studies that speak to neurological correlates of these age-related differences point to the hippocampus, parahippocampal gyrus, posterior cingulate gyrus (retrosplenial cortex), parietal lobes and pre-frontal cortex as structures critically involved in age effects on navigation. Outstanding issues in the field are addressed and productive avenues of future research are suggested. Among these outstanding issues include the necessity of performing longitudinal studies and differentiating between hippocampal and extra-hippocampal contributions to aging in navigation. The field may also be advanced by empirical assessment of navigational strategies and investigations into the multisensory nature of navigation including assessing the relative contributions of visual, vestibular, and proprioceptive function to age differences in navigational skill.     

空间导航的测量及其在认知老化中的应用

空间导航是日常生活所必需的高级认知功能, 参与空间导航的海马及内嗅皮层等脑区易受到老化的影响并导致结构萎缩或功能紊乱。早期研究多利用动物实验、纸笔测验、现实环境等实验范式考察老年人的空间导航老化特点。由于具有与现实环境相似的场景、兼容磁共振成像扫描以及导航者可以与场景交互等优点, 虚拟现实技术被越来越多地被应用到空间导航的老化研究中, 并进一步揭示了海马等内侧颞叶脑区在空间导航老化中的重要作用。     

Visual field dependence as a navigational strategy

Visual perception is an important component of environmental navigation. Previous research has revealed large individual differences in navigational strategies (i.e., the body’s kinesthetic and embodied approach to movement) and the perception of environmental surfaces (via distance estimations), but little research has investigated the potential relationship between these sources of individual variation. An important navigational strategy is the interaction between reliance on visual cues and vestibular or proprioceptive cues. We investigated the role of this navigational strategy in the perception of environmental surfaces. The results supported three embodied evolutionary predictions: Individuals who were most reliant on visual context (1) overestimated vertical surfaces significantly more, and (2) feared falling significantly more, than did those who were least reliant on visual context; and (3) all individuals had roughly accurate horizontal distance estimates, regardless of their navigational strategy. These are among the first data to suggest that individual differences in perception are closely related to the individual differences in navigation that derive from navigational risks. Variable navigational strategies may reflect variable capacities to perceive and navigate the environment.     

Experience,action and representations: Critical realism and the enactive theory of vision

This paper defends a dynamic model of the way in which perception is integrated with action, a model I refer to as ‘the navigational account’. According to this account, employing vision and other forms of distance perception, a creature acquires information about its surroundings via the senses, information that enables it to select and navigate routes through its environment, so as to attain objects that satisfy its needs. This form of perceptually guided activity should be distinguished from other kinds of semi-automatic responses to visual stimuli that do not necessarily involve conscious experiences. It essentially involves inner states, which involve both the awareness of phenomenal qualities, and also a representational component. The navigational account is compared here with the enactive approach to perception, which opposes the view that perceptual experiences are inner states. This paper argues that a full account of perception raises a number of different questions. One central explanatory project concerns questions about the kinds of processes that currently enable a creature to identify and respond appropriately to distant objects: the answer, it is argued, lies in acknowledging the role of conscious inner representations in guiding navigational behaviour through complex environments. The fact that perception and action are interdependent does not conflict with the claim that inner representational states comprise an essential stage in visual processing.

Visual search for rare targets: distracter tuning as a mechanism for learning from repeated target-absent searches

In the typical visual search experiment, participants search for targets that are present on half of the trials and absent on the other half. However, many real-world tasks involve targets that are present only occasionally. Given this, it is important to know how people deal with the problem of finding targets they have little experience with. One possibility is that they develop an awareness of the degree to which they have effectively completed a search through complex target-absent scenes. To test this hypothesis, we had participants complete two relatively long search tasks in which only a minority of trials included targets. Stimuli were cluttered real-world scenes, and targets were defined by category. We examined participants' ability to terminate search on the target-absent scenes based on an accurate assessment of scene difficulty. Scene difficulty was estimated by computing the mean correct-trial response time (RT) for each of the target-absent scenes across all participants. These group RTs were then correlated with each participants' individual correct-trial RTs for the same stimuli to assess the degree to which a given participant's search-termination times were correlated with those of the group. These correlations successfully predicted participants' target-detection success in both experiments. These experiments suggest that an integral part of visual search is the need to calibrate search behaviour to scenes of varying levels of complexity even when no targets are present.     

Evidence against integration of spatial maps in humans: generality across real and virtual environments

A real-world open-field search task was implemented with humans as an analogue of Blaisdell and Cook’s (Anim Cogn 8:7–16, 2005) pigeon foraging task and Sturz, Bodily, and Katz’s (Anim Cogn 9:207–217, 2006) human virtual foraging task to 1) determine whether humans were capable of integrating independently learned spatial maps and 2) make explicit comparisons of mechanisms used by humans to navigate real and virtual environments. Participants searched for a hidden goal located in one of 16 bins arranged in a 4 × 4 grid. In Phase 1, the goal was hidden between two landmarks (blue T and red L). In Phase 2, the goal was hidden to the left and in front of a single landmark (blue T). Following training, goal-absent trials were conducted in which the red L from Phase 1 was presented alone. Bin choices during goal-absent trials assessed participants’ strategies: association (from Phase 1), generalization (from Phase 2), or integration (combination of Phase 1 and 2). Results were inconsistent with those obtained with pigeons but were consistent with those obtained with humans in a virtual environment. Specifically, during testing, participants did not integrate independently learned spatial maps but used a generalization strategy followed by a shift in search behavior away from the test landmark. These results were confirmed by a control condition in which a novel landmark was presented during testing. Results are consistent with the bulk of recent findings suggesting the use of alternative navigational strategies to cognitive mapping. Results also add to a growing body of literature suggesting that virtual environment approaches to the study of spatial learning and memory have external validity and that spatial mechanisms used by human participants in navigating virtual environments are similar to those used in navigating real-world environments.     

Underlying Spatial Skills to Support Navigation Through Large,Unconstrained Environments

Studies of spatial navigation in real‐world settings have been limited to neighborhoods, campuses, and buildings. These locations have structural components, such as roads or hallways, which may direct navigation. The current study assessed navigational skills within a large‐scale forested environment that contained few pre‐established paths. Participants were asked to find flags using only a map and compass; dependent variables included target‐finding accuracy and efficiency. In addition, measurements of sense of direction, strategy, and working memory were taken to identify how these cognitive abilities influence performance. The results demonstrate the expected correlations between sense of direction and navigational success. An unexpected correlation between spatial working memory and navigational success was also found, which was the only significant predictor of performance when all measures were regressed together. These results suggest that studies should not forget basic cognitive abilities, which may predict success more than measures of sense of direction. Copyright © 2015 John Wiley & Sons, Ltd.     

边界促进空间导航的认知神经机制

边界是指在人的视野中占据较大比例,且具有立体拓展平面的障碍物,对于人类和动物的空间导航行为具有极大的促进作用。认知发展研究发现儿童早期(1岁半～2岁)通过加工边界的空间几何结构实现物体定位,并且随着年龄的发展逐渐学会利用边界的高度信息(3.1岁～4.7岁)、长度信息(4～5岁)、视觉阻碍性信息(5岁)等完成空间导航。基于这些认知过程,神经影像学研究主要以成人为研究被试,发现大脑中的内侧颞叶和顶叶脑区在边界加工中有着不同功能作用。具体而言,边界的空间几何结构及构成要素(高度、长度和角度)体位置的学习和提取则由海马负责。但是,仍存在一些研究问题值得未来深入S探c讨i。e第n一c,e拓展深化边界促进与后顶叶之间的功能交互。第三,密切关注大脑对场地边界与场地中心编码的心理或神经表征的区别和联系。第四,重点考察阿尔兹海默症有关基因易感人群在基于边界导航的行为受损情况。最后,延伸探讨边界在长时记忆、时间知觉、视觉空间、社交网络等领域的影响机制。     

Incongruent object/context relationships in visual scenes: Where are they processed in the brain?

Rapid object visual categorization in briefly flashed natural scenes is influenced by the surrounding context. The neural correlates underlying reduced categorization performance in response to incongruent object/context associations remain unclear and were investigated in the present study using fMRI. Participants were instructed to categorize objects in briefly presented scenes (exposure duration = 100 ms). Half of the scenes consisted of objects pasted in an expected (congruent) context, whereas for the other half, objects were embedded in incongruent contexts. Object categorization was more accurate and faster in congruent relative to incongruent scenes. Moreover, we found that the two types of scenes elicited different patterns of cerebral activation. In particular, the processing of incongruent scenes induced increased activations in the parahippocampal cortex, as well as in the right frontal cortex. This higher activity may indicate additional neural processing of the novel (non experienced) contextual associations that were inherent to the incongruent scenes. Moreover, our results suggest that the locus of object categorization impairment due to contextual incongruence is in the right anterior parahippocampal cortex. Indeed in this region activity was correlated with the reaction time increase observed with incongruent scenes. Representations for associations between objects and their usual context of appearance might be encoded in the right anterior parahippocampal cortex.     

场景知觉中物体加工的背景效应

在场景中加工物体信息时, 与物体相伴随的背景会影响对物体的加工。这种物体加工的背景效应在很多的研究中得到了证实。场景知觉中的背景效应有不同的表现, 对于场景中物体识别和背景的关系, 研究者从功能独立、相互作用和背景引导等理论角度给予了解释。其次, 自然场景材料和非自然场景材料所提供的背景信息不同, 研究者从不同的刺激水平探讨了这二者之间的背景效应存在的差异。同时, 随着技术的进步, 研究者也在探讨场景知觉过程中物体加工背景效应的生理机制, 并发现了一些与物体识别的背景效应有关的脑区定位。这些相关的研究为深入了解人是如何知觉和加工真实而复杂的环境提供了新的研究内容和视角。     

The information content of panoramic images II: view-based navigation in nonrectangular experimental arenas

Two recent studies testing navigation of rats in swimming pools have posed problems for any account of the use of purely geometric properties of space in navigation (M. Graham, M. A. Good, A. McGregor, & J. M. Pearce, 2006; J. M. Pearce, M. A. Good, P. M. Jones, & A. McGregor, 2004). The authors simulated 1 experiment from each study in a virtual reality environment to test whether experimental results could be explained by view-based navigation. The authors recorded a reference image at the target location and then determined global panoramic image differences between this image and images taken at regularly spaced locations throughout the arena. A formal model, in which an agent attempts to minimize image differences between the reference image and current views, generated trajectories that could be compared with the search performance of rats. For both experiments, this model mimics many aspects of rat behavior. View-based navigation provides a sufficient and parsimonious explanation for a range of navigational behaviors of rats under these experimental conditions.     

Anatomical Specialization of the Anterior Motor Speech Area: Hemispheric Differences in Magnopyramidal Neurons

The lateralization of motor speech function to the left hemisphere is supported by multiple lines of evidence, but relatively little is known about the anatomical basis of that specialization. In a preliminary study, we recently reported that area 45 of the left hemisphere (Broca′s area) contained a subpopulation of magnopyramidal neurons which were significantly larger than any seen in the homotopic region of the right hemisphere (Hayes and Lewis, 1993a). In the present study we examined a larger sample of cases in order to determine how consistently this difference is present in the population, if it is specific to Broca′s area or is a general feature of cortical regions mediating lateralized functions, and whether the subpopulation of large magnopyramidal neurons in left area 45 can be distinguished by their chemical phenotype. In Nissl-stained sections from 19 human brains, the mean (±SD) cross-sectional area of the largest layer III pyramidal neurons in area 45 was significantly (p < .0001) greater in the left hemisphere (522.1 ± 128.3 μm²) than in the right (454.1 ± 121.5 μm²). This interhemispheric difference appeared to be a unique characteristic of the largest neurons, since the mean size of all layer III pyramids in this area was not significantly different in the left (206.2 ± 93.5 μm²) and right (213.3 ± 103.9 μm²) hemispheres. In contrast to area 45, there was no interhemispheric difference in the mean cross-sectional area of the largest layer III pyramids in another lateralized region, primary motor cortex. in addition, in area 46, a region of prefrontal association cortex not known to be functionally lateralized, the mean somal size of the largest layer III pyramidal neurons was significantly (p < .001) smaller in the left hemisphere (402.4 ± 84.9 μm²) than in the right (437.8 ± 88.3 μm²). Finally, although the large layer III pyramids in area 45 were immunoreactive for nonphosphorylated neurofilament protein in both hemispheres, the mean cross-sectional area of the largest labeled neurons was significantly larger (p < .002) in the left hemisphere (525.2 ± 149.0 μm²) than in the right (490.3 ± 154.1 μm²). These findings demonstrate that layer III of Broca′s area contains a distinctive subpopulation of neurons that may play an important role in the specific functional architecture of this region.     

Using real-world scenes as contextual cues for search

Research on contextual cueing has demonstrated that with simple arrays of letters and shapes, search for a target increases in efficiency as associations between a search target and its surrounding visual context are learned. We investigated whether the visual context afforded by repeated exposure to real-world scenes can also guide attention when the relationship between the scene and a target position is arbitrary. Observers searched for and identified a target letter embedded in photographs of real-world scenes. Although search time within novel scenes was consistent across trials, search time within repeated scenes decreased across repetitions. Unlike previous demonstrations of contextual cueing, however, memory for scene-target covariation was explicit. In subsequent memory tests, observers recognized repeated contexts more often than those that were presented once and displayed superior recall of target position within the repeated scenes. In addition, repetition of inverted scenes, which made the scene more difficult to identify, produced a markedly reduced rate of learning, suggesting semantic information concerning object and scene identity are used to guide attention.