The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze

BackgroundPresent evidence suggests that the hippocampus (HC) and the parahippocampal cortex (PHC) are involved in allocentric (world-centered) spatial memory. However, the putative role of the PHC in egocentric (body-centered) spatial learning has received only limited systematic investigation.MethodsTo examine the role of the PHC in egocentric learning, 19 healthy volunteers learned to find their way in a virtual maze during functional magnetic resonance imaging (fMRI). The virtual maze presented a first-person view, lacked any topographical landmarks and could be learned only using egocentric navigation strategies.ResultsDuring learning, increased medial temporal lobe activity was observed in the PHC bilaterally. Activity was also observed in cortical areas known to project to the PHC and proposed to contribute to egocentric spatial navigation and memory.ConclusionsOur results point to a role of the PHC for the representation and storage of egocentric information. It seems possible that the PHC contributes to egocentric memory by its feedback projections to the posterior parietal cortex. Moreover, access to allocentric and egocentric streams of spatial information may enable the PHC to construct a global and comprehensive representation of spatial environments and to promote the construction of stable cognitive maps by translating between egocentric and allocentric frames of memory.     

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.     

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。相比于路标等其他环境线索,边界对于空间导航的促进具有优势效应,那么边界感知的发展动态过程有着怎样的异质性,以及潜在的神经基础是什么呢?本文首次对近十年的相关研究进行了系统性地回顾和梳理,并提出了该领域未来发展的研究方向。首先,我们总结出边界感知的发展过程,具体表现为儿童早期(1岁半~2岁)可以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。其次,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的功能作用。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)由大脑中的旁海马位置区(parahippocampal place area, PPA)和压后皮层联合区(retrosplenial complex, RSC)负责表征,其中PPA和RSC均可以表征边界的空间几何及其高度,但边界的长度及边界间的构成角度仅由PPA表征;与边界绑定的物体位置的学习和提取则由海马负责,当海马的结构损害时,基于边界的学习也伴随着一定的受损。除此之外,本研究首次将边界所具有的导航可供性(affordance)这一研究热点区分为物理可供性和视觉可供性。边界的物理可供性由枕叶位置区负责表征(occipital parietal area, OPA,也被叫做 transverse occipital sulcus, TOS),并且OPA很可能主要负责表征以自我为参照的空间导航信息。而现有研究并未探讨边界视觉可供性的神经基础,但它为视觉引导的空间导航研究提供新的视角。总之,以往研究对基于边界的导航进行了初步的探索,丰富了我们对该领域的认识和理解。但是仍存在一些研究问题值得未来深入探讨。第一,拓展探索边界促进空间导航的认知过程中潜在的影响因素及其发展规律。未来应考虑构建一个综合的认知网络或者计算模型,以探明各个认知过程在基于边界导航中所发挥的作用。第二,深入挖掘边界促进空间导航中广泛涉及的脑功能基础(尤其是脑区间的功能协作),及关注儿童的大脑发育变化。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,全面而深入地探究携带易感基因以及临床前期的阿尔兹海默症群体中基于边界导航能力的特定受损情况。最后,将边界的概念延伸长时记忆、时间知觉、视觉空间、社交网络等领域,明晰边界在时间和空间中影响机制的异同。     

Remembering the past and imagining the future: a neural model of spatial memory and imagery

The authors model the neural mechanisms underlying spatial cognition, integrating neuronal systems and behavioral data, and address the relationships between long-term memory, short-term memory, and imagery, and between egocentric and allocentric and visual and ideothetic representations. Long-term spatial memory is modeled as attractor dynamics within medial-temporal allocentric representations, and short-term memory is modeled as egocentric parietal representations driven by perception, retrieval, and imagery and modulated by directed attention. Both encoding and retrieval/imagery require translation between egocentric and allocentric representations, which are mediated by posterior parietal and retrosplenial areas and the use of head direction representations in Papez's circuit. Thus, the hippocampus effectively indexes information by real or imagined location, whereas Papez's circuit translates to imagery or from perception according to the direction of view. Modulation of this translation by motor efference allows spatial updating of representations, whereas prefrontal simulated motor efference allows mental exploration. The alternating temporal-parietal flows of information are organized by the theta rhythm. Simulations demonstrate the retrieval and updating of familiar spatial scenes, hemispatial neglect in memory, and the effects on hippocampal place cell firing of lesioned head direction representations and of conflicting visual and ideothetic inputs.     

Age-related neural activity during allocentric spatial memory

Age-related decline in allocentric (viewer-independent) spatial memory is seen across species. We employed a virtual reality analogue of the Morris Water Maze to study the effect of healthy ageing on neural activity during allocentric spatial memory using functional magnetic resonance imaging. Voxel-based morphometry was used to ascertain hippocampal volumetric integrity. A widespread neural network comprising frontal, parietal, occipital, thalamic, and cerebellar regions was activated in young and older adults, but only young adults significantly activated bilateral hippocampus and left parahippocampus, as well as right frontal pole and dorso-lateral prefrontal cortex (DLPFC) during encoding and right DLPC during retrieval. Hippocampal grey matter volume was unchanged in older adults; however, prefrontal and parahippocampal functional attenuation was accompanied by volumetric reduction. We conclude that the decline in allocentric spatial memory with age is associated with attenuated hippocampal function, as well as compromised function and structure of prefrontal and parahippocampal regions.     

Introducing a new age-and-cognition-sensitive measurement for assessing spatial orientation using a landmark-less virtual reality navigational task

Age-related impairments during spatial navigation have been widely reported in egocentric and allocentric paradigms. However, the effect of age on more specific navigational components such as the ability to drive or update directional information has not received enough attention. In this study we investigated the effect of age on spatial updating of a visual target after a series of whole–body rotations and transitions using a novel landmark-less virtual reality (VR) environment. Moreover, a significant number of previous studies focused on measures susceptible to a general decline in motor skills such as the spent time navigating, the distance traversed. The current paper proposes a new compound spatial measure to assess navigational performance, examines its reliability and compares its power with those of the measures of duration and traversed distance in predicting participants' age and cognitive groups assessed by Montreal Cognitive Assessment (MoCA) scores. Using data from 319 adults (20–83 years), our results confirm the reliability, the age sensitivity, and the cognitive validity of the designed spatial measure as well as its superiority to the measures of duration and traversed distance in predicting age and MoCA score. In addition, the results show the significant effect of age cognitive status on spatial updating.     

Egocentric and allocentric navigation strategies in Williams syndrome and typical development

Recent findings suggest that difficulties on small‐scale visuospatial tasks documented in Williams syndrome (WS) also extend to large‐scale space. In particular, individuals with WS often present with difficulties in allocentric spatial coding (encoding relationships between items within an environment or array). This study examined the effect of atypical spatial processing in WS on large‐scale navigational strategies, using a novel 3D virtual environment. During navigation of recently learnt large‐scale space, typically developing (TD) children predominantly rely on the use of a sequential egocentric strategy (recalling the sequence of left–right body turns throughout a route), but become more able to use an allocentric strategy between 5 and 10 years of age. The navigation strategies spontaneously employed by TD children between 5 and 10 years of age and individuals with WS were analysed. The ability to use an allocentric strategy on trials where spatial relational knowledge was required to find the shortest route was also examined. Results showed that, unlike TD children, during spontaneous navigation the WS group did not predominantly employ a sequential egocentric strategy. Instead, individuals with WS followed the path until the correct environmental landmarks were found, suggesting the use of a time‐consuming and inefficient view‐matching strategy for wayfinding. Individuals with WS also presented with deficits in allocentric spatial coding, demonstrated by difficulties in determining short‐cuts when required and difficulties developing a mental representation of the environment layout. This was found even following extensive experience in an environment, suggesting that – unlike in typical development – experience cannot contribute to the development of spatial relational processing in WS. This atypical presentation of both egocentric and allocentric spatial encoding is discussed in relation to specific difficulties on small‐scale spatial tasks and known atypical cortical development in WS.     

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.     

Neural correlates of viewing paintings: Evidence from a quantitative meta-analysis of functional magnetic resonance imaging data

Many studies involving functional magnetic resonance imaging (fMRI) have exposed participants to paintings under varying task demands. To isolate neural systems that are activated reliably across fMRI studies in response to viewing paintings regardless of variation in task demands, a quantitative meta-analysis of fifteen experiments using the activation likelihood estimation (ALE) method was conducted. As predicted, viewing paintings was correlated with activation in a distributed system including the occipital lobes, temporal lobe structures in the ventral stream involved in object (fusiform gyrus) and scene (parahippocampal gyrus) perception, and the anterior insula—a key structure in experience of emotion. In addition, we also observed activation in the posterior cingulate cortex bilaterally—part of the brain’s default network. These results suggest that viewing paintings engages not only systems involved in visual representation and object recognition, but also structures underlying emotions and internalized cognitions.     

Generating an image from an ambiguous visual input: an electroencephalographic (EEG) investigation

Fourteen right-handed males were shown slides of common objects (e.g., wristwatch), familiar situations (e.g., two people shaking hands), and inkblots from a popular projective test (Holtzman, 1986) and then asked to name the object, assess the situation, or describe the most salient image emerging from the inkblot. Alpha power suppression was monitored over the left and right frontal, temporal, parietal, and occipital lobes to determine the brain circuitry responsible for the processing of each type of stimulus. When processing common objects and familiar situations there was bilateral activation of the parietal and occipital lobes; when processing inkblots, bilateral activation of the parietal and occipital lobes was again obtained, but complemented by selective activation of the right frontal lobe. The later suggests that anterior regions of the right cerebral hemisphere contribute to the generation of dynamic images like those evoked by visually ambiguous inkblots.     

认知重评和表达抑制情绪调节策略的脑网络分析：来自EEG和ERP的证据

本文旨在对认知重评和表达抑制两种常用情绪调节策略的自发脑网络特征及认知神经活动进行深入探讨。研究采集36名在校大学生的静息态和任务态脑电数据, 经过源定位和图论分析发现节点效率与两种情绪调节显著相关的脑区, 以及脑区之间的功能连接。研究结果表明, 在使用认知重评进行情绪调节时会激活前额叶皮质、前扣带回、顶叶、海马旁回和枕叶等多个脑区, 在使用表达抑制进行情绪调节时会激活前额叶皮质、顶叶、海马旁回、枕叶、颞叶和脑岛等多个脑区。因此, 这些脑区的节点效率或功能连接强度可能成为评估个体使用认知重评和表达抑制调节情绪效果的指标。     

Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain

Imaging, electrophysiological studies, and lesion work have shown that the medial temporal lobe (MTL) is important for episodic memory; however, it is unclear whether different MTL regions support the spatial, temporal, and item elements of episodic memory. In this study we used fMRI to examine retrieval performance emphasizing different aspects of episodic memory in the context of a spatial navigation paradigm. Subjects played a taxi-driver game ("yellowcab"), in which they freely searched for passengers and delivered them to specific landmark stores. Subjects then underwent fMRI scanning as they retrieved landmarks, spatial, and temporal associations from their navigational experience in three separate runs. Consistent with previous findings on item memory, perirhinal cortex activated most strongly during landmark retrieval compared with spatial or temporal source information retrieval. Both hippocampus and parahippocampal cortex activated significantly during retrieval of landmarks, spatial associations, and temporal order. We found, however, a significant dissociation between hippocampal and parahippocampal cortex activations, with spatial retrieval leading to greater parahippocampal activation compared with hippocampus and temporal order retrieval leading to greater hippocampal activation compared with parahippocampal cortex. Our results, coupled with previous findings, demonstrate that the hippocampus and parahippocampal cortex are preferentially recruited during temporal order and spatial association retrieval--key components of episodic "source" memory.     

Neural activation pattern in self-deceivers

While deception is a conscious cognitive effort and self-deception is an unconscious cognitive effort. Such effort possibly shapes the working memory and generates a neural activation pattern in self-deception. Little attempt was made to identify activation pattern in self-deception. The present study investigated the phenomenon of self-deception by increasing the working memory functions using a boxcar design. functional magnetic resonance imaging (fMRI) revealed more activation in bilateral inferior parietal lobule (BA 40), superior parietal lobule (BA 7), middle frontal gyrus (BA 9), medial frontal gyrus (BA 6), thalamus and cerebellum. Activated areas in frontal and parietal cortex suggest significant role of working memory during self-deception.     

Expert athletes activate somatosensory and motor planning regions of the brain when passively listening to familiar sports sounds

The present functional magnetic resonance imaging study examined the neural response to familiar and unfamiliar, sport and non-sport environmental sounds in expert and novice athletes. Results revealed differential neural responses dependent on sports expertise. Experts had greater neural activation than novices in focal sensorimotor areas such as the supplementary motor area, and pre- and postcentral gyri. Novices showed greater activation than experts in widespread areas involved in perception (i.e. supramarginal, middle occipital, and calcarine gyri; precuneus; inferior and superior parietal lobules), and motor planning and processing (i.e. inferior frontal, middle frontal, and middle temporal gyri). These between-group neural differences also appeared as an expertise effect within specific conditions. Experts showed greater activation than novices during the sport familiar condition in regions responsible for auditory and motor planning, including the inferior frontal gyrus and the parietal operculum. Novices only showed greater activation than experts in the supramarginal gyrus and pons during the non-sport unfamiliar condition, and in the middle frontal gyrus during the sport unfamiliar condition. These results are consistent with the view that expert athletes are attuned to only the most familiar, highly relevant sounds and tune out unfamiliar, irrelevant sounds. Furthermore, these findings that athletes show activation in areas known to be involved in action planning when passively listening to sounds suggests that auditory perception of action can lead to the re-instantiation of neural areas involved in producing these actions, especially if someone has expertise performing the actions.     

Spatial navigation deficits in amnestic mild cognitive impairment with neuropsychiatric comorbidity

Aims: To find out whether neuropsychiatric comorbidity (comMCI) influences spatial navigation performance in amnestic mild cognitive impairment (aMCI).

Methods: We recruited aMCI patients with (n = 21) and without (n = 21) neuropsychiatric comorbidity or alcohol abuse, matched for global cognitive impairment and cognitively healthy elderly participants (HE, n = 22). They completed the Mini-Mental State Examination and a virtual Hidden Goal Task in egocentric, allocentric, and delayed recall subtests.

Results: In allocentric navigation, aMCI and comMCI performed significantly worse than HE and similarly to each other. Although aMCI performed significantly worse at egocentric navigation than HE, they performed significantly better than patients with comMCI.

Conclusions: Despite the growing burden of dementia and the prevalence of neuropsychiatric symptoms in the elderly population, comMCI remains under-studied. Since trials often assess “pure” aMCI, we may underestimate patients’ navigation and other deficits. This finding emphasizes the importance of taking account of the cognitive effects of psychiatric disorders in aMCI.     

Cognitive and neuronal processes involved in sequential generation of general and specific mental images

Mental image generation is a complex process mediated by dynamically interrelated components, e.g. image generation and image enrichment of details. This study investigated the cognitive and neural correlates of sequential image generation. An event-related fMRI experiment was carried out in which general and specific images had to be generated sequentially in two different positions. Participants had to generate either a general image first and then a specific one or a specific image first and then a general one, in response to the same word-stimulus. Generation times showed that specific images took shorter to be produced if they had been preceded by the generation of a general image. The fMRI results showed that position of generation and type of image was associated with different patterns of neurofunctional change. When an image was generated as first, areas of activation were found in the parahippocampal, fusiform and occipital regions. These are areas associated with memory retrieval and visual processing. When an image was generated as second, significant activations were found in superior temporal and precuneus areas, brain structures that are involved in the storage of visual memory for object shapes and imagery, respectively. The generation of a general image was supported by frontal areas and by the precuneus. The generation of a specific image involved frontal and thalamic areas (structures associated with visual processing of details) and the posterior cingulate cortex. When shifting from a specific image to a general one, a higher level of activity was found in the middle frontal gyrus involved in global visuo-spatial processing, suggesting that the generation of specific images required the retrieval of an object’s global shape. Altogether, these data suggest that the sequential generation of different types of image is associated with discrete processes but also shares common cognitive and neural components.     

Spatial strategy elaboration in egocentric and allocentric tasks following medial prefrontal cortex lesions in the rat

We evaluated the role of the medial prefrontal cortex (mPFC) in the elaboration of egocentric navigation strategies in a water maze (WM). Lesions of mPFC cell bodies was achieved in 21 rats using bilateral injections of ibotenic acid (IA); 13 control rats were injected with saline. After 17 days, rats had to learn an allocentric (using external cues: 10 lesioned, 7 saline rats) or an egocentric WM (using internal/kinetic cues: 10 lesioned, 6 saline rats) over six trials in a same session. The initial trajectory on the sixth trial was used as an index of the elaboration of a navigation strategy. In the egocentric test, lesioned rats were more rarely located in the target quadrant than control rats. No differences were found between lesioned and control rats in the allocentric test. These results show that lesions of the mPFC impairs the capacity to elaborate an egocentric navigation strategy.     

The multiple neural networks of familiarity: A meta-analysis of functional imaging studies

Recent research has demonstrated the critical role of the feeling of familiarity in recognition memory. Various neuroimaging paradigms have been developed to identify the brain regions that sustain the processing of familiarity; however, there is still considerable controversy about the functional significance of each brain region implicated in familiarity-based retrieval. Here, we focused on the differences between paradigms that assess familiarity, with or without the encoding phase. We used the activation likelihood estimation (ALE) algorithm to conduct a whole-brain meta-analysis of neuroimaging studies that involved a familiarity task. Sixty-nine studies, performed in healthy subjects to determine the specific functions of the identified regions in familiarity processing, were finally selected. Distinct subanalyses were performed according to the experimental procedures used in the original studies. The ALE clusters that were highlighted revealed common activations for paradigms with and without encoding in the prefrontal cortex and in the parietal cortex. Additionally, supplementary activations related to specific familiarity (i.e., without the encoding phase) were observed in the limbic system (i.e., the amygdala, hippocampus, cingulate cortex, and insula) and in the associative sensory areas. The differences in the reported findings for different procedures are possibly due to differences in the concept of familiarity. To aid the exploration of the neural correlates of familiarity in future studies, the strengths and weaknesses of these experimental procedures are critically discussed.     

Dorsal striatal dopamine depletion impairs both allocentric and egocentric navigation in rats

Successful navigation requires interactions among multiple but overlapping neural pathways mediating distinct capabilities, including egocentric (self-oriented, route-based) and allocentric (spatial, map-based) learning. Route-based navigation has been shown to be impaired following acute exposure to the dopaminergic (DA) drugs (+)-methamphetamine and (+)-amphetamine, but not the serotoninergic (5-HT) drugs (±)-3,4-methylenedioxymethamphetamine or (±)-fenfluramine. The dopaminergic-rich neostriatum is involved in both allocentric and egocentric navigation. This experiment tested whether dorsal striatal DA loss using bilateral 6-hydroxydopamine (6-OHDA) injections impaired one or both types of navigation. Two weeks following 6-OHDA injections, rats began testing in the Cincinnati water maze (CWM) followed by the Morris water maze (MWM) for route-based and spatial navigation, respectively. 6-OHDA treatment significantly increased latency and errors in the CWM and path length, latency, and cumulative distance in the MWM with no difference on cued MWM trials. Neostriatal DA levels were reduced by 80% at 2 and 7 weeks post-treatment. In addition, 6-OHDA increased DA turnover and decreased norepinephrine (NE) levels. 6-OHDA injections did not alter monoamine levels in the prefrontal cortex. The data support that neostriatal DA modulates both types of navigation.     

自我构念启动对空间参照框架的影响

采用圈代词启动法及空间参照框架判断任务,探究自我构念启动能否改变被试对空间参照框架判断的认知加工过程。结果发现:(1)客体中心参照框架判断的整体正确率大于自我中心参照框架判断;(2)仅在独立型自我构念启动的一致条件下,被试的自我中心参照框架判断正确率高于客体中心参照框架的判断正确率;(3)独立型自我构念使男性更少受到自我中心干扰。结果表明,独立型自我构念启动可能对自我中心参照框架判断具有促进效应,但互倚型自我构念启动不能促进客体中心参照框架判断。