The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings

The clinical and neuroimaging literatures are surveyed in order to collate for the first time the available data on retrosplenial involvement in human navigation. Several notable features emerge from consideration of the case reports of relatively pure topographical disorientation in the presence of a retrosplenial lesion. The majority of cases follow damage to the right retrosplenial cortex, with Brodmann's area 30 apparently compromised in most cases. All patients displayed impaired learning of new routes, and defective navigation in familiar environments complaining they could not use preserved landmark recognition to aid orientation. The deficit generally resolved within eight weeks of onset. The majority of functional neuroimaging studies involving navigation or orientation in large-scale space also activate the retrosplenial cortex, usually bilaterally, with good concordance in the locations of the voxel of peak activation across studies, again with Brodmann's area 30 featuring prominently. While there is strong evidence for right medial temporal lobe involvement in navigation, it now seems that the inputs the hippocampus and related structures receive from and convey to right retrosplenial cortex have a similar spatial preference, while the left medial temporal and left retrosplenial cortices seem primarily concerned with more general aspects of episodic memory.     

Cue combination in human spatial navigation

This project investigated the ways in which visual cues and bodily cues from self-motion are combined in spatial navigation. Participants completed a homing task in an immersive virtual environment. In Experiments 1A and 1B, the reliability of visual cues and self-motion cues was manipulated independently and within-participants. Results showed that participants weighted visual cues and self-motion cues based on their relative reliability and integrated these two cue types optimally or near-optimally according to Bayesian principles under most conditions. In Experiment 2, the stability of visual cues was manipulated across trials. Results indicated that cue instability affected cue weights indirectly by influencing cue reliability. Experiment 3 was designed to mislead participants about cue reliability by providing distorted feedback on the accuracy of their performance. Participants received feedback that their performance with visual cues was better and that their performance with self-motion cues was worse than it actually was or received the inverse feedback. Positive feedback on the accuracy of performance with a given cue improved the relative precision of performance with that cue. Bayesian principles still held for the most part. Experiment 4 examined the relations among the variability of performance, rated confidence in performance, cue weights, and spatial abilities. Participants took part in the homing task over two days and rated confidence in their performance after every trial. Cue relative confidence and cue relative reliability had unique contributions to observed cue weights. The variability of performance was less stable than rated confidence over time. Participants with higher mental rotation scores performed relatively better with self-motion cues than visual cues. Across all four experiments, consistent correlations were found between observed weights assigned to cues and relative reliability of cues, demonstrating that the cue-weighting process followed Bayesian principles. Results also pointed to the important role of subjective evaluation of performance in the cue-weighting process and led to a new conceptualization of cue reliability in human spatial navigation.     

Active and passive contributions to spatial learning

It seems intuitively obvious that active exploration of a new environment will lead to better spatial learning than will passive exposure. However, the literature on this issue is decidedly mixed—in part, because the concept itself is not well defined. We identify five potential components of active spatial learning and review the evidence regarding their role in the acquisition of landmark, route, and survey knowledge. We find that (1) idiothetic information in walking contributes to metric survey knowledge, (2) there is little evidence as yet that decision making during exploration contributes to route or survey knowledge, (3) attention to place–action associations and relevant spatial relations contributes to route and survey knowledge, although landmarks and boundaries appear to be learned without effort, (4) route and survey information are differentially encoded in subunits of working memory, and (5) there is preliminary evidence that mental manipulation of such properties facilitates spatial learning. Idiothetic information appears to be necessary to reveal the influence of attention and, possibly, decision making in survey learning, which may explain the mixed results in desktop virtual reality. Thus, there is indeed an active advantage in spatial learning, which manifests itself in the task-dependent acquisition of route and survey knowledge.     

Damage to the retrosplenial cortex produces specific impairments in spatial working memory

Mounting evidence indicates that the retrosplenial cortex (RSP) has a critical role in spatial navigation. The goal of the present study was to characterize the specific nature of spatial memory deficits that are observed following damage to RSP. Rats with RSP lesions or sham lesions were first trained in a working memory task using an 8-arm radial arm maze. Rats were allowed 5 min to visit each arm and retrieve food pellets and a 5-s delay was imposed between arm choices. Consistent with previous research, rats with RSP damage committed more errors than controls. In particular, RSP-lesioned rats committed more errors of omission (failing to visit an arm of the maze), but there were no lesion effects on errors of commission (revisiting an arm). Neither group of rats exhibited a turn bias (i.e., always turning a certain direction when choosing an arm). At the end of the training phase of the experiment, both groups had reached asymptote and committed very few errors. In the subsequent test phase, a longer delay (30-s) was imposed during some sessions. Both control and RSP-lesioned rats continued to make few errors during sessions with the standard 5-s delay, but RSP-lesioned rats were impaired at the 30-s delay and committed more errors of commission, consistent with an increase in taxing spatial working memory.     

空间导航的脑网络基础和调控机制

空间导航在生活中时刻发生,空间能力衰退是阿尔兹海默症的重要早期表现。早期关于空间导航神经机制的研究主要关注单个脑区的特异性功能,但这些脑区如何交互以整合不同模态的信息支持复杂导航行为尚不清楚。脑成像技术、脑网络建模方法和神经调控手段的发展,为在脑网络水平理解人类空间导航的认知神经机制提供了重要研究手段。本研究试图融合空间导航认知神经机制研究的最新进展,借助脑网络建模、大数据分析、微电流刺激等前沿研究手段,研究空间导航脑网络的关键拓扑属性特征(如模块化、核心节点等),探寻该功能特异性神经网络的重要影响因素和调控机制,并构建空间导航的脑网络理论模型。研究成果将有利于理解人类复杂导航行为的脑网络基础,为阿尔兹海默症等相关认知障碍脑疾病的筛查和诊断提供重要参考。     

Lost in virtual space: studies in human and ideal spatial navigation

The authors describe 3 human spatial navigation experiments that investigate how limitations of perception, memory, uncertainty, and decision strategy affect human spatial navigation performance. To better understand the effect of these variables on human navigation performance, the authors developed an ideal-navigator model for indoor navigation whose optimizing algorithm uses a partially observable Markov decision process. The model minimizes the number of actions (translations and rotations) required to move from an unknown starting state to a specific goal state in indoor environments that have perceptual ambiguity. The authors compared the model's performance with that of the human observer to measure human navigation efficiency. Experiment 1 investigated the effect of increasing the layout size on spatial way-finding efficiency and found that participants' efficiencies decreased as layout size increased. The authors investigated whether this reduction in navigation efficiency was due to visual perception (Experiment 2), memory, spatial updating strategy, or decision strategy (Experiment 3).     

Active navigation and orientation-free spatial representations

In this study, we examined the orientation dependency of spatial representations following various learning conditions. We assessed the spatial representations of human participants after they had learned a complex spatial layout via map learning, via navigating within a real environment, or via navigating through a virtual simulation of that environment. Performances were compared between conditions involving (1) multiple- versus single-body orientation, (2) active versus passive learning, and (3) high versus low levels of proprioceptive information. Following learning, the participants were required to produce directional judgments to target landmarks. Results showed that the participants developed orientation-specific spatial representations following map learning and passive learning, as indicated by better performance when tested from the initial learning orientation. These results suggest that neither the number of vantage points nor the level of proprioceptive information experienced are determining factors; rather, it is the active aspect of direct navigation that leads to the development of orientation-free representations.     

Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory

The prefrontal cortex is thought to be critical for goal-directed action and the hippocampus is known to be importantly involved in spatial memory. Several studies have been suggestive of a role for the orbitofrontal cortex (OFC) in spatial navigation. However, the medial prefrontal cortex (mPFC) receives projections directly from the intermediate CA1 (iCA1) region of hippocampus and this link may be critical for spatial navigation. The purpose of the present investigation was to test the performance of rats receiving bilateral or disconnection infusions of lidocaine into OFC, mPFC, or iCA1 to determine the contribution of these structures to encoding and retrieval of spatial memory using the Hebb–Williams maze. A total of 92 male Long-Evans rats received chronic bilateral, contralateral, or ipsilateral implantation of cannulas into OFC, mPFC, or iCA1. Prior to testing on day 1 or day 2, subjects received central infusions of saline or lidocaine. The number of errors committed on the first five trials compared to the second five trials of day 1 was used to determine encoding, whereas retrieval was determined by comparing the second five trials of day 1 with the first five trials of day 2. The present findings suggest that mPFC and iCA1 are necessary and interact during encoding and retrieval; however, the OFC does not appear to be essential for either process. While the nature of the interaction between mPFC and iCA1 during encoding and retrieval is unclear, it may be supported by the integration of goals and spatial cues or strategy switching.     

Spatial and temporal contributions to the structure of spatial memory.

Three experiments investigated the effects of spatial and temporal contiguity in item recognition, location judgment, and distance estimation tasks. Ss learned the locations of object names in spatial arrays, which were divided into 2 regions. The names of locations were presented during map learning so that critical pairs appeared close in space and close in time, close in space but far in time, far in space but close in time, and far in space and far in time. Names primed each other in recognition only when they were neighbors in both space and time. In contrast, the effects of spatial and temporal contiguity in priming in location judgments were additive. Finally, temporal contiguity affected estimates of Euclidean distance when locations were close together, but not when they were far apart.     

Three contributions to understanding human sexuality

A critical review of three recent studies of sexuality is placed against the background of four groups that have, for the past decade, attempted to discern the most important facts—known or still to be discovered—about human sexuality. The books reviewed are:The Pleasure Bond by William H. Masters and Virginia Johnson;Christian, Celebrate Your Sexuality by Dwight Hervey Small; andMale Homosexuals: Their Problems and Adaptations by Martin S. Weinberg and Colin J. Williams.     

Quantitative and qualitative sex differences in spatial navigation

We examined sex differences in spatial navigation performance using an ecologically relevant experimental paradigm in which virtual maze-like museums are projected in front of a treadmill. Thirty-two 20-30-year-old adults (16 women/16 men) performed a way-finding task in city-block (straight corridors) or variable (irregular corridors) topographies while walking on the treadmill. Sex differences in spatial navigation performance were reduced in variable topographies, suggesting less reliance on spatial relational learning among women. Also, spatial geometric knowledge of the mazes continued to be higher in men after all participants had attained perfect place-finding performance. Results indicate that sex differences in spatial navigation performance are modulated by interactions between environmental demands and sex differences in spatial processing.     

Orienting in space and time: Joint contributions to exogenous spatial cuing effects

We examined whether the time course of exogenous spatial-cuing effects is sensitive to the allocation of attention in time. Expectation for a target within a particular time window following the cue was manipulated by varying the proportion of trials that appeared at each of three stimulus onset asynchronies in both a detection task and a two-alternative forced-choice discrimination task. The time course of spatial-cuing effects was sensitive to the temporal expectation manipulation only in the discrimination task. The results are discussed with reference to the role of attentional set in exogenous spatialcuing paradigms.     

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.     

Exploring the contributions of spatial and non-spatial working memory to priming of pop-out

Priming of pop-out (PoP) refers to the facilitation of performance that occurs when a target-defining feature is repeated across consecutive trials in a pop-out oddball search task. The underlying mechanism of PoP has been poorly understood and raises important questions about how our visual system is guided by past experiences, even during bottom-up processing. Lee, Mozer, and Vecera (Attention, Perception, & Psychophysics, 71, 1059–1071, 2009) demonstrated that PoP remained unaffected by a concurrent non-spatial visual working memory (VWM) load, and they concluded that PoP occurs through feature gain modulation, essentially eliminating the contribution of memory representations in VWM to PoP. In the present study, we followed up on those results by (a) replicating the null effect of non-spatial VWM load on PoP and (b) examining the effect of spatial VWM load on PoP. The results showed that spatial VWM load does interfere with PoP, supporting the notion that spatial VWM is involved in PoP. In Experiment 2, we extended this finding by manipulating VWM load and observing its consequence on the magnitude of PoP. Increasing spatial VWM load decreased the amount of PoP observed, in a dose-dependent manner, whereas changes in non-spatial VWM load did not. Contrary to Lee et al.’s conclusions, these results suggest that VWM resources appear to contribute to the occurrence of PoP, supporting the theory that PoP is, in fact, a multilevel process in which the deployment of spatial attention, relying on VWM representations, plays an important role.     

Differences in spatial knowledge acquired from maps and navigation

Models of the spatial knowledge people acquire from maps and navigation and the procedures required for spatial judgments using this knowledge are proposed. From a map, people acquire survey knowledge encoding global spatial relations. This knowledge resides in memory in images that can be scanned and measured like a physical map. From navigation, people acquire procedural knowledge of the routes connecting diverse locations. People combine mental simulation of travel through the environment and informal algebra to compute spatial judgments. An experiment in which subjects learned an environment from navigation or from a map evaluates predictions of these models. With moderate exposure, map learning is superior for judgments of relative location and straight-line distances among objects. Learning from navigation is superior for orienting oneself with respect to unseen objects and estimating route distances. With extensive exposure, the performance superiority of maps over navigation vanishes. These and other results are consonant with the proposed mechanisms.     

Using hippocampal-striatal loops for spatial navigation and goal-directed decision-making

The hippocampus plays a central role in spatial representation, declarative and episodic memory. In this area, so-called place cells possess high spatial selectivity, firing preferentially when the individual is within a small area of the environment. Interestingly, it has been found in rats that these cells can be active also when the animal is outside the location or context of their corresponding place field producing so-called "forward sweeps". These typically occur at decision points during task execution and seem to be utilized, among other things, for the evaluation of potential alternative paths. Anticipatory firing is also found in the ventral striatum, a brain area that is strongly interconnected with the hippocampus and is known to encode value and reward. In this paper, we describe a biologically based computational model of the hippocampal-ventral striatum circuit that implements a goal-directed mechanism of choice, with the hippocampus primarily involved in the mental simulation of possible navigation paths and the ventral striatum involved in the evaluation of the associated reward expectancies. The model is validated in a navigation task in which a rat is placed in a complex maze with multiple rewarding sites. We show that the rat mentally activates place cells to simulate paths, estimate their value, and make decisions, implementing two essential processes of model-based reinforcement learning algorithms of choice: look-ahead prediction and the evaluation of predicted states.     

Using hippocampal-striatal loops for spatial navigation and goal-directed decision-making

The hippocampus plays a central role in spatial representation, declarative and episodic memory. In this area, so-called place cells possess high spatial selectivity, firing preferentially when the individual is within a small area of the environment. Interestingly, it has been found in rats that these cells can be active also when the animal is outside the location or context of their corresponding place field producing so-called “forward sweeps”. These typically occur at decision points during task execution and seem to be utilized, among other things, for the evaluation of potential alternative paths. Anticipatory firing is also found in the ventral striatum, a brain area that is strongly interconnected with the hippocampus and is known to encode value and reward. In this paper, we describe a biologically based computational model of the hippocampal-ventral striatum circuit that implements a goal-directed mechanism of choice, with the hippocampus primarily involved in the mental simulation of possible navigation paths and the ventral striatum involved in the evaluation of the associated reward expectancies. The model is validated in a navigation task in which a rat is placed in a complex maze with multiple rewarding sites. We show that the rat mentally activates place cells to simulate paths, estimate their value, and make decisions, implementing two essential processes of model-based reinforcement learning algorithms of choice: look-ahead prediction and the evaluation of predicted states.     

Egocentric organization of spatial activities in imagined navigation

Studies on spatial frameworks suggest that the way we locate objects in imagined environments is influenced by the physical and functional properties of the world and our body. The present study provides evidence that such an influence also characterizes imagined navigation. In Experiment 1, participants followed spatial directions to construct an imagined path, while either keeping constant or updating their orientation at each step. A pattern of step times diagnostic of spatial frameworks was obtained in the updated-orientation but not in the constant-orientation condition. In Experiment 2, participants performed the updated-orientation condition with two levels of external support for the reference frame being used. Step times conformed to the predictions of spatial frameworks in both conditions. Both experiments also provided support that the processes involved in imagined navigation exhibit the operator-operand dynamics of other mental skills previously documented in the mental arithmetic domain. These results reinforce Piaget's (1954) notion that spatial displacements and integer arithmetic share a set of structural characteristics