Border cells without theta rhythmicity in the medial prefrontal cortex.

The medial prefrontal cortex (mPFC) is a key brain structure for higher cognitive functions such as decision-making and goal-directed behavior, many of which require awareness of spatial variables including one's current position within the surrounding environment. Although previous studies have reported spatially tuned activities in mPFC during memory-related trajectory, the spatial tuning of mPFC network during freely foraging behavior remains elusive. Here, we reveal geometric border or border-proximal representations from the neural activity of mPFC ensembles during naturally exploring behavior, with both allocentric and egocentric boundary responses. Unlike most of classical border cells in the medial entorhinal cortex (MEC) discharging along a single wall, a large majority of border cells in mPFC fire particularly along four walls. mPFC border cells generate new firing fields to external insert, and remain stable under darkness, across distinct shapes, and in novel environments. In contrast to hippocampal theta entrainment during spatial working memory tasks, mPFC border cells rarely exhibited theta rhythmicity during spontaneous locomotion behavior. These findings reveal spatially modulated activity in mPFC, supporting local computation for cognitive functions involving spatial context and contributing to a broad spatial tuning property of cortical circuits.

The Anterior Thalamus Preferentially Drives Allocentric But Not Egocentric Orientation Tuning in Postrhinal Cortex.

Navigating a complex world requires integration of multiple spatial reference frames, including information about one's orientation in both allocentric and egocentric coordinates. Combining these two information sources can provide additional information about one's spatial location. Previous studies have demonstrated that both egocentric and allocentric spatial signals are reflected by the firing of neurons in the rat postrhinal cortex (POR), an area that may serve as a hub for integrating allocentric head direction (HD) cell information with egocentric information from center-bearing and center-distance cells. However, we have also demonstrated that POR HD cells are uniquely influenced by the visual properties and locations of visual landmarks, bringing into question whether the POR HD signal is truly allocentric as opposed to simply being a response to visual stimuli. To investigate this issue, we recorded HD cells from the POR of female rats while bilaterally inactivating the anterior thalamus (ATN), a region critical for expression of the "classic" HD signal in cortical areas. We found that ATN inactivation led to a significant decrease in both firing rate and tuning strength for POR HD cells, as well as a disruption in the encoding of allocentric location by conjunctive HD/egocentric cells. In contrast, POR egocentric cells without HD tuning were largely unaffected in a consistent manner by ATN inactivation. These results indicate that the POR HD signal originates at least partially from projections from the ATN and supports the view that the POR acts as a hub for the integration of egocentric and allocentric spatial representations.

EEG markers of successful allocentric spatial working memory maintenance in humans.

Several brain regions in the frontal, occipital and medial temporal lobes are known to contribute to spatial information processing. In contrast, the oscillatory patterns contributing to allocentric spatial working memory maintenance are poorly understood, especially in humans. Here, we tested twenty-three 21- to 32-year-old and twenty-two 64- to 76-year-old healthy right-handed adults in a real-world, spatial working memory task and recorded electroencephalographic (EEG) activity during the maintenance period. We established criteria for designating recall trials as perfect (no errors) or failed (errors and random search) and identified 8 young and 13 older adults who had at least 1 perfect and 1 failed trial amongst 10 recall trials. Individual alpha frequency-based analyses were used to identify oscillatory patterns during the maintenance period of perfect and failed trials. Spectral scalp topographies showed that individual theta frequency band relative power was stronger in perfect than in failed trials in the frontal midline and posterior regions. Similarly, gamma band (30-40 Hz) relative power was stronger in perfect than in failed trials over the right motor cortex. Exact low-resolution brain electromagnetic tomography in the frequency domain identified greater theta power in perfect than in failed trials in the secondary visual area (BA19) and greater gamma power in perfect than in failed trials in the right supplementary motor area. The findings of this exploratory study suggest that theta oscillations in the occipital lobe and gamma oscillations in the secondary motor cortex (BA6) play a particular role in successful allocentric spatial working memory maintenance.

Hierarchical processing of feature, egocentric and relational information for spatial orientation in domestic chicks.

Animals can use different types of information for navigation. Domestic chicks (Gallus gallus) prefer to use local features as a beacon over spatial relational information. However, the role of egocentric navigation strategies is less understood. Here, we tested domestic chicks' egocentric and allocentric orientation abilities in a large circular arena. In experiment 1, we investigated whether domestic chicks possess a side bias during viewpoint-dependent egocentric orientation, revealing facilitation for targets on the chicks' left side. Experiment 2 showed that local features are preferred over viewpoint-dependent egocentric information when the two conflict. Lastly, in experiment 3, we found that in a situation where there is a choice between egocentric and allocentric spatial relational information provided by free-standing objects, chicks preferentially rely on egocentric information. We conclude that chicks orient according to a hierarchy of cues, in which the use of the visual appearance of an object is the dominant strategy, followed by viewpoint-dependent egocentric information and finally by spatial relational information.

Cortical Correlates of Visuospatial Switching Processes Between Egocentric and Allocentric Frames of Reference: A fNIRS Study.

Human beings represent spatial information according to egocentric (body-to-object) and allocentric (object-to-object) frames of reference. In everyday life, we constantly switch from one frame of reference to another in order to react effectively to the specific needs of the environment and task demands. However, to the best of our knowledge, no study to date has investigated the cortical activity of switching and non-switching processes between egocentric and allocentric spatial encodings. To this aim, a custom-designed visuo-spatial memory task was administered and the cortical activities underlying switching vs non-switching spatial processes were investigated. Changes in concentrations of oxygenated and deoxygenated haemoglobin were measured using functional near-infrared spectroscopy (fNIRS). Participants were asked to memorize triads of geometric objects and then make two consecutive judgments about the same triad. In the non-switching condition, both spatial judgments considered the same frame of reference: only egocentric or only allocentric. In the switching condition, if the first judgment was egocentric, the second one was allocentric (or vice versa). The results showed a generalized activation of the frontal regions during the switching compared to the non-switching condition. Additionally, increased cortical activity was found in the temporo-parietal junction during the switching condition compared to the non-switching condition. Overall, these results illustrate the cortical activity underlying the processing of switching between body position and environmental stimuli, showing an important role of the temporo-parietal junction and frontal regions in the preparation and switching between egocentric and allocentric reference frames.

Perspective matters in goal-predictive gaze shifts during action observation: Results from 6-, 9-, and 12-month-olds and adults.

Research on goal-predictive gaze shifts in infancy so far has mostly focused on the effect of infants' experience with observed actions or the effect of agency cues that the observed agent displays. However, the perspective from which an action is presented to the infants (egocentric vs. allocentric) has received only little attention from researchers despite the fact that the natural observation of own actions is always linked to an egocentric perspective, whereas the observation of others' actions is often linked to an allocentric perspective. The current study investigated the timing of 6-, 9-, and 12-month-olds' goal-predictive gaze behavior, as well as that of adults, during the observation of simple human grasping actions that were presented from either an egocentric or allocentric perspective (within-participants design). The results showed that at 6 and 9 months of age, the infants predicted the action goal only when observing the action from the egocentric perspective. The 12-month-olds and adults, in contrast, predicted the action in both perspectives. The results therefore are in line with accounts proposing an advantage of egocentric versus allocentric processing of social stimuli, at least early in development. This study is among the first to show this egocentric bias already during the first year of life.

Striatal Cholinergic Interneurons Are Required for Contending Strategy Selection While Solving Spatial Navigation Problems.

How do animals adopt a given behavioral strategy to solve a recurrent problem when several effective strategies are available to reach the goal? Here we provide evidence that striatal cholinergic interneurons (SCINs) modulate their activity when mice must select between different strategies with similar goal-reaching effectiveness. Using a cell type-specific transgenic murine system, we show that adult SCIN ablation impairs strategy selection in navigational tasks where a goal can be independently achieved by adopting an allocentric or egocentric strategy. SCIN-depleted mice learn to achieve the goal in these tasks, regardless of their appetitive or aversive nature, in a similar way as controls. However, they cannot shift away from their initially adopted strategies, as control mice do, as training progresses. Our results indicate that SCINs are required for shaping the probability function used for strategy selection as experience accumulates throughout training. Thus, SCINs may be critical for the resolution of cognitive conflicts emerging when several strategies compete for behavioral control while adapting to environmental demands. Our findings may increase our understanding about the emergence of perseverative/compulsive traits in neuropsychiatric disorders with a reported SCIN reduction, such as Tourette and Williams syndromes.SIGNIFICANCE STATEMENT Selecting the best suited strategy to solve a problem is vital. Accordingly, available strategies must be compared across multiple dimensions, such as goal attainment effectiveness, cost-benefit trade-off, and cognitive load. The striatum is involved in strategy selection when strategies clearly diverge in their goal attainment capacity; however, its role whenever several strategies can be used for goal reaching-therefore making selection dependent on additional strategy dimensions-remains poorly understood. Here, we show that striatal cholinergic interneurons can signal strategy competition. Furthermore, they are required to adopt a given strategy whenever strategies with similar goal attainment capacity compete for behavioral control. Our study suggests that striatal cholinergic dysfunction may result in anomalous resolution of problems whenever complex cognitive valuations are required.

A thalamo-parietal cortex circuit is critical for place-action coordination.

The anterior and lateral thalamus (ALT) contains head direction cells that signal the directional orientation of an individual within the environment. ALT has direct and indirect connections with the parietal cortex (PC), an area hypothesized to play a role in coordinating viewer-dependent and viewer-independent spatial reference frames. This coordination between reference frames would allow an individual to translate movements toward a desired location from memory. Thus, ALT-PC functional connectivity would be critical for moving toward remembered allocentric locations. This hypothesis was tested in rats with a place-action task that requires associating an appropriate action (left or right turn) with a spatial location. There are four arms, each offset by 90°, positioned around a central starting point. A trial begins in the central starting point. After exiting a pseudorandomly selected arm, the rat had to displace the correct object covering one of two (left versus right) feeding stations to receive a reward. For a pair of arms facing opposite directions, the reward was located on the left, and for the other pair, the reward was located on the right. Thus, each reward location had a different combination of allocentric location and egocentric action. Removal of an object was scored as correct or incorrect. Trials in which the rat did not displace any objects were scored as "no selection" trials. After an object was removed, the rat returned to the center starting position and the maze was reset for the next trial. To investigate the role of the ALT-PC network, muscimol inactivation infusions targeted bilateral PC, bilateral ALT, or the ALT-PC network. Muscimol sessions were counterbalanced and compared to saline sessions within the same animal. All inactivations resulted in decreased accuracy, but only bilateral PC inactivations resulted in increased non selecting, increased errors, and longer latency responses on the remaining trials. Thus, the ALT-PC circuit is critical for linking an action with a spatial location for successful navigation.

A place with a view: A first-person perspective in the hippocampal memory space.

How do rodents' and primates' differences in visual perception impact the way the brain constructs egocentric and allocentric reference frames to represent stimuli in space? Strikingly, there are important similarities in the egocentric spatial reference frames through which cortical regions represent objects with respect to an animal's head or body in rodents and primates. These egocentric representations are suitable for navigation across species. However, while the rodent hippocampus represents allocentric place, I draw on several pieces of evidence suggesting that an egocentric reference frame is paramount in the primate hippocampus, and relates to the first-person perspective characteristic of a primate's field of view. I further discuss the link between an allocentric reference frame and a conceptual frame to suggest that an allocentric reference frame is a semantic construct in primates. Finally, I discuss how views probe memory recall and support prospective coding, and as they are based on a first-person perspective, are a powerful tool for probing episodic memory across species.

A model for transforming egocentric views into goal-directed behavior.

Neurons in the rat postrhinal cortex (POR) respond to the egocentric (observer-centered) bearing and distance of the boundaries, or geometric center, of an enclosed space. Understanding of the precise geometric and sensory properties of the environment that generate these signals is limited. Here we model how this signal may relate to visual perception of motion parallax along environmental boundaries. A behavioral extension of this tuning is the known 'centering response', in which animals follow a spatial gradient function based on boundary parallax to guide behavior toward the center of a corridor or enclosure. Adding an allocentric head direction signal to this representation can translate the gradient across two-dimensional space and provide a new gradient for directing behavior to any location. We propose a model for how this signal may support goal-directed navigation via projections to the dorsomedial striatum. The result is a straightforward code for navigational variables derived from visual geometric properties of the surrounding environment, which may be used to map space and transform incoming sensory information into an appropriate motor output.

Neurobehavioral basis of Maier 3-table and other matching-to-place tasks.

The Maier 3-table task comprises three phases conducted each day. During the exploration phase, rats explore the entire apparatus. During the information phase, the rats are placed on one of the three tables where food is found. During the test phase, the animals are placed at the starting point on one of the two remaining tables and must enter the goal table where they previously ate. The acquisition of the Maier 3-table task was slowed down after lesions of the septum, fornix, hippocampus, medial prefrontal cortex, or posterior parietal cortex. Because of its time-consuming nature, the Maier 3-table task has more recently been superseded by appetitive matching-to-place in Y- or T-mazes or the circular water maze, because experimenters skip over the exploration phase. Nevertheless, like the Maier 3-table task, the acquisition of the Y- or T-maze matching-to-place task was retarded after lesions of the medial septum or medial prefrontal cortex, more particularly its prelimbic-infralimbic part. Like the previous task, the water-maze version is sensitive to lesions of the medial septum or retrosplenial cortex. Despite methodological differences between the three procedures, these results indicate common neurobiological bases of matching-to-place learning.

Neglecting the bottom space: an object-based disorder? A two-case observational study.

Altitudinal neglect is an atypical form of spatial neglect where brain-damaged patients neglect the lower, or sometimes the upper, part of the space. Our understanding of this phenomena is limited, with unknown occurrence across different reference frames, such as distance (peripersonal vs. extrapersonal) and system of reference (egocentric vs. allocentric). Two patients with acute bilateral (P1) or right hemispheric (P2) stroke, with signs of bottom altitudinal neglect, underwent an extensive evaluation of neglect within 10 days post-stroke. Assessments involved altitudinal neglect and unilateral spatial neglect (USN) in peripersonal space, exploring egocentric and allocentric signs and in extrapersonal space. Compared to a control group of 15 healthy age-matched subjects, patients showed allocentric and egocentric left USN in peripersonal space, and mostly allocentric signs of altitudinal neglect. No signs of neglect were evidenced in extrapersonal space. Altitudinal neglect could thus present as an allocentric form of spatial neglect, suggesting that allocentric representations may not only affect the deployment of attentional resources along horizontal dimensions but also operate along vertical dimensions. Future studies should deepen our understanding of altitudinal neglect, eventually leading to further unravel spatial processes that control attention, their corresponding brain mechanisms, and implications for patients' rehabilitation and functional outcome.

Timing of Allocentric and Egocentric Spatial Processing in Human Intracranial EEG.

Spatial reference frames (RFs) play a key role in spatial cognition, especially in perception, spatial memory, and navigation. There are two main types of RFs: egocentric (self-centered) and allocentric (object-centered). Although many fMRI studies examined the neural correlates of egocentric and allocentric RFs, they could not sample the fast temporal dynamics of the underlying cognitive processes. Therefore, the interaction and timing between these two RFs remain unclear. Taking advantage of the high temporal resolution of intracranial EEG (iEEG), we aimed to determine the timing of egocentric and allocentric information processing and describe the brain areas involved. We recorded iEEG and analyzed broad gamma activity (50-150 Hz) in 37 epilepsy patients performing a spatial judgment task in a three-dimensional circular virtual arena. We found overlapping activation for egocentric and allocentric RFs in many brain regions, with several additional egocentric- and allocentric-selective areas. In contrast to the egocentric responses, the allocentric responses peaked later than the control ones in frontal regions with overlapping selectivity. Also, across several egocentric or allocentric selective areas, the egocentric selectivity appeared earlier than the allocentric one. We identified the maximum number of egocentric-selective channels in the medial occipito-temporal region and allocentric-selective channels around the intraparietal sulcus in the parietal cortex. Our findings favor the hypothesis that egocentric spatial coding is a more primary process, and allocentric representations may be derived from egocentric ones. They also broaden the dominant view of the dorsal and ventral streams supporting egocentric and allocentric space coding, respectively.

Memory recall: New behavioral protocols for examining distinct forms of context specific recall in animals.

This study outlines two novel protocols for examining context specific recall in animals prior to embarking on neurobiological studies. The approach is distinct from and contrasts with studies investigating associative familiarity that depend upon procedural variations of the widely used novel object recognition task. It uses an event arena in which animals are trained across numerous sessions to search for, find and dig up reward from sandwells during sample and choice trials - a prominent spatial event for a rodent. The arena could be laid out as either of two highly distinct contexts with which the animals became fully familiar throughout training. In one protocol, the location of the correct sandwell in each context remained stable across days, whereas in the other, the correct digging location varied in a counterbalanced manner across each successive session. Thus, context-specific recall of the spatial location of successful digging during choice trials was either from a stable long-term memory or could reflect context specific spatial recency of the location where reward had been available that session. Both protocols revealed effective memory recall in choice and probe tests which, at the point of test, were procedurally identical in both cases.

Overcoming navigational challenges: A novel approach to the study and assessment of topographical orientation.

Several studies investigating environmental navigation require participants to navigate in virtual environments, in which the proprioceptive and vestibular components present during real environmental navigation are lost. Here, we aimed to provide a novel computerized ecological navigational battery, investigating whether the absence of proprioceptive and vestibular inputs yields a representation of the navigational space comparable to that acquired ecologically. In Study 1, 38 participants underwent two sets of tasks, one performed in a laboratory-based setting (LBS) and the other in an ecological environment (EE), with both including evaluation of route, landmark, and survey knowledge and a landmark ordering task. All tasks, except the route task, significantly correlated between EE and LBS. In LBS, performance in the landmark ordering task was predicted by that in the survey task, but not by those in the route and landmark tasks. Results of Study 1 were replicated in Study 2, in which 44 participants completed a modified and shorter online version of LBS tests. Reliability of the online LBS tests was also tested and showed a moderate-to-high internal consistency. Overall, results show that the conditions in which tasks are performed affect the acquisition of route knowledge, likely due to the lack of proprioceptive and vestibular information in LBS. However, LBS tasks presented here provide a standard battery of tests that can overcome the replicability problems encountered by ecological navigation tests, while taking into consideration all the complexities of navigational processes in terms of the use of landmark, route, and survey strategies.

For me or for others? The better-than-average effect and negative feelings toward average others during the COVID-19 pandemic.

During the first outbreak of the coronavirus disease 2019 (COVID-19), many people expressed hatred toward others whom they believed were responsible for the situation. Such increase in negative affect could be resultant of the better-than-average effect (BTAE), which refers to the phenomenon of believing that one is superior to average others. This study investigated the relationship between the BTAE and emotional valence toward others and tested whether the relationship was moderated by allocentric goals (i.e., concerned with the interests of others rather than themselves) and culture. Participants from the U.S. (N = 210) and South Korea (N = 214) were asked about their perceptions on whether they were better than others at preventing the COVID-19 infection, how they felt about others regarding COVID-19, and for whom they were preventing COVID-19. The results indicated that people showing more BTAE in relation to preventing the COVID-19 infection reported more negative emotional valence toward others, but the relationship was moderated by allocentric goals. In particular, the U.S. participants with higher allocentric goals reported less negatively valenced emotions, while the same was not found in Korean participants. The findings suggest the power of allocentric goals in diminishing the BTAE in some cultures, which may possibly explain the negative emotions some people experience when following social distancing rules.

The neural underpinnings of allocentric thinking in a novel signaling task.

The ability to adopt the perspectives of others is fundamental to effective communication in social interactions. However, the neural correlates of allocentric thinking in communicative signaling remain unclear. We adapted a novel signaling task in which the signaler was given the target word and must choose a one-word signal to help the receiver guess the target. Behavioral results suggest that speakers can use allocentric thinking to choose signals that are salient from the perspective of the receiver rather than their own point of view. At the neural level, functional magnetic resonance imaging (fMRI) data reveal that the medial prefrontal cortex (mPFC), ventral striatum, and temporal-parietal junction are more activated when signalers engage in allocentric than egocentric thinking. Moreover, functional connectivity between the mPFC and ventral striatum predicted individuals' perspective-taking ability during successful communication. These findings reveal that neural representations in the mPFC-striatum network support perspective-taking in complex social decision making, providing a new perspective on how the brain arbitrates between allocentric thinking and egocentric thinking in communication and social coordination.

Human spatial navigation: Neural representations of spatial scales and reference frames obtained from an ALE meta-analysis.

Humans use different spatial reference frames (allocentric or egocentric) to navigate successfully toward their destination in different spatial scale spaces (environmental or vista). However, it remains unclear how the brain represents different spatial scales and different spatial reference frames. Thus, we conducted an activation likelihood estimation (ALE) meta-analysis of 47 fMRI articles involving human spatial navigation. We found that both the environmental and vista spaces activated the parahippocampal place area (PPA), retrosplenial complex (RSC), and occipital place area in the right hemisphere. The environmental space showed stronger activation than the vista space in the occipital and frontal regions. No brain region exhibited stronger activation for the vista than the environmental space. The allocentric and egocentric reference frames activated the bilateral PPA and right RSC. The allocentric frame showed more stronger activations than the egocentric frame in the right culmen, left middle frontal gyrus, and precuneus. No brain region displayed stronger activation for the egocentric than the allocentric navigation. Our findings suggest that navigation in different spatial scale spaces can evoke specific and common brain regions, and that the brain regions representing spatial reference frames are not absolutely separated.

Is habitat selection in the wild shaped by individual-level cognitive biases in orientation strategy?

Cognitive biases for encoding spatial information (orientation strategies) in relation to self (egocentric) or landmarks (allocentric) differ between species or populations according to the habitats they occupy. Whether biases in orientation strategy determine early habitat selection or if individuals adapt their biases following experience is unknown. We determined orientation strategies of pheasants, Phasianus colchicus, using a dual-strategy maze with an allocentric probe trial, before releasing them (n = 20) into a novel landscape, where we monitored their movement and habitat selection. In general, pheasants selected for woodland over non-woodland habitat, but allocentric-biased individuals exhibited weaker avoidance of non-woodland habitat, where we expected allocentric navigation to be more effective. Sex did not influence selection but was associated with speed and directional persistence in non-woodland habitat. Our results suggest that an individual's habitat selection is associated with inherent cognitive bias in early life, but it is not yet clear what advantages this may offer.

Neurons including hippocampal spatial view cells, and navigation in primates including humans.

A new theory is proposed of mechanisms of navigation in primates including humans in which spatial view cells found in the primate hippocampus and parahippocampal gyrus are used to guide the individual from landmark to landmark. The navigation involves approach to each landmark in turn (taxis), using spatial view cells to identify the next landmark in the sequence, and does not require a topological map. Two other cell types found in primates, whole body motion cells, and head direction cells, can be utilized in the spatial view cell navigational mechanism, but are not essential. If the landmarks become obscured, then the spatial view representations can be updated by self-motion (idiothetic) path integration using spatial coordinate transform mechanisms in the primate dorsal visual system to transform from egocentric to allocentric spatial view coordinates. A continuous attractor network or time cells or working memory is used in this approach to navigation to encode and recall the spatial view sequences involved. I also propose how navigation can be performed using a further type of neuron found in primates, allocentric-bearing-to-a-landmark neurons, in which changes of direction are made when a landmark reaches a particular allocentric bearing. This is useful if a landmark cannot be approached. The theories are made explicit in models of navigation, which are then illustrated by computer simulations. These types of navigation are contrasted with triangulation, which requires a topological map. It is proposed that the first strategy utilizing spatial view cells is used frequently in humans, and is relatively simple because primates have spatial view neurons that respond allocentrically to locations in spatial scenes. An advantage of this approach to navigation is that hippocampal spatial view neurons are also useful for episodic memory, and for imagery.