Path Integration Systems Research Articles

Impaired speed encoding and grid cell periodicity in a mouse model of tauopathy.

Dementia is associated with severe spatial memory deficits which arise from dysfunction in hippocampal and parahippocampal circuits. For spatially sensitive neurons, such as grid cells, to faithfully represent the environment these circuits require precise encoding of direction and velocity information. Here, we have probed the firing rate coding properties of neurons in medial entorhinal cortex (MEC) in a mouse model of tauopathy. We find that grid cell firing patterns are largely absent in rTg4510 mice, while head-direction tuning remains largely intact. Conversely, neural representation of running speed information was significantly disturbed, with smaller proportions of MEC cells having firing rates correlated with locomotion in rTg4510 mice. Additionally, the power of local field potential oscillations in the theta and gamma frequency bands, which in wild-type mice are tightly linked to running speed, was invariant in rTg4510 mice during locomotion. These deficits in locomotor speed encoding likely severely impact path integration systems in dementia.

Landmark navigation in a mantis shrimp.

Mantis shrimp commonly occupy burrows in shallow, tropical waters. These habitats are often structurally complex where many potential landmarks are available. Mantis shrimp of the species Neogonodactylus oerstedii return to their burrows between foraging excursions using path integration, a vector-based navigational strategy that is prone to accumulated error. Here, we show that N. oerstedii can navigate using landmarks in parallel with their path integration system, correcting for positional uncertainty generated when navigating using solely path integration. We also report that when the path integration and landmark navigation systems are placed in conflict, N. oerstedii will orientate using either system or even switch systems enroute. How they make the decision to trust one navigational system over another is unclear. These findings add to our understanding of the refined navigational toolkit N. oerstedii relies upon to efficiently navigate back to its burrow, complementing its robust, yet error prone, path integration system with landmark guidance.

IMPAIRED NEURAL CODE OF SPATIAL INFORMATION IN A MOUSE MODEL OF TAU PATHOLOGY

Dementias are associated with severe spatial memory deficits which likely arises due to dysfunction in hippocampal and parahippocampal circuits. These circuits rely on precise encoding of directional and velocity information for spatially-sensitive neurons, such as grid cells in the medial entorhinal cortex (mEC), to faithfully represent the environment. In this study we examined the impact of tau pathology on the spatial coding properties of neurons in the mEC, using a well-studied transgenic mouse model of tauopathy, the rTg4510 mouse. We have used high density silicon probe electrode arrays to examine the local field potential (LFP) and firing rate coding properties of mEC neurons in male rTg4510 mice (7-8 month old), a mouse model of tauopathy which displays severe spatial memory deficits. Grid cell firing patterns were largely absent in rTg4510 mice, suggesting deficiencies in some, or all, of the information required for path integration. Interestingly, we find that head-direction cells, a key component of any path integration system, are largely intact. In contrast, representation of running speed is significantly disturbed in several ways. A significantly smaller proportion of mEC cells from rTg4510 mice display firing rates correlated with locomotion. Of those cells, a much greater proportion are negatively modulated. Finally, we show large scale changes to neuronal oscillations in rTg4510 mice, which in wildtype animals are tightly linked to running speed. Deficits in locomotor speed encoding are likely to severely impact the ability of animals to continuously update positional information and thus disrupt path integration systems in these mice and in dementia patients.

Exclusive shift from path integration to visual cues during the rapid escape run of fiddler crabs

Animals are equipped with sophisticated guidance systems that enable them to navigate efficiently. Previous studies suggest that foraging animals such as desert ants tend to combine guidance systems in a weighted manner, where the weight given to each cue gradually changes during the approach to the goal. However, when subjected to rapid enforced decision making (e.g. under predation risk), the animal may use alternative mechanisms, as recently suggested for ecologically relevant decisions involving time constraints in humans. We show here that fiddler crabs, Uca perplexa, scuttling to their burrows when threatened, responded to visual cues only if their path integration (PI) systems indicated nearness to their burrows. When homing errors were imposed by placing fake entrances (visual cues) along their homing paths and masking their true burrows (the goal of PI), the threatened crabs altered their behaviour towards visual cues according to the remaining PI vector length; if it was long, they continued running until they arrived at the masked true burrow, ignoring the visual cue, but if it was short, they suddenly stopped at the fake entrance. Our results suggest that, for fiddler crabs, PI and the view are mutually exclusive cues and that they instantly shift from one to the other if they approach the end of the home vector, instead of combining systems in a weighted manner. This could enable them to avoid entering the wrong burrow, where they would be ejected by the resident crab and be subject to predation.

Piloting systems reset path integration systems during position estimation.

During locomotion, individuals can determine their positions with either idiothetic cues from movement (path integration systems) or visual landmarks (piloting systems). This project investigated how these 2 systems interact in determining humans' positions. In 2 experiments, participants studied the locations of 5 target objects and 1 single landmark. They walked a path after the targets and the landmark had been removed and then replaced the targets at the end of the path. Participants' position estimations were calculated based on the replaced targets' locations (Mou & Zhang, 2014). In Experiment 1, participants walked a 2-leg path. The landmark reappeared in a different location during or after walking the second leg. The results showed that participants' position estimations followed idiothetic cues in the former case, but the displaced landmark in the latter case. In Experiment 2, participants saw the displaced landmark when they reached the end of the second leg and then walked a third leg without the view of the landmark. Participants were asked or not to point to 1 of the targets before they walked the third leg. The results showed that the initial position of the third leg was still influenced by the displaced landmark in the former case, but was determined by idiothetic cues in the latter case. These results suggest that the path integration system works dynamically and the piloting system resets the path integration system when people judge their positions in the presence of conflicting piloting cues. (PsycINFO Database Record

Building a cognitive map by assembling multiple path integration systems

Path integration and cognitive mapping are two of the most important mechanisms for navigation. Path integration is a primitive navigation system which computes a homing vector based on an animal's self-motion estimation, while cognitive map is an advanced spatial representation containing richer spatial information about the environment that is persistent and can be used to guide flexible navigation to multiple locations. Most theories of navigation conceptualize them as two distinctive, independent mechanisms, although the path integration system may provide useful information for the integration of cognitive maps. This paper demonstrates a fundamentally different scenario, where a cognitive map is constructed in three simple steps by assembling multiple path integrators and extending their basic features. The fact that a collection of path integration systems can be turned into a cognitive map suggests the possibility that cognitive maps may have evolved directly from the path integration system.

Fine-Tuning and the Stability of Recurrent Neural Networks

A central criticism of standard theoretical approaches to constructing stable, recurrent model networks is that the synaptic connection weights need to be finely-tuned. This criticism is severe because proposed rules for learning these weights have been shown to have various limitations to their biological plausibility. Hence it is unlikely that such rules are used to continuously fine-tune the network in vivo. We describe a learning rule that is able to tune synaptic weights in a biologically plausible manner. We demonstrate and test this rule in the context of the oculomotor integrator, showing that only known neural signals are needed to tune the weights. We demonstrate that the rule appropriately accounts for a wide variety of experimental results, and is robust under several kinds of perturbation. Furthermore, we show that the rule is able to achieve stability as good as or better than that provided by the linearly optimal weights often used in recurrent models of the integrator. Finally, we discuss how this rule can be generalized to tune a wide variety of recurrent attractor networks, such as those found in head direction and path integration systems, suggesting that it may be used to tune a wide variety of stable neural systems.

Which coordinate system for modelling path integration?

Path integration is a navigation strategy widely observed in nature where an animal maintains a running estimate, called the home vector, of its location during an excursion. Evidence suggests it is both ancient and ubiquitous in nature, and has been studied for over a century. In that time, canonical and neural network models have flourished, based on a wide range of assumptions, justifications and supporting data. Despite the importance of the phenomenon, consensus and unifying principles appear lacking. A fundamental issue is the neural representation of space needed for biological path integration. This paper presents a scheme to classify path integration systems on the basis of the way the home vector records and updates the spatial relationship between the animal and its home location. Four extended classes of coordinate systems are used to unify and review both canonical and neural network models of path integration, from the arthropod and mammalian literature. This scheme demonstrates analytical equivalence between models which may otherwise appear unrelated, and distinguishes between models which may superficially appear similar. A thorough analysis is carried out of the equational forms of important facets of path integration including updating, steering, searching and systematic errors, using each of the four coordinate systems. The type of available directional cue, namely allothetic or idiothetic, is also considered. It is shown that on balance, the class of home vectors which includes the geocentric Cartesian coordinate system, appears to be the most robust for biological systems. A key conclusion is that deducing computational structure from behavioural data alone will be difficult or impossible, at least in the absence of an analysis of random errors. Consequently it is likely that further theoretical insights into path integration will require an in-depth study of the effect of noise on the four classes of home vectors.

What could homing pigeons tell us about navigational impairments in Alzheimer’s patients? Activational effects of odors

Navigation by path integration has been demonstrated in species as diverse as ants, homing pigeons, and humans. In a recent study of olfactory effects on path integration in young homing pigeons, we showed that birds deprived of odors during displacement to nearby release sites were disoriented, while those exposed to natural odors, or to artificial/novel odors, were homeward oriented. These findings show that olfactory input activates non-olfactory path integration systems and, in the absence of olfactory stimulation, cues normally used by young pigeons for path integration, failed to produce homeward orientation. Interestingly, in humans, olfactory dysfunction is frequently observed in patients in the early stages of Alzheimer’s disease. A large portion of those patients also exhibit a specific failure of path integration ability, including a deficit in perception of radial optic flow cues necessary for accurate heading determination (“motion blindness”). Here we suggest that loss of olfactory activation of path integrations systems could explain the navigational impairment in the early stages of Alzheimer's disease patients. Moreover, we propose that odor exposures, similar to experiments carried out with pigeons, provide a powerful non-invasive technique to determine whether deficits on olfactory activation play a significant role in this debilitating disease.

Gender differences in cue preference during path integration in virtual environments

Three studies were conducted to examine whether men and women differ in how they recalibrate their path-integration systems when walking without vision in virtual environments. Distance cues provided by a scene and a tone, which ended each trial, were placed in conflict. Participants briefly viewed a room with a target, which was offset from their midlines and hung inside a doorframe on the far wall. After viewing, participants walked to the target's position until a tone sounded, ending the trial. In two experiments the doorframe was placed at 6 m and the tone sounded at 4 or 8 m. The rooms had minimal or photorealistic texturing applied. The third experiment used photorealistic texturing, but here the tone sounded at 6 m and the doorframe was presented at 4 or 8 m. Path angles were recorded to estimate perceived distance to the target. In all conditions tested, the women failed to scale their path angles. The men, however, scaled their path-angles with the auditory cue in the minimal-texture condition, but with the visual cue in the photorealistic-texture conditions. These results suggest that gender differences exist in the way that humans recalibrate their path-integration systems when walking without vision in virtual environments.

The ant's path integration system: a neural architecture

A model is developed by which path integration as observed in many animal species could be implemented neurobiologically. The proposed architecture is able to describe the navigation behaviour of Cataglyphis ants, and that of other social insects, at the level of interacting neurons. The basic idea of this architecture is the concept of activity patterns travelling along neural chains. Although experimental evidence has yet to be provided, this concept seems biologically plausible and not limited to the navigation problem. Neural chains are able to represent variables by activity patterns with high accuracy and temporal stability. Moreover, they are able to integrate incremental signals with high precision. Cyclical chains of neurons show superior performance as soon as cyclical variables are to be represented and integrated. Finally, representation of cyclical variables by travelling activity peaks allows simple approximations of goniometric functions as they are used in path integration systems.