A unified theory for the computational and mechanistic origins of grid cells

The discovery of entorhinal grid cells has generated considerable interest in how and why hexagonal firing fields might mechanistically emerge in a generic manner from neural circuits, and what their computational significance might be. Here we forge an intimate link between the computational problem of path-integration and the existence of hexagonal grids, by demonstrating that such grids arise generically in biologically plausible neural networks trained to path integrate. Moreover, we develop a unifying theory for why hexagonal grids are so ubiquitous in path-integrator circuits. Such trained networks also yield powerful mechanistic hypotheses, exhibiting realistic levels of biological variability not captured by hand-designed models. We furthermore develop methods to analyze the connectome and activity maps of our trained networks to elucidate fundamental mechanisms underlying path integration. These methods provide an instructive roadmap to go from connectomic and physiological measurements to conceptual understanding in a manner that might be generalizable to other settings.

Role of the pheromone for orientation in the group foraging ant, Veromessor pergandei

Role of the pheromone for orientation in the group foraging ant, Veromessor pergandei Navigation is comprised of a variety of strategies which rely on multiple external cues to shape a navigator’s behavioral output. An additional navigational challenge is coping with forces such as wind and water currents that push navigators off-course. Here, we explore the cue interactions that dictate orientation and foragers’ ability to counter course altering rotational changes in the desert ant, Veromessor pergandei. We found a cross sensory interaction between the pheromone cue and the path integrator underlies correct orientation during the inbound journey. The celestial compass provides directional information while the presence of the trail pheromone acts as a critical context cue, triggering distinct behavioral responses (vector orientation, search and backtracking). A particularly interesting interaction occurs between the pheromone and the forager’s vector state. While exposed to the pheromone, foragers orient to the vector direction regardless of vector state, while in the pheromone’s absence the current vector triggers the switch between behaviors. Such interactions maximize the foragers’ return to the nest and inhibit movement off the trail. Finally, our manipulations continuously pushed foragers away from their desired heading, yet foragers were highly proficient at counteracting these changes, steering to maintain a correct heading even at rotational speeds of ~40°/s.

Traveling through light clutter: Path integration and panorama guided navigation in the Sonoran Desert ant, Novomessor cockerelli

Foraging ants use multiple navigational strategies, including path integration and visual panorama cues, which are used simultaneously and weighted based upon context, the environment and the species’ sensory ecology. In particular, the amount of visual clutter in the habitat predicts the weighting given to the forager’s path integrator and surrounding panorama cues. Here, we characterize the individual cue use and cue weighting of the Sonoran Desert ant, Novomessor cockerelli, by testing foragers after local and distant displacement. Foragers attend to both a path-integration-based vector and the surrounding panorama to navigate, on and off foraging routes. When both cues were present, foragers initially oriented to their path integrator alone, yet weighting was dynamic, with foragers abandoning the vector and switching to panorama-based navigation after a few meters. If displaced to unfamiliar locations, experienced foragers travelled almost their full homeward vector (~85%) before the onset of search. Through panorama analysis, we show views acquired on-route provide sufficient information for orientation over only short distances, with rapid parallel decreases in panorama similarity and navigational performance after even small local displacements. These findings are consistent with heavy path integrator weighting over the panorama when the local habitat contains few prominent terrestrial cues.

Path integration error and adaptable search behaviors in a mantis shrimp

ABSTRACTMantis shrimp of the species Neogonodactylus oerstedii occupy small burrows in shallow waters throughout the Caribbean. These animals use path integration, a vector-based navigation strategy, to return to their homes while foraging. Here, we report that path integration in N. oerstedii is prone to error accumulated during outward foraging paths and we describe the search behavior that N. oerstedii employs after it fails to locate its home following the route provided by its path integrator. This search behavior forms continuously expanding, non-oriented loops that are centered near the point of search initiation. The radius of this search is scaled to the animal's positional uncertainty during path integration, improving the effectiveness of the search. The search behaviors exhibited by N. oerstedii bear a striking resemblance to search behaviors in other animals, offering potential avenues for the comparative examination of search behaviors and how they are optimized in disparate taxa.

Path integration error and adaptable search behaviors in a mantis shrimp

Mantis shrimp of the species Neogonodactylus oerstedii occupy small burrows in shallow waters throughout the Caribbean. These animals use path integration, a vector-based navigation strategy, to return to their homes while foraging. Here we report that path integration in N. oerstedii is prone to error accumulated during outward foraging paths and we describe the search behavior that N. oerstedii employs after it fails to locate its home following the route provided by its path integrator. This search behavior forms continuously expanding, non-oriented loops that are centered near the point of search initiation. The radius of this search is apparently scaled to the animal’s accumulated error during path integration, improving the effectiveness of the search. The search behaviors exhibited by N. oerstedii bear a striking resemblance to search behaviors in other animals, offering potential avenues for the comparative examination of search behaviors and how they are optimized in disparate taxa.Summary StatementMantis shrimp use path integration, an error-prone navigational strategy, when travelling home. When path integration fails, mantis shrimp employ a stereotyped yet flexible search pattern to locate their homes.

How do backward walking ants (Cataglyphis velox) cope with navigational uncertainty?

ABSTRACTCurrent opinion in insect navigation assumes that animals need to align with the goal direction to recognise familiar views and approach it. Yet, ants sometimes drag heavy food items backward to the nest and it is still unclear to what extent they rely on visual memories while doing so. In this study displacement experiments and alterations of the visual scenery reveal that ants do indeed recognise and use the learnt visual scenery to guide their path while walking backward. In addition, the results show that backward homing ants estimate their directional certainty by combining visual familiarity with other cues such as their path integrator and the time spent backward. A simple model that combines path integration with repulsive and attractive visual memories captures the results.

Multiple orientation cues in an Australian trunk-trail-forming ant, Iridomyrmex purpureus

Ants use multiple cues for navigating to a food source or nest location. Directional information is derived from pheromone trails or visual landmarks or celestial objects. Some ants use the celestial compass information along with an ‘odometer’ to determine the shortest distance home, a strategy known as path integration. Some trail-following ants utilise visual landmark information whereas few of the solitary-foraging ants rely on both path integration and visual landmark information. However, it is unknown to what degree trail-following ants use path integration and we investigated this in a trunk-trail-following ant, Iridomyrmex purpureus. Trunk-trail ants connect their nests to food sites with pheromone trails that contain long-lasting orientation information. We determined the use of visual landmarks and the ability to path integrate in a trunk-trail forming ant. We found that experienced animals switch to relying on visual landmark information, and naïve individuals rely on odour trails. Ants displaced to unfamiliar locations relied on path integration, but, surprisingly, they did not travel the entire homebound distance. We found that as the homebound distance increased, the distance ants travelled relying on the path integrator reduced.

Place field expansion after focal MEC inactivations is consistent with loss of Fourier components and path integrator gain reduction

Both hippocampal place fields and medial entorhinal cortex (MEC) grid fields increase in scale along the dorsoventral axis. Because the connections from MEC to hippocampus are topographically organized and divergent, it has been hypothesized that place fields are generated by a Fourier-like summation of inputs over a range of spatial scales. This hypothesis predicts that inactivation of dorsal MEC should cause place field expansion, whereas inactivation of ventral MEC should cause field contraction. Inactivation of dorsal MEC caused substantial expansion of place fields; however, as inactivations were made more ventrally, the effect diminished but never switched to contraction. Expansion was accompanied by proportional decreases in theta power, intrinsic oscillation frequencies, phase precession slopes, and firing rates. Our results are most consistent with the predicted loss of specific Fourier components coupled with a path integration gain reduction, which raises the overall place field scale and masks the contraction expected from ventral inactivations.