Corrigendum: NEURONAL MECHANISMS UNDERLYING THE INTERACTION BETWEEN VISUAL LANDMARKS AND PATH INTEGRATION IN THE RAT

Place- and direction-specific firing properties of hippocampal and thalamic neurons are not strongly tied to visual landmarks when a rat is disoriented. These results suggest that rats rely more on path integration mechanisms than on landmarks, until they have learned that the landmarks are stable directional references.

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Path integration and visual landmarks: Optimal combination or multiple systems?

PsycEXTRA Dataset ◽

10.1037/e520592012-897 ◽

2010 ◽

Cited By ~ 2

Author(s):

Mintao Zhao ◽

William H. Warren

Keyword(s):

Path Integration ◽

Optimal Combination ◽

Visual Landmarks ◽

Multiple Systems

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Rotation of Water in the Morris Water Maze Interferes with Path Integration Mechanisms of Place Navigation

Neurobiology of Learning and Memory ◽

10.1006/nlme.1997.3800 ◽

1997 ◽

Vol 68 (3) ◽

pp. 239-251 ◽

Cited By ~ 13

Author(s):

Mojdeh Moghaddam ◽

Jan Bures

Keyword(s):

Morris Water Maze ◽

Path Integration ◽

Water Maze ◽

Place Navigation ◽

Integration Mechanisms

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Recalibration of path integration in hippocampal place cells

10.1101/319269 ◽

2018 ◽

Cited By ~ 1

Author(s):

Ravikrishnan P. Jayakumar ◽

Manu S. Madhav ◽

Francesco Savelli ◽

Hugh T. Blair ◽

Noah J. Cowan ◽

...

Keyword(s):

Path Integration ◽

Gain Factor ◽

Place Cells ◽

Cognitive Map ◽

Mammalian Brain ◽

Positional Error ◽

Visual Landmarks ◽

Augmented Reality System ◽

Behavioral Evidence ◽

Integration Gain

SummaryHippocampal place cells are spatially tuned neurons that serve as elements of a “cognitive map” in the mammalian brain1. To detect the animal’s location, place cells are thought to rely upon two interacting mechanisms: sensing the animal’s position relative to familiar landmarks2,3 and measuring the distance and direction that the animal has travelled from previously occupied locations4–7. The latter mechanism, known as path integration, requires a finely tuned gain factor that relates the animal’s self-movement to the updating of position on the internal cognitive map, with external landmarks necessary to correct positional error that eventually accumulates8,9. Path-integration-based models of hippocampal place cells and entorhinal grid cells treat the path integration gain as a constant9–14, but behavioral evidence in humans suggests that the gain is modifiable15. Here we show physiological evidence from hippocampal place cells that the path integration gain is indeed a highly plastic variable that can be altered by persistent conflict between self-motion cues and feedback from external landmarks. In a novel, augmented reality system, visual landmarks were moved in proportion to the animal’s movement on a circular track, creating continuous conflict with path integration. Sustained exposure to this cue conflict resulted in predictable and prolonged recalibration of the path integration gain, as estimated from the place cells after the landmarks were extinguished. We propose that this rapid plasticity keeps the positional update in register with the animal’s movement in the external world over behavioral timescales (mean 50 laps over 35 minutes). These results also demonstrate that visual landmarks not only provide a signal to correct cumulative error in the path integration system, as has been previously shown4,8,16–19, but also rapidly fine-tune the integration computation itself.

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The irregular firing properties of thalamic head direction cells mediate turn-specific modulation of the directional tuning curve

Journal of Neurophysiology ◽

10.1152/jn.00583.2013 ◽

2014 ◽

Vol 112 (9) ◽

pp. 2316-2331 ◽

Cited By ~ 7

Author(s):

Marian Tsanov ◽

Ehsan Chah ◽

Muhammad S. Noor ◽

Catriona Egan ◽

Richard B. Reilly ◽

...

Keyword(s):

High Voltage ◽

Tuning Curve ◽

Current Injection ◽

Head Direction ◽

Separation Angle ◽

Head Direction Cells ◽

Thalamic Neurons ◽

Directional Information ◽

Sinusoidal Current ◽

Firing Properties

Head direction cells encode an animal's heading in the horizontal plane. However, it is not clear why the directionality of a cell's mean firing rate differs for clockwise, compared with counterclockwise, head turns (this difference is known as the “separation angle”) in anterior thalamus. Here we investigated in freely behaving rats whether intrinsic neuronal firing properties are linked to this phenomenon. We found a positive correlation between the separation angle and the spiking variability of thalamic head direction cells. To test whether this link is driven by hyperpolarization-inducing currents, we investigated the effect of thalamic reticular inhibition during high-voltage spindles on directional spiking. While the selective directional firing of thalamic neurons was preserved, we found no evidence for entrainment of thalamic head direction cells by high-voltage spindle oscillations. We then examined the role of depolarization-inducing currents in the formation of separation angle. Using a single-compartment Hodgkin-Huxley model, we show that modeled neurons fire with higher frequencies during the ascending phase of sinusoidal current injection (mimicking the head direction tuning curve) when simulated with higher high-threshold calcium channel conductance. These findings demonstrate that the turn-specific encoding of directional signal strongly depends on the ability of thalamic neurons to fire irregularly in response to sinusoidal excitatory activation. Another crucial factor for inducing phase lead to sinusoidal current injection was the presence of spike-frequency adaptation current in the modeled neurons. Our data support a model in which intrinsic biophysical properties of thalamic neurons mediate the physiological encoding of directional information.

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

Australian Journal of Zoology ◽

10.1071/zo16046 ◽

2016 ◽

Vol 64 (3) ◽

pp. 227 ◽

Cited By ~ 9

Author(s):

Ashley Card ◽

Caitlin McDermott ◽

Ajay Narendra

Keyword(s):

Path Integration ◽

Trail Following ◽

Visual Landmarks ◽

Directional Information ◽

Nest Location ◽

Visual Landmark ◽

Pheromone Trails ◽

Orientation Cues ◽

Celestial Compass ◽

Path Integrator

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.

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Path integration in mammals and its interaction with visual landmarks.

Journal of Experimental Biology ◽

10.1242/jeb.199.1.201 ◽

1996 ◽

Vol 199 (1) ◽

pp. 201-209 ◽

Cited By ~ 5

Author(s):

A S Etienne ◽

R Maurer ◽

V Séguinot

Keyword(s):

Path Integration ◽

Visual Cues ◽

Dead Reckoning ◽

Visual Landmarks ◽

Integration System ◽

External Cues ◽

Rapid Accumulation ◽

Types Of Information ◽

Point Of Departure ◽

Inertial Cues

During locomotion, mammals update their position with respect to a fixed point of reference, such as their point of departure, by processing inertial cues, proprioceptive feedback and stored motor commands generated during locomotion. This so-called path integration system (dead reckoning) allows the animal to return to its home, or to a familiar feeding place, even when external cues are absent or novel. However, without the use of external cues, the path integration process leads to rapid accumulation of errors involving both the direction and distance of the goal. Therefore, even nocturnal species such as hamsters and mice rely more on previously learned visual references than on the path integration system when the two types of information are in conflict. Recent studies investigate the extent to which path integration and familiar visual cues cooperate to optimize the navigational performance.

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Interactions Between Idiothetic Cues and External Landmarks in the Control of Place Cells and Head Direction Cells

Journal of Neurophysiology ◽

10.1152/jn.1998.80.1.425 ◽

1998 ◽

Vol 80 (1) ◽

pp. 425-446 ◽

Cited By ~ 178

Author(s):

James J. Knierim ◽

Hemant S. Kudrimoti ◽

Bruce L. McNaughton

Keyword(s):

Visual Cues ◽

Place Cells ◽

Exact Nature ◽

Head Direction ◽

Sources Of Information ◽

Visual Landmarks ◽

Head Direction Cells ◽

Directional Information ◽

Idiothetic Cues ◽

Firing Properties

Knierim, James J., Hemant S. Kudrimoti, and Bruce L. McNaughton. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80: 425–446, 1998. Two types of neurons in the rat brain have been proposed to participate in spatial learning and navigation: place cells, which fire selectively in specific locations of an environment and which may constitute key elements of cognitive maps, and head direction cells, which fire selectively when the rat's head is pointed in a specific direction and which may serve as an internal compass to orient the cognitive map. The spatially and directionally selective properties of these cells arise from a complex interaction between input from external landmarks and from idiothetic cues; however, the exact nature of this interaction is poorly understood. To address this issue, directional information from visual landmarks was placed in direct conflict with directional information from idiothetic cues. When the mismatch between the two sources of information was small (45°), the visual landmarks had robust control over the firing properties of place cells; when the mismatch was larger, however, the firing fields of the place cells were altered radically, and the hippocampus formed a new representation of the environment. Similarly, the visual cues had control over the firing properties of head direction cells when the mismatch was small (45°), but the idiothetic input usually predominated over the visual landmarks when the mismatch was larger. Under some conditions, when the visual landmarks predominated after a large mismatch, there was always a delay before the visual cues exerted their control over head direction cells. These results support recent models proposing that prewired intrinsic connections enable idiothetic cues to serve as the primary drive on place cells and head direction cells, whereas modifiable extrinsic connections mediate a learned, secondary influence of visual landmarks.

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