Path integration: how the head direction signal maintains and corrects spatial orientation

Valério, Stéphane; Taube, Jeffrey S.

doi:10.1038/nn.3215

Cited by 127 publications

(105 citation statements)

References 51 publications

(59 reference statements)

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“…Although we did not combine all of our experimental techniques into a single unified experiment (due to the technical difficulty of simultaneously implementing electrophysiology, optogenetics, and trained navigational behavior), this study provides additional evidence of a causal relationship between HD cell firing and behavior. This additional evidence critically supplements and expands upon previous studies that have found correlational evidence of this relationship [11][12][13][14][15]. Specifically, this study is the first one to directly and selectively manipulate HD cell firing and subsequently show that this manipulation has a significant effect on behavioral performance.…”

Section: Discussionsupporting

confidence: 74%

“…The results from these studies have been mixed; different studies have shown either correlation or lack of correlation between HD cells and spatial responding depending on the behavior being tested [11,12,13]. More recently, two studies have had success demonstrating a significant correlation between HD cells and navigation in the form of homing behavior [14,15]. However, one limitation of these experiments is that they did not manipulate neural circuits in a way that would allow them to conclude that there is a causal relationship between HD cell firing and navigation.…”

Section: Discussionmentioning

confidence: 99%

“…However, attempts to relate the firing of these cells to behavior have yielded mixed results depending on the type of spatial task used [11,12,13]. The most convincing evidence that HD cells may provide a directional signal for guiding behavior has come from recording studies using a path integration task, which found that HD cell tuning strongly correlates with the direction of animals' behavioral choices in two variations of a homing task [14,15]. Correlations between place cell firing and spatial behavior, especially in relation to goaldriven behavior [16], have prompted recent work showing that there is a causal link between place cells and an animal's sense of location [17].…”

Section: Introductionmentioning

confidence: 99%

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The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Butler¹,

Smith²,

Meer³

et al. 2017

Current Biology

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SUMMARYThe rat limbic system contains head direction (HD) cells that fire according to heading in the horizontal plane, and these cells are thought to provide animals with an internal compass. Previous work has found that HD cell tuning correlates with behavior on navigational tasks, but a direct, causal link between HD cells and navigation has not been demonstrated. Here, we show that pathway-specific optogenetic inhibition of the nucleus prepositus caused HD cells to become directionally unstable under dark conditions without affecting the animals' locomotion. Then, using the same technique, we found that this decoupling of the HD signal in the absence of visual cues caused the animals to make directional homing errors, and that the magnitude and direction of these errors were in a range that corresponded to the degree of instability observed in the HD signal. These results provide evidence that the HD signal plays a causal role as a neural compass in navigation.

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Section: Discussionsupporting

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Butler¹,

Smith²,

Meer³

et al. 2017

Current Biology

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“…These results imply a common solution for the interaction of path integration and landmarks in human and animal navigation (Zhao & Warren, 2015). Specifically, visual landmarks reset the path integrator by reorienting the head direction cell system, the grid cell system, and the directional coordinates of the place cell system (Knierim & Hamilton, 2011;Valerio & Taube, 2012;Yoder et al, 2011).…”

Section: Comparison To Animal Navigationmentioning

confidence: 72%

“…Because path integration drifts and error accumulates rapidly (e.g., Loomis et al, 1993), a navigator can take an environmental 'fix' on visual landmarks and re-initialize the path integrator, thereby facilitating reorientation and selflocalization (Etienne & Jeffery, 2004;Etienne, Maurer, Boulens, Levy, & Rowe, 2004;Valerio & Taube, 2012; see also Knierim & Hamilton, 2011). Covertly shifting a visual beacon not only captures an animal's homing behavior, but also induces a corresponding shift in the spatial tuning of underlying neural mechanisms (e.g., place cells, head direction cells, and grid cells; Hafting et al, 2005;Knierim, Kudrimoti, & McNaughton, 1998;Taube et al, 1990).…”

Section: Interaction Between Path Integration and Landmark Navigationmentioning

confidence: 99%

Environmental stability modulates the role of path integration in human navigation

Zhao

Warren

2015

Cognition

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Path integration has long been thought of as an obligatory process that automatically updates one's position and orientation during navigation. This has led to the hypotheses that path integration serves as a back-up system in case landmark navigation fails, and a reference system that detects discrepant landmarks. Three experiments tested these hypotheses in humans, using a homing task with a catch-trial paradigm. Contrary to the back-up system hypothesis, when stable landmarks unexpectedly disappeared on catch trials, participants were completely disoriented, and only then began to rely on path integration in subsequent trials (Experiment 1).Contrary to the reference system hypothesis, when stable landmarks unexpectedly shifted by 115° on catch trials, participants failed to detect the shift and were completely captured by the landmarks (Experiment 2). Conversely, when chronically unstable landmarks unexpectedly remained in place on catch trials, participants failed to notice and continued to navigate by path integration (Experiment 3). In the latter two cases, they gradually sensed the instability (or stability) of landmarks on later catch trials. These results demonstrate that path integration does not automatically serve as a back-up system, and does not function as a reference system on individual sorties, although it may contribute to monitoring environmental stability over time. Rather than being automatic, the roles of path integration and landmark navigation are thus dynamically modulated by the environmental context.

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Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus

2021

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Specialized circuitry in the brain processes spatial information to provide a sense of direction used for navigation. The dorsal tegmental nucleus (DTN) is a core component of this circuitry and utilizes vestibular inputs to generate neural activity encoding the animal's directional heading. Projections arising from the nucleus prepositus hypoglossi (NPH) and the medial vestibular nucleus (MVe) are thought to transmit critical vestibular signals to the DTN and other brain areas, including the abducens nucleus (ABN), a component of eye movement circuitry. Here, we utilized a dual retrograde tracer approach in rats to investigate whether overlapping or distinct populations of neurons project from the NPH or MVe to the DTN and ABN. We report that individual MVe neurons project to both the DTN and ABN. In contrast, we observed individual NPH neurons that project to either the DTN or ABN, but rarely to both structures simultaneously. We also examined labeling patterns in other structures located in the brainstem and posterior cortex and observed (1) complex patterns of interhemispheric connectivity between the left and right DTN, (2) projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN, (3) projections from the lateral superior olive to the ABN, and (4) a unique population of cerebrospinal fluid‐contacting neurons in the dorsal raphe nucleus. Collectively, our experiments provide valuable new information that extends our understanding of the anatomical organization of the brain's spatial processing circuitry.

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Path integration: how the head direction signal maintains and corrects spatial orientation

Cited by 127 publications

References 51 publications

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Environmental stability modulates the role of path integration in human navigation

Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus

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