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Spatial navigation. Disruption of the head direction cell network impairs the parahippocampal grid cell signal.

ABSTRACT: Navigation depends on multiple neural systems that encode the moment-to-moment changes in an animal's direction and location in space. These include head direction (HD) cells representing the orientation of the head and grid cells that fire at multiple locations, forming a repeating hexagonal grid pattern. Computational models hypothesize that generation of the grid cell signal relies upon HD information that ascends to the hippocampal network via the anterior thalamic nuclei (ATN). We inactivated or lesioned the ATN and subsequently recorded single units in the entorhinal cortex and parasubiculum. ATN manipulation significantly disrupted grid and HD cell characteristics while sparing theta rhythmicity in these regions. These results indicate that the HD signal via the ATN is necessary for the generation and function of grid cell activity.

SUBMITTER: Winter SS

PROVIDER: S-EPMC4476794 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Spatial navigation. Disruption of the head direction cell network impairs the parahippocampal grid cell signal.

Winter Shawn S SS Clark Benjamin J BJ Taube Jeffrey S JS

Science (New York, N.Y.) 20150205 6224

Navigation depends on multiple neural systems that encode the moment-to-moment changes in an animal's direction and location in space. These include head direction (HD) cells representing the orientation of the head and grid cells that fire at multiple locations, forming a repeating hexagonal grid pattern. Computational models hypothesize that generation of the grid cell signal relies upon HD information that ascends to the hippocampal network via the anterior thalamic nuclei (ATN). We inactivat ...[more]

PMID: 25700518

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The head-direction signal is critical for navigation requiring a cognitive map but not for learning a spatial habit.

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Project description:Head-direction cells have frequently been regarded as an internal 'compass' that can be used for navigation, although there is little evidence showing a link between their activity and spatial behavior. In a navigational task requiring the use of internal cues to return to a home location without vision (path integration), we found a robust correlation between head-direction cell activity and the rat's heading error in the rat's homing behavior. We observed two different correction processes that rats used to improve performance after an error. The more frequent one consists of 'resetting' the cell whenever the rat returns to the home location. However, we found that when large errors occur, the head-direction system has the ability to 'remap' and set a new reference frame, which is then used in subsequent trials. We also offer some insight into how these two correction processes operate when rats make an error.

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Project description:Head direction (HD) cells in the rat anterodorsal thalamic nucleus (ADN) fire relative to the animal's directional heading. Lesions of the entire vestibular labyrinth have been shown to severely alter VIIIth nerve input and disrupt these HD signals. To assess the specific contributions of the semicircular canals without altering tonic VIIIth nerve input, ADN cells were recorded from chinchillas after bilateral semicircular canal occlusion. Although ADN HD cells (and also hippocampal place cells and theta cells) were identified in intact chinchillas, no direction-specific activity was seen after canal occlusions. Instead, "bursty" cells were observed that exhibited burst-firing patterns similar to normal HD cells but with firing unrelated to the animal's actual head direction. Importantly, when pairs of bursty cells were recorded, the temporal order of their firing was dependent on the animal's turning direction, as is the case for pairs of normal HD cells. These results suggest that bursty cells are actually disrupted HD cells. The present findings further suggest that the HD cell network is still able to generate spiking activity after canal occlusions, but the semicircular canal input is critical for updating the network activity in register with changes in the animal's HD.

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Direct recordings of grid-like neuronal activity in human spatial navigation.

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Non-rhythmic head-direction cells in the parahippocampal region are not constrained by attractor network dynamics.

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Project description:Navigation is usually thought of relative to landmarks, but neural signals representing space also use information generated by an animal's movements. These signals include grid cells, which fire at multiple locations, forming a repeating grid pattern. Grid cell generation depends upon theta rhythm, a 6-10 Hz electroencephalogram (EEG) oscillation that is modulated by the animals' movement velocity. We passively moved rats in a clear cart to eliminate motor related self-movement cues that drive moment-to-moment changes in theta rhythmicity. We found that passive movement maintained theta power and frequency at levels equivalent to low active movement velocity, spared overall head-direction (HD) cell characteristics, but abolished both velocity modulation of theta rhythmicity and grid cell firing patterns. These results indicate that self-movement motor cues are necessary for generating grid-specific firing patterns, possibly by driving velocity modulation of theta rhythmicity, which may be used as a speed signal to generate the repeating pattern of grid cells.

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