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

ABSTRACT: The 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.

SUBMITTER: Butler WN

PROVIDER: S-EPMC5425164 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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

Butler William N WN Smith Kyle S KS van der Meer Matthijs A A MAA Taube Jeffrey S JS

Current biology : CB 20170413 9

The 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 und ...[more]

PMID: 28416119

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Project description:Insects and vertebrates harbor specific neurons that encode the animal's head direction (HD) and provide an internal compass for spatial navigation. Each HD cell fires most strongly in one preferred direction. As the animal turns its head, however, HD cells in rat anterodorsal thalamic nucleus (ADN) and other brain areas fire already before their preferred direction is reached, as if the neurons anticipated the future HD. This phenomenon has been explained at a mechanistic level, but a functional interpretation is still missing. To close this gap, we use a computational approach based on the movement statistics of male rats and a simple model for the neural responses within the ADN HD network. Network activity is read out using population vectors in a biologically plausible manner, so that only past spikes are taken into account. We find that anticipatory firing improves the representation of the present HD by reducing the motion-induced temporal bias inherent in causal decoding. The amount of anticipation observed in ADN enhances the precision of the HD compass read-out by up to 40%. More generally, our theoretical framework predicts that neural integration times not only reflect biophysical constraints, but also the statistics of behaviorally relevant stimuli; in particular, anticipatory tuning should be found wherever neurons encode sensory signals that change gradually in time.SIGNIFICANCE STATEMENT Across different brain regions, populations of noisy neurons encode dynamically changing stimuli. Decoding a time-varying stimulus from the population response involves a trade-off: For short read-out times, stimulus estimates are unreliable as the number of stochastic spikes is small; for long read-outs, estimates are biased because they lag behind the true stimulus. We show that optimal decoding of temporally correlated stimuli not only relies on finding the right read-out time window but requires neurons to anticipate future stimulus values. We apply this general framework to the rodent head-direction system and show that the experimentally observed anticipation of future head directions can be explained at a quantitative level from the neuronal tuning properties, network size, and the animal's head-movement statistics.

Dataset Information

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

Publications

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

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