An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex.
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ABSTRACT:
SUBMITTER: Jacob PY
PROVIDER: S-EPMC5274535 | biostudies-literature | 2017 Feb
REPOSITORIES: biostudies-literature
Publications
An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex.
Jacob Pierre-Yves PY Casali Giulio G Spieser Laure L Page Hector H Overington Dorothy D Jeffery Kate K
Nature neuroscience 20161219 2
We investigated how landmarks influence the brain's computation of head direction and found that in a bidirectionally symmetrical environment, some neurons in dysgranular retrosplenial cortex showed bidirectional firing patterns. This indicates dominance of neural activity by local environmental cues even when these conflicted with the global head direction signal. It suggests a mechanism for associating landmarks to or dissociating them from the head direction signal, according to their directi ...[more]
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Project description:Maintaining a sense of direction is fundamental to navigation, and is achieved in the brain by a network of head direction (HD) cells, which update their signal using stable environmental landmarks. How landmarks are detected and their stability determined is still unknown. Recently we reported a new class of cells (Jacob et al., 2017), the bidirectional cells, in a brain region called retrosplenial cortex (RSC) which relays environmental sensory information to the HD system. A subset of these cells, between-compartment (BC) cells, are directionally tuned (like ordinary HD cells) but follow environmental cues in preference to the global HD signal, resulting in opposing (i.e., bidirectional) tuning curves in opposed environments. Another subset, within-compartment (WC) cells, unexpectedly expressed bidirectional tuning curves in each one of the opposed compartments. Both BC and WC cells lost directional tuning in an open field, unlike HD cells. Two questions arise from this discovery: (i) how do these cells acquire their unusual response properties, and (ii) what are they for? We propose that bidirectional cells reflect a two-way interaction between local direction, as indicated by the visual environment, and global direction as signaled by the HD system. We suggest that BC cells receive strong inputs from visual cues, while WC cells additionally receive modifiable inputs from HD cells which, due to Hebbian coactivation of visual inputs plus two opposing sets of HD inputs, acquire the ability to fire in both directions. A neural network model instantiating this hypothesis is presented, which indeed forms both BC and WC bidirectional cells with properties similar to those seen experimentally. We then demonstrate how tuning specificity degrades when WC/BC cells are exposed to multiple directionalities, replicating the observed loss of WC and BC directional tuning in the open field. We suggest that the function of these neurons is to assess the stability of environmental landmarks, thereby determining their utility as reference points by which to set the HD sense of direction. This role could extend to the ability of the HD system to prefer distal over proximal landmarks, and to correct for parallax errors.
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Project description:BackgroundVisual landmarks are used by head direction (HD) cells to establish and help update the animal's representation of head direction, for use in orientation and navigation. Two cortical regions that are connected to primary visual areas, postsubiculum (PoS) and retrosplenial cortex (RSC), possess HD cells: we investigated whether they differ in how they process visual landmarks.MethodsWe compared PoS and RSC HD cell activity from tetrode-implanted rats exploring an arena in which correct HD orientation required discrimination of two opposing landmarks having high, moderate or low discriminability.ResultsRSC HD cells had higher firing rates than PoS HD cells and slightly lower modulation by angular head velocity, and anticipated actual head direction by ~48 ms, indicating that RSC spiking leads PoS spiking. Otherwise, we saw no differences in landmark processing, in that HD cells in both regions showed equal responsiveness to and discrimination of the cues, with cells in both regions having unipolar directional tuning curves and showing better discrimination of the highly discriminable cues. There was a small spatial component to the signal in some cells, consistent with their role in interacting with the place cell navigation system, and there was also slight modulation by running speed. Neither region showed theta modulation of HD cell spiking.ConclusionsThat the cells can immediately respond to subtle differences in spatial landmarks is consistent with rapid processing of visual snapshots or scenes; similarities in PoS and RSC responding may be due either to similar computations being performed on the visual inputs, or to rapid sharing of information between these regions. More generally, this two-cue HD cell paradigm may be a useful method for testing rapid spontaneous visual discrimination capabilities in other experimental settings.
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Project description:To successfully navigate the environment, animals depend on their ability to continuously track their heading direction and speed. Neurons that encode angular head velocity (AHV) are fundamental to this process, yet the contribution of various motion signals to AHV coding in the cortex remains elusive. By performing chronic single-unit recordings in the retrosplenial cortex (RSP) of the mouse and tracking the activity of individual AHV cells between freely moving and head-restrained conditions, we find that vestibular inputs dominate AHV signaling. Moreover, the addition of visual inputs onto these neurons increases the gain and signal-to-noise ratio of their tuning during active exploration. Psychophysical experiments and neural decoding further reveal that vestibular-visual integration increases the perceptual accuracy of angular self-motion and the fidelity of its representation by RSP ensembles. We conclude that while cortical AHV coding requires vestibular input, where possible, it also uses vision to optimize heading estimation during navigation.
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Project description:The electrophysiological activities of head direction (HD) cells under visual and vestibular input dissociation are important to understanding the formation of the sense of direction in animals. In this paper, we fabricated a PtNPs/PEDOT:PSS-modified MEA to detect changes in the discharge of HD cells under dissociated sensory conditions. The electrode shape was customized for the retrosplenial cortex (RSC) and was conducive to the sequential detection of neurons at different depths in vivo when combined with a microdriver. The recording sites of the electrode were modified with PtNPs/PEDOT:PSS to form a three-dimensional convex structure, leading to closer contact with neurons and improving the detection performance and signal-to-noise ratio of the MEA. We designed a rotating cylindrical arena to separate the visual and vestibular information of the rats and detected the changes in the directional tuning of the HD cells in the RSC. The results showed that after visual and vestibular sensory dissociation, HD cells used visual information to establish newly discharged directions which differed from the original direction. However, with the longer time required to process inconsistent sensory information, the function of the HD system gradually degraded. After recovery, the HD cells reverted to their newly established direction rather than the original direction. The research based on our MEAs revealed how HD cells process dissociated sensory information and contributes to the study of the spatial cognitive navigation mechanism.
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