Abstract
Environmental information is required to stabilize estimates of head direction (HD) based on angular path integration. However, it is unclear how this happens in real-world (visually complex) environments. We present a computational model of how visual feedback can stabilize HD information in environments that contain multiple cues of varying stability and directional specificity. We show how combinations of feature-specific visual inputs can generate a stable unimodal landmark bearing signal, even in the presence of multiple cues and ambiguous directional specificity. This signal is associated with the retrosplenial HD signal (inherited from thalamic HD cells) and conveys feedback to the subcortical HD circuitry. The model predicts neurons with a unimodal encoding of the egocentric orientation of the array of landmarks, rather than any one particular landmark. The relationship between these abstract landmark bearing neurons and head direction cells is reminiscent of the relationship between place cells and grid cells. Their unimodal encoding is formed from visual inputs via a modified version of Oja's Subspace Algorithm. The rule allows the landmark bearing signal to disconnect from directionally unstable or ephemeral cues, incorporate newly added stable cues, support orientation across many different environments (high memory capacity), and is consistent with recent empirical findings on bidirectional HD firing reported in the retrosplenial cortex. Our account of visual feedback for HD stabilization provides a novel perspective on neural mechanisms of spatial navigation within richer sensory environments, and makes experimentally testable predictions.
Highlights
The global sense of direction is believed to be supported by head direction (HD) cells
We show how visual/sensory feedback may be conveyed from abstract landmark bearing (aLB) cells to HD cells via retrosplenial cortex (RSC), and how the model is coherent with recent empirical findings
Similar multimodal firing profiles of dysgranular RSC (dRSC) cells are found in the simulation with three conflicting environments (S5 Appendix and S7 Fig), replicating a similar simulation result from [30]. These results suggest that the simulated dRSC cells in our model are consistent with the within-compartment BD cells (WC-BD) cells reported by Jacob et al [28], integrating abstract visual information with internal HD signals
Summary
The global sense of direction is believed to be supported by head direction (HD) cells. HD signals were found in other cortical regions, including the medial parietal cortex in humans [5,16], as well as medial prestriate cortex (or visual association cortex) [17] and deep layers of the primary visual cortex (V1) [18]. HD cells are controlled by both external landmarks and self-motion information [19,20,21]. The self-motion information includes angular path integration in the vestibular system, which generates unimodal HD signals even before eye-opening [3,22,23]. Path integration via vestibular inputs can maintain HD in darkness, yet is subject to accumulated path integration error resulting in drift in the absence of sensory reset [24]
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