Flexible cue anchoring strategies enable stable head direction coding in both sighted and blind animals

Abstract

Vision plays a crucial role in instructing the brains spatial navigation systems. However, little is known about how vision loss affects the neuronal encoding of spatial information. Here, recording from head direction (HD) cells in the anterior dorsal nucleus of the thalamus in mice, we find stable and robust HD tuning in blind animals. In contrast, placing sighted animals in darkness significantly impairs HD cell tuning. We find that blind mice use olfactory cues to maintain stable HD tuning and that prior visual experience leads to refined HD cell tuning in blind adult mice compared to congenitally blind animals. Finally, in the absence of both visual and olfactory cues, the HD attractor network remains intact but the preferred firing direction of HD cells continuously drifts over time. We thus demonstrate remarkable flexibility in how the brain uses diverse sensory information to generate a stable directional representation of space. HighlightsO_LIHead direction (HD) cell tuning in ADn is robust in blind animals, but unstable in sighted animals placed in the dark C_LIO_LIBlind mice use olfaction to stabilize HD cell tuning C_LIO_LIPrior visual experience leads to refined HD cell tuning in blind adult mice C_LIO_LIIn the absence of both vision and olfaction, the HD attractor network in ADn remains intact but the preferred firing direction of HD cells continuously drifts C_LI