The dorsal thalamic lateral geniculate nucleus is required for visual control of head direction cell firing direction in rats

Abstract

Head direction (HD) neurons, signalling facing direction, generate a signal that is primarily anchored to the outside world by visual inputs. We investigated the route for visual landmark information into the HD system in rats. There are two candidates: an evolutionarily older, larger subcortical (retino-tectal) pathway specialised for coarse vision, and a smaller cortical (retino-geniculo-striate) pathway for higher acuity vision. We disrupted the cortical pathway by lesioning the dorsal lateral geniculate (dLGN) thalamic nuclei bilaterally, and recorded HD cells in postsubicular (PoS) cortex as rats foraged in a visual-cue-controlled enclosure. In dLGN-lesioned rats we found the expected number of PoS HD cells. Although directional tuning curves were broader across a trial, this was due to increased instability of otherwise normal-width tuning curves. Tuning curves were also poorly responsive to polarizing visual landmarks, and did not distinguish cues based on their visual pattern. Thus, the retino-geniculo-striate pathway is not critical for generation of an underlying, tightly-tuned directional signal, but does provide the main route for vision-based anchoring of the signal to the outside world, even when visual cues are high-contrast and low in detail. Key pointsO_LIHead direction (HD) cells indicate the facing direction of the head, using visual landmarks to distinguish directions C_LIO_LIIn rats, we investigated whether this visual information is routed through the thalamus to visual cortex or arrives via the superior colliculus: a phylogenetically older and (in rodents) larger pathway, but not known for pattern vision. C_LIO_LIWe lesioned the thalamic dorsal lateral geniculate nucleus (dLGN) in rats and recorded the responsiveness of cortical HD cells to visual cues. C_LIO_LIWe found that cortical HD cells had normal tuning curves but these were slightly more unstable during a trial. Most notably, HD cells in dLGN-lesioned animals showed little ability to distinguish highly distinct cues and none to distinguish more similar cues. C_LIO_LIThese results suggest that directional processing of visual landmarks in mammals requires the geniculo-cortical pathway, which raises questions about when and how visual directional landmark processing appeared during evolution. C_LI