Head-direction coding in the hippocampal formation of birds

Abstract

Birds strongly rely on spatial memory and navigation. Therefore, it is of utmost interest to reveal how space is represented in the avian brain. Here we used tetrodes to record neurons from the hippocampal formation of Japanese quails – a ground-dwelling species – while the quails roamed a 1×1-meter arena (>2,100 neurons from 23 birds). Whereas spatially-modulated cells (place-cells, border-cells, etc.) were generally not encountered, the firing-rate of 12% of the neurons was unimodally and significantly modulated by the head-azimuth – i.e. these were head-direction cells (HD cells). Typically, HD cells were maximally active at one preferred-direction and minimally at the opposite null-direction, with preferred-directions spanning all 360°. The HD tuning was relatively broad (mean width ∼130°), independent of the animal’s position and speed, and was stable during the recording-session. Similarly to findings in rodents, the HD tuning usually rotated with the rotation of a salient visual cue in the arena. These findings support the existence of an allocentric head-direction representation in the quail hippocampal formation, and provide the first demonstration of head-direction cells in birds.