Stabilizing gaze reflexes in the pigeon (Columba livia). II. Vestibulo-ocular (VOR) and vestibulo-collic (closed-loop VCR) reflexes

Abstract

The vestibulo-ocular reflex (VOR) and the closed-loop vestibulo-collic reflex (CL-VCR) were investigated in the pigeon. The animals, placed either in the fixed-head condition (VOR) or in the free-head condition (CL-VCR) were rotated in darkness (vestibular responses) or in the presence of visual surroundings (visuo-vestibular responses). The linear range of the reflexes were determined both in the frequency and in the velocity domains. Results show that: 1. Pigeons develop a strong VOR, which presents the same asymmetry observed with the OKN, the gain being higher when the slow-phase occurs in the T-N direction. This asymmetry persists in the light (VOR + OKN). In the free-head condition, both the eye and the head display a synchronized nystagmus whose effects are additive. The head reflex (CL-VCR) contributes about 80% of the gaze stabilization. 2. In the medium-low frequency range, the head response (CL-VCR) has a lower gain than the VOR (head-fixed), but the gain of both reflexes increases with frequency, up to about 1 at 0.6-1 Hz. The gaze response (eye + head) presents an optimal gain above 0.06 Hz. The phase lead is higher for the VOR than for the CL-VCR (40 degrees and 32 degrees respectively at 0.03 Hz), but both phases also become nul around 1 Hz. The time constants are 6.5 s for the VOR, 8.5 s for the CL-VCR and 9.6 s for the gaze response (VOR + CL-VCR). 3. While the VOR gain shows a saturation at peak stimulation velocities (PV) higher than 20 degrees/s (at 0.3 Hz), the CL-VCR gain is linear at least up to 60 degrees/s (the highest PV used). However, the phase lead declines when the PV is greater than 20 degrees/s, both for the VOR and the CL-VCR. 4. When the vestibular stimulation is delivered in the light (visuo-vestibular stimulation), there is no phase shift. The VOR gain (fixed-head) is optimal and linear over the entire frequency range, but it saturates for PV higher than 40 degrees/s. In the free-head condition, while the gaze gain is linear and close to 1 in both the frequency and the velocity domains, the head response gain (CL-VCR) remains lower especially in the low frequency and in the low velocity ranges.