Role of the cervico-ocular reflex in the "flying" pigeon: interactions with the optokinetic reflex

We studied the cervico-ocular reflex (COR) alone and in combination with the optokinetic (OKN) reflex in head-fixed pigeons. We analyzed these responses in two behavioral conditions: (1) animals were hung in a harness ("resting" condition); and (2) animals were additionally submitted to a frontal airflow that provoked a flight posture ("flying" condition). In both conditions, cervical stimulation provoked a slow phase of very low gain (around 0.05) in the opposite direction to that of the stimulation and fast phases triggered near the head-body alignment in the same direction as the stimulation. The slow phase showed a phase lag of 20 deg at 0.5 Hz. The gain of the slow phase was not modified by the velocity, amplitude, or frequency of the stimuli. This gain was not changed by the presence of a fixed visual surround. When cervical stimuli (0.05-0.5 Hz) were added to an optokinetic stimulation (30 deg/s) in the "resting" condition, the slow phase velocity (SPV) of the optokinetic reflex was modulated with a time course close to that produced by the cervico-ocular reflex alone. The SPV was alternately increased and decreased round the SPV level corresponding to the steady-state OKN. In the "flying" condition, optokinetic-cervical stimulation provoked an eye beating field and a strong SPV modulation synchronized with the position of the cervical stimulation. The number of nystagmic beats (OKN) and the amplitude and velocity of the fast phases were modulated in correlation with the SPV. Consequently, the optokinetic response was increased or decreased according to whether the cervical stimuli were in the reverse direction or in the same direction as the optokinetic stimulation, respectively. These data are interpreted as an improvement of gaze stabilization by the COR. This mechanism is context dependent, since it is strongly reinforced during the flight.