Neuronal circuitry and discharge patterns controlling eye movements in the pigeon

Horizontal eye movements in humans and other vertebrates are actuated by the lateral and medial rectus muscles that are innervated by the abducens and oculomotor nuclei. Here we show by single-cell recording in the pigeon that there exist three types of abducens neurons in terms of discharge patterns, which generate the shift and/or oscillation components of a horizontal saccadic eye movement. Shift-related neurons discharged sustained firing around saccadic shift, oscillation-related neurons produced several bursts accompanying saccadic oscillations, and saccade-related neurons discharged both sustained firing and several bursts perisaccadically. Oscillation- and saccade-related neurons were each divided into two groups according to their firing behaviors during nasotemporal saccades: bursting activity began before (leading) or after (lagging) the onset of saccades. Abducens neurons in the lagging group but not those in the leading group were activated by antidromic stimulation of the contralateral oculomotor nucleus. Blockade of the nucleus lentiformis mesencephali and the nucleus of the basal optic root, both of which are involved in optokinetic nystagmus, abolished sustained firing in abducens neurons and shift component of saccades, whereas blockade of the saccade-related raphe complex eliminated bursting activity in abducens neurons and oscillation component of saccades. The present study revealed oculomotor circuitry in the pigeon, in which the optokinetic nuclei and the raphe complex send differential signals to abducens neurons to generate three types of discharge patterns, and thereby initiate the shift and oscillation components of a horizontal saccade.