Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I: Behavioral properties

The activity of 24 reticulo-spinal neurons (RSN) identified by antidromic stimulation at the C1-C2 level has been recorded intra-axonally in the pons of alert head-fixed cats during spontaneous gaze shifts and orienting towards novel targets. Relationship of neuronal discharge to saccadic eye movements, positions of fixation and EMG of dorsal neck muscles were analysed. The present report describes behavioral properties of a group of 14 RSN showing similar types of correlations with motor parameters during eye-head synergies. These "eye-neck" RSN (EN-RSN) generate bursts in synchrony with phasic components of ipsilateral neck EMG and leading ipsiversive saccades by a variable lead time. Bursts are followed by a prolonged discharge whose frequency decays even when eccentric eye position is maintained constant and accompanied by sustained neck muscle activity. The firing rate of EN-RSNs depends on eye position: they are silent with saccades in their ON-direction when the eyes are deviated towards the contralateral half of the oculomotor range and the ipsilateral neck muscles are relaxed. When the eyes cross the vertical meridian, the frequency of phasic and tonic components related to eye-head synergies increase proportionally to ipsilateral eye position. Ten of the 14 EN-RSNs, located in the pontine reticular formation, received monosynaptic input from the contralateral superior colliculus. Two were labeled by intra-axonal injection of HRP which revealed extensive branching in the abducens, facial, medial and lateral vestibular, prepositus and intercalatus nuclei and in the caudal pontine and bulbar reticular formation. It is concluded that the caudal pontine tegmentum, including the region just anterior to the abducens nucleus, contains RSNs whose signals seem appropriate to control phasic neck muscle activity and which also project to structures related to ocular and facial movements. Comparisons with the perisaccadic activity of tectal neurons projecting in the predorsal bundle reveals a profound transformation of the descending signal at the level of EN-RSNs which represent first order relay neurons of the tecto-reticulo-spinal pathway.