Orienting-related eye-neck neurons of the medial ponto-bulbar reticular formation do not participate in horizontal canal-dependent vestibular reflexes of alert cats.

Ponto-bulbar reticular formation neurons, including identified reticulospinal neurons, were studied in alert, head-fixed cats. Orienting-related neurons of "eye-neck" type (ENNs) were selected on the basis of qualitative correlations of their discharges with visually triggered eye saccades and electromyographic activity (EMG) of dorsal neck muscles. It was tested whether ENNs participate both in visually triggered gaze shifts requiring eye-head coordination and in gaze-stabilizing movements, such as vestibulo-ocular and vestibulo-collic reflexes (VOR, VCR). Firing patterns were studied during passive sinusoidal rotation (0.2-1.0 Hz; 2.0-21.5 deg peak-to-peak) in the horizontal plane. Responses to electrical stimulation of the superior colliculus and the vestibular nerve were recorded to assess the convergence of tectal and vestibular synaptic inputs. The same methods were applied to a control sample of neurons with discharges apparently "unrelated" to orienting movements. ENNs did not show any modulation of firing rate correlated to compensatory VOR or VCR during passive sinusoidal rotations. Among "unrelated" cells, the fraction of modulated units was close to that reported for reticular neurons projecting in the medial reticulospinal tract. Phasic and sustained components of ENN bursts were associated with anticompensatory movements induced by rotation, such as quick phases, ocular beating field shift, and the increase of EMG activity in neck muscles acting in the direction of passive rotation. Monosynaptic excitation from the contralateral superior colliculus was observed in 92.3% of ENNs, but only 2 out of 17 tested showed an excitatory response to vestibular nerve stimulation. In the control group of "unrelated" neurons the proportions of monosynaptic tectal and excitatory vestibular nerve inputs were, respectively, 75.6 and 71.4%. It is concluded that ENNs are specifically related to active gaze shifts, derived from either visual or from head velocity inputs. Rhombencephalic connections of vestibular nuclei to these neurons appear to be quite weak. Parallel inputs from the mid- or forebrain must be assumed to explain their firing patterns during rotation-induced anticompensatory gaze shifts. Within the studied range of frequencies and amplitudes of passive rotation, ENNs did not participate in the vestibulo-collic reflex. It is therefore unlikely that reticular neurons controlling orienting eye-neck synergies act also as a premotor pathway for gaze-stabilizing movements.