The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections

Abstract

The activity of tectoreticulospinal neurons (TRSN) during orienting gaze shifts was studied in alert, head-fixed cats by intra-axonal recordings. The scope of the study was to evaluate the role of this class of superior colliculus neurons in the generation of slow eye movements (drifts) which often follow main-sequence saccades and sometimes appear as an independent motor event of orienting. The parameters of such movements are described in the first part of the paper. The organization of underlying pathways in the lower brainstem has been studied by intra-axonal horseradish peroxidase (HRP) tracing. The mean amplitude of postsaccadic drifts (PSD) is 1.21° (SD 0.63), but it can eventually reach 6–8°. PSDs have mean velocity of 14.9°/s (SD 4.28) and mean duration of 104.2 ms (SD 50.8). These two parameters are positively correlated with PSD amplitude. The presence of PSDs is usually associated with an increased neck muscle activity on the side toward which the eyes move. The durations of these two motor events show a reliable positive correlation. PSDs appear to occur when gaze error persists after a saccade and a correction is attempted by means of a slow eye movement and a head turn. The durations of TRSN bursts are, on average, longer than the sum of the lead time and the saccade duration. Bursts associated with combinations of saccades and PSD are significantly longer than those recorded in the absence of PSDs. The probability of occurrence of PSDs is higher when firing of TRSNs continues after saccade termination. Such prolonged discharges usually coincide with a combination of PSDs and phasic activation of the neck electromyogram. The mean firing rate of TRSNs during PSDs is 62% of that during saccade-related portions of the burst and declines to 45% after the end of PSDs. According to its timing and intensity, postsaccadic firing of TRSNs is appropriate as a signal underlying slow, corrective eye movements and later portions of phasic neck muscle contractions during orienting. Intraaxonal HRP labeling showed that visuomotor TRSNs of the X type (n = 3) terminate in the abducens nucleus, with 145–331 boutons terminaux and en passant. Average bouton densities in the nucleus are lower than in the periabducens reticular formation, but higher than in more rostral paramedian pontine reticular formation (PPRF) regions. Terminal fields in the PPRF match the locations of “eye-neck” reticulospinal neurons (RSNs) and exitatory burst neurons. Termination densities comparable with those in the caudal PPRF are found also in the rostral nucleus reticularis gigantocellularis, which contains phasic RSNs (“neck bursters”) and inhibitory burst neurons. Morphological observations alone do not exclude firing rate modulation of abducens motoneurons through the monosynaptic tectal pathway. However, the available physiological data point to a major role of a multiple convergent connection involving the eye-neck RSNs. In conclusion, the signals of X type TRSNs, reinforced by parallel connection through RSNs, encode mainly the intended head movement. Collateral actions of these two populations may be sufficient to induce slow, orienting eye movements, independently of the burst output from the classic saccadic generator.