Functions of the nucleus of the optic tract (NOT). II. Control of ocular pursuit

Abstract

Ocular pursuit in monkeys, elicited by sinusoidal and triangular (constant velocity) stimuli, was studied before and after lesions of the nucleus of the optic tract (NOT). Before NOT lesions, pursuit gains (eye velocity/target velocity) were close to unity for sinusoidal and constant-velocity stimuli at frequencies up to 1 Hz. In this range, retinal slip was less than 2 degrees. Electrode tracks made to identify the location of NOT caused deficits in ipsilateral pursuit, which later recovered. Small electrolytic lesions of NOT reduced ipsilateral pursuit gains to below 0.5 in all tested conditions. Pursuit was better, however, when the eyes moved from the contralateral side toward the center (centripetal pursuit) than from the center ipsilaterally (centrifugal pursuit), although the eyes remained in close proximity to the target with saccadic tracking. Effects of lesions on ipsilateral pursuit were not permanent, and pursuit gains had generally recovered to 60-80% of baseline after about 2 weeks. One animal had bilateral NOT lesions and lost pursuit for 4 days. Thereafter, it had a centrifugal pursuit deficit that lasted for more than 2 months. Vertical pursuit and visually guided saccades were not affected by the bilateral NOT lesions in this animal. We also compared effects of these and similar NOT lesions on optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN). Correlation of functional deficits with NOT lesions from this and previous studies showed that rostral lesions of NOT in and around the pretectal olivary nucleus, which interrupted cortical input through the brachium of the superior colliculus (BSC), affected both smooth pursuit and OKN. In two animals in which it was tested, NOT lesions that caused a deficit in pursuit also decreased the rapid and slow components of OKN slow-phase velocity and affected OKAN. It was previously shown that slightly more caudal NOT lesions were more effective in altering gain adaptation of the angular vestibulo-ocular reflex (aVOR). The present findings suggest that cortical pathways through rostral NOT play an important role in maintenance of ipsilateral ocular pursuit. Since lesions that affected ocular pursuit had similar effects on ipsilateral OKN, processing for these two functions is probably closely linked in NOT, as it is elsewhere.

Fig. 1

Samples of sinusoidal (A, C) and constant-velocity (B, C) ocular pursuit obtained before (A, B) and after (C, D) unilateral lesion of the nucleus of the optic tract (NOT) in monkey M9121. Target and eye position are overlaid in the top row of each panel, and eye and target velocity are shown superimposed in the third traces. Retinal error (degrees, 2^nd trace), retinal-slip velocity (°/s, 3^rd trace), and instantaneous gain (5^th trace) are also shown. Time (s) is on the abscissa. There was an increase in saccadic tracking when the eyes moved ipsilateral to the lesion (C, D). Note also that the drop in gain was maximal as the eye moved to the contralateral side for both sinusoidal (C) and smooth (D) pursuit

Fig. 2A–L

Gain of sinusoidal smooth pursuit in monkey M9121 before and after first and second lesions in the left nucleus of the optic tract (NOT). Unity gain is shown by the dashed lines. Open circles represent gains before lesion, while filled symbols represent gains at various times after lesions (see inserts in D and G for specific times). The ipsilateral gain was reduced in the first days after lesion and then recovered. There was no effect on the contralateral pursuit gain. Changes in pursuit after the second lesion were the same as after the first lesion. Vmax Maximum target velocity

Fig. 3A–F

Gain of ipsilateral smooth pursuit during constant velocity (triangular) tracking in monkey M9121 before and after first and second lesions in the left nucleus of the optic tract (NOT). Effects were similar to those observed during sinusoidal pursuit. Vmax Maximum target velocity

Fig. 4

Gain of sinusoidal smooth pursuit in monkeys M9121 (A–F) and M8916 (G–L) before and after one nucleus of the optic tract (NOT) had been penetrated with a microelectrode. Deficits in pursuit were to the side ipsilateral to the penetrations. The effects observed in the first several days were compatible with the effects of unilateral NOT lesions. Vmax Maximum target velocity

Fig. 5

Samples of sinusoidal (A) and constant-velocity (B) ocular pursuit obtained after bilateral lesions of the nuclei of the optic tract in monkey M9314. The schema is similar to that shown in Fig. 1. Note that pursuit away from the midline (centrifugal pursuit) was saccadic after lesion, while pursuit toward the midline (centripetal pursuit) was intact

Fig. 6

Gain of centrifugal sinusoidal (A–F) and constant-velocity (G–L) smooth pursuit before and after bilateral lesions of the nuclei of the optic tract in monkey M9314. Open circles represent gains before lesions, while filled symbols represent gains at various times after lesions (see insert in C for specific times). Pursuit to the left was more affected and the deficit was still present 2 months after the lesions (filled diamonds). The deficits were more pronounced at higher velocities, and the animal was unable to follow targets moving at 40°/s constant velocity as long as 2 months after the lesions. Vmax Maximum target velocity

Fig. 7

Vertical smooth pursuit before (A) and 6 days after (B) bilateral lesions of the nuclei of the optic tract (NOT) in monkey M9314. Target position and eye position are superimposed in the top trace. The second trace is superimposed eye and target velocity. On average, there was no effect of the NOT lesions on vertical pursuit in either direction (C)

Fig. 8

Effect of unilateral lesions of the nucleus of the optic tract (NOT) in monkey M9121 on optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN) before (A) and on different days after the first (B, C) and second (D–F) left NOT lesions. Only the envelopes of slow-phase velocity are shown. The remnants of the saccades that were removed are represented by dotted lines. Zero velocity is shown by the horizontal dashed line. The stimulus was full-field movement of the visual surround at 60°/s for the period shown by the solid bars under F. OKAN was recorded in darkness. OKN and OKAN to the right were not affected by either lesion (left column). OKN and OKAN to the left (right column) were reduced after the first lesion, but recovered by the 23^rd day after lesion. The effects of the second lesion were more profound, and there was no recovery after 4.5 months. Spontaneous nystagmus to the right was present after both lesions in left NOT. H_eye Vel Horizontal eye velocity

Fig. 9A–D

Diagram of transverse sections through the pretectum. A Filled circles show the extent of the nucleus of the optic tract (NOT) from rostral (left) to caudal (right). B–D Location of lesions that caused changes in smooth pursuit (B), optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN) (C), and adaptive reduction in the gain of the angular vestibulo-ocular reflex (D). The first lesion in monkey M9121 and both lesions in monkey M9314 are shown in B. The second lesion in M9121, the left lesion in M9314, and the lesion in M1169 and M1176 are shown in C. Monkeys M1169 and M1176 are from an earlier study (Schiff et al. 1990) and were not tested for smooth pursuit. The second lesion in monkey M9121, the right lesion in M9314, and the kainic-acid lesion in M9221 are shown in D. Scale in mm shown below D. BSC Brachium of the superior colliculus, DTN dorsal terminal nucleus, LI nucleus limitans, MGN medial geniculate nucleus, NIII oculomotor nucleus, OLN pretectal olivary nucleus, PUL pulvinar, SC superior colliculus