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Smooth pursuitlike eye movements evoked by microstimulation in macaque nucleus reticularis tegmenti pontis
T Yamada1, D A Suzuki, R D Yee
1Department of Ophthalmology, Indiana University School of Medicine, Indianapolis 46202, USA.
Abstract:
1. Smooth pursuitlike eye movements were evoked with low current microstimulation delivered to rostral portions of the nucleus reticularis tegmenti pontis (rNRTP) in alert macaques. Microstimulation sites were selected by the observation of modulations in single-cell firing rates that were correlated with periodic smoothpursuit eye movements. Current intensities ranged from 10 to 120 microA and were routinely < 40 microA. Microstimulation was delivered either in the dark with no fixation, 100 ms after a fixation target was extinguished, or during maintained fixation of a stationary or moving target. Evoked eye movements also were studied under open-loop conditions with the target image stabilized on the retina. 2. Eye movements evoked in the absence of a target rapidly accelerated to a constant velocity that was maintained for the duration of the microstimulation. Evoked eye speeds ranged from 3.7 to 23 deg/s and averaged 11 deg/s. Evoked eye speed appeared to be linearly related to initial eye position with a sensitivity to initial eye position that averaged 0.23 deg.s-1.deg-1. While some horizontal and oblique smooth eye movements were elicited, microstimulation resulted in upward eye movements in 89% of the sites. 3. Evoked eye speed was found to be dependent on microstimulation pulse frequency and current intensity. Within limits, evoked eye speed increased with increases in stimulation frequency or current intensity. For stimulation frequencies < 300-400 Hz, only smooth pursuit-like eye movements were evoked. At higher stimulation frequencies, accompanying saccades consistently were elicited. 4. Feedback of retinal image motion interacted with the evoked eye movements to decrease eye speed if the visual motion was in the opposite direction as the evoked, pursuit-like eye movements. 5. The results implicate rNRTP as part of the neuronal substrate that controls smooth-pursuit eye movements. NRTP appears to be divided functionally into a rostral, pursuit-related portion and a caudal, saccade-related area. rNRTP is a component of a corticopontocerebellar circuit that presumably involves the pursuit area of the frontal eye field and that parallels the middle and medial superior temporal cerebral cortical/dorsalateral pontine nucleus (MT/MST-DLPN-cerebellum) pathway known to be involved also with regulating smooth-pursuit eye movements.
Insights
Researchers stimulated the nucleus reticularis tegmenti pontis (rNRTP) in macaques, evoking smooth pursuit eye movements. This study identifies the rNRTP as crucial for controlling eye movements and suggests functional divisions within the nucleus.
Area of Science:
- Neuroscience
- Ophthalmology
- Systems Neuroscience
Background:
- Smooth pursuit eye movements are essential for visual tracking.
- The neural circuitry underlying smooth pursuit is complex and not fully understood.
- The nucleus reticularis tegmenti pontis (NRTP) is a potential component of this circuitry.
Purpose of the Study:
- To investigate the role of rostral NRTP (rNRTP) in generating smooth pursuit eye movements.
- To determine the effects of microstimulation parameters on evoked eye movements.
- To explore the functional organization of the NRTP.
Main Methods:
- Microstimulation of rNRTP in alert, behaving macaques.
- Recording of evoked eye movements under various visual conditions (dark, fixation, open-loop).
- Analysis of eye speed, direction, and dependence on stimulation parameters (frequency, intensity).
Main Results:
- Low current microstimulation of rNRTP reliably evoked smooth pursuit-like eye movements.
- Evoked eye speed was dependent on stimulation intensity and frequency, and initial eye position.
- Upward eye movements were most commonly elicited (89% of sites).
- Retinal image motion feedback modulated evoked eye speed.
- Higher stimulation frequencies elicited saccades in addition to smooth pursuit.
Conclusions:
- The rNRTP is implicated as a key component of the neuronal substrate controlling smooth pursuit eye movements.
- Evidence suggests a functional division within the NRTP, with rostral portions related to pursuit and caudal portions to saccades.
- The rNRTP participates in a corticopontocerebellar circuit for smooth pursuit, paralleling known pathways.