Gaze Pursuit Responses in Nucleus Reticularis Tegmenti Pontis of Head-Unrestrained Macaques

Abstract

Suzuki DA, Betelak KF, Yee RD. Gaze pursuit responses in nucleus reticularis tegmenti pontis of head-unrestrained macaques. J Neurophysiol 101: 460 -473, 2009. First published November 5, 2008 doi:10.1152/jn.00615.2007. Eye-head gaze pursuit-related activity was recorded in rostral portions of the nucleus reticularis tegmenti pontis (rNRTP) in alert macaques. The head was unrestrained in the horizontal plane, and macaques were trained to pursue a moving target either with their head, with the eyes stationary in the orbits, or with their eyes, with their head voluntarily held stationary in space. Head-pursuit-related modulations in rNRTP activity were observed with some cells exhibiting increases in firing rate with increases in head-pursuit frequency. For many units, this head-pursuit response appeared to saturate at higher frequencies (Ͼ0.6 Hz). The response phase re:peak head-pursuit velocity formed a continuum, containing cells that could encode head-pursuit velocity and those encoding head-pursuit acceleration. The latter cells did not exhibit head position-related activity. Sensitivities were calculated with respect to peak head-pursuit velocity and averaged 1.8 spikes/s/deg/s. Of the cells that were tested for both head-and eye-pursuit-related activity, 86% exhibited responses to both head-and eye-pursuit and therefore carried a putative gaze-pursuit signal. For these gaze-pursuit units, the ratio of head to eye response sensitivities averaged ϳ1.4. Pursuit eccentricity seemed to affect head-pursuit response amplitude even in the absence of a head position response per se. The results indicated that rNRTP is a strong candidate for the source of an active headpursuit signal that projects to the cerebellum, specifically to the target-velocity and gaze-velocity Purkinje cells that have been observed in vermal lobules VI and VII. I N T R O D U C T I O NProper visual function is dependent on the accurate pointing of the fovea toward visual objects of interest. Rotations of the eyeball are the common means of accomplishing this foveation. However, head movements often accompany eye movements when large gaze shifts are required as we navigate our visual environment. Although much is known about the neuronal mechanisms involved with rotating the eyeball, less is known about the control of head movements.The numerous motor-related inputs to the nucleus reticularis tegmenti pontis (NRTP) together with functions known to date indicate that NRTP could be involved with the coordinated control of eye-and-head motor behavior. Projections to NRTP include inputs from the frontal and supplementary eye fields and the premotor and motor cortices (Brodal 1980a;Giolli et al. 2001;Hartmann-von Monakow et al. 1981;Huerta et al. 1986; Künzle and Akert 1977;Leichnetz 1986;Leichnetz et al. 1984; Shook et al. 1990;Stanton et al. 1988). Both the frontal eye field and NRTP have been shown to be involved with the control of smooth pursuit eye movements (Gottlieb et al. 1993(Gottlieb et al. , 1994Keating 1991;Lynch 1987;MacAvoy 1991;Ono...

The interaction of visual, vestibular and extra‐retinal mechanisms in the control of head and gaze during head‐free pursuit

“…6 ). It is likely that the output from FEF contains both visual and non-visual components of pursuit that interact with the VOR in the brainstem to control eye movement ( Roy & Cullen, 2003 ; Ono & Mustari, 2009 ; Suzuki et al 2009 ).…”

Pursuit disorder and saccade dysmetria after caudal fastigial inactivation in the monkey

“…Clinical and experimental neurological studies should determine whether perturbations in the cerebral cortex, the pontine nuclei, the thalamus, and even the paraflocculus lead to correlated or uncorrelated saccade and pursuit deficits when the behavioral test requires tracking the same visual target. Anatomical studies are also required to identify the cerebellar territories involved in the adjustment of the vertical component of eye movements, as well as the streams by which the activity of reticulospinal neurons is modulated when the head accompanies the tracking eye movements (e.g., Belton and McCrea 2000;Roy and Cullen 2003;Suzuki et al 2009;Takahashi et al 2014).…”

Target position relative to the head is essential for predicting head movement during head-free gaze pursuit

“…It has been well established that cognitive factors such as expectation and anticipation play a significant role in the generation of smooth pursuit eye movements as well as head movements (Barnes and Collins 2008; Ackerley and Barnes 2011). Further, monkeys can be trained to voluntarily pursue targets while maintaining the head in a relatively stable position (Suzuki et al 2009). For our analysis, we wanted a dataset that could be analyzed on a trial-by-trial basis, in order to isolate the effects of the velocity and position of the target.…”

“…We intended this to put the monkeys in situations where making large head movements was advantageous or even required to complete the tasks. Other studies have kept pursuit amplitudes small, even when the head is free to move in order to facilitate direct comparison with head-fixed data, but compensate by training monkeys to pursue targets with their heads (Suzuki et al 2009). Our methods are more comparable with behavior in the natural world, where visual targets do not always remain observable within the oculomotor limits, and can change direction and velocity at any time.…”