Smooth-Pursuit Eye Movement Representation in the Primate Frontal Eye Field

Abstract

Physiological and behavioral data reported here show an involvement of the primate frontal eye field (FEF) cortex in smooth-pursuit eye movements, in addition to its well-established role in saccadic eye movements. Microstimulation just ventral to the small saccade representation of the FEF elicits eye movements that, in contrast to elicited saccades, have low velocities, continue smoothly without interruption during prolonged stimulation, and are usually directed ipsilaterally to the stimulated hemisphere. Neurons in this region respond in association with smooth-pursuit eye movements and visual motion. Tracking deficits following experimental lesions of the FEF depend critically upon the status of this ventral region: superficial lesions sparing it leave smooth-pursuit eye movements intact, whereas lesions removing it produce substantial deficits in the anticipatory initiation, motion-induced acceleration, asymptotic velocity, and predictive continuation of ipsilateral smooth pursuit.

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation

“…1A5-7, B5-7, upward arrows) were clearly shorter than the response latencies during pursuit for the same neurons ( Fig. 1A4 and B4, upward arrows, e.g., MacAvoy et al 1991;Tanaka and Fukushima 1998), indicating that the former responses cannot be induced by visual feedback.…”

“…Vertical and horizontal components of eye movements were recorded by the scleral search coil method (Fuchs and Robinson 1966;Judge et al 1980). Extracellular recordings of pursuit neurons were made mostly in the fundus of the arcuate sulcus as reported previously (e.g., MacAvoy et al 1991;Tanaka and Fukushima 1998) while the monkeys were rewarded with apple juice for tracking a target spot moving sinusoidally at 0.3 or 0.5 Hz (±10°). The inter-aural midpoint of the animals' heads was positioned close to the axis of horizontal rotation.…”

“…During head and/or whole body movement, this system is coordinated with the vestibular system to maintain the accuracy of eye-movements in space (see Leigh and Zee 1999 for a review). The caudal part of the frontal eye fields (FEF) in the fundus of the arcuate sulcus contains many smooth-pursuit related neurons (pursuit neurons) (e.g., MacAvoy et al 1991;Gottlieb et al 1993Gottlieb et al , 1994Tanaka and Fukushima 1998). Using sinusoidal whole body rotation in the presence of a pursuit target, previous studies in our laboratory have shown that virtually all FEF pursuit neurons tested responded to vestibular stimulation (Fukushima et al 2000).…”

Vector Averaging for Smooth Pursuit Eye Movements Initiated by Two Moving Targets in Monkeys

“…Lisberger et al (1995) have recorded the responses of MT cells during target speeds and accelerations like those experienced during pursuit, so that much is currently known about this distributed representation of image motion. MT receives its visual inputs mainly from the primary visual cortex (V1) (Maunsell and Van Essen, 1983b) and provides visual inputs for pursuit via projections to a series of higher cortical areas (Ungerleider and Desimone, 1986;Tusa and Ungerleider, 1988;Boussaoud et al, 1992b;Tian and Lynch, 1996) that include the medial superior temporal area (MST) in the parietal cortex (Dürsteler and Wurtz, 1988) and the frontal pursuit area (FPA) in the depths of the arcuate sulcus (Lynch, 1987;MacAvoy et al, 1991). MT, MST, and FPA all project to the pontine nuclei (Glickstein et al, 1980;Ungerleider et al, 1984;Leichnitz, 1989;Boussaoud et al, 1992a), which in turn project to the parts of the cerebellum that are involved in pursuit (Brodal, 1979(Brodal, , 1982Gerrits and Voogd, 1989).…”

Activity of pursuit neurons in the caudal part of the frontal eye fields during static roll-tilt

“…The caudal part of the frontal eye fields (FEF) in the fundus of the arcuate sulcus contains pursuit neurons (e.g., MacAvoy et al 1991;Gottlieb et al 1993Gottlieb et al , 1994Tanaka and Fukushima 1998). The majority of FEF pursuit neurons carry not only visual signals about target motion but also vestibular signals about whole-body rotation that activates primarily semi-circular canals (Fukushima et al 2000(Fukushima et al , 2002aAkao et al 2005Akao et al , 2006.…”