Predictive responses of periarcuate pursuit neurons to visual target motion

Abstract

The smooth pursuit eye movement system uses retinal information about the image-slip-velocity of the target in order to match the eye-velocity-in-space (i.e., gaze-velocity) to the actual target velocity. To maintain the target image on the fovea during smooth gaze tracking, and to compensate for the long delays involved in processing visual motion information and/or eye velocity commands, the pursuit system must use prediction. We have shown recently that both retinal image-slip-velocity and gaze-velocity signals are coded in the discharge of single pursuit-related neurons in the simian periarcuate cortex. To understand how periarcuate pursuit neurons are involved in predictive smooth pursuit, we examined the discharge characteristics of these neurons in trained Japanese macaques. When a stationary target abruptly moved sinusoidally along the preferred direction at 0.5 Hz, the response delays of pursuit cells seen at the onset of target motion were compensated in succeeding cycles. The monkeys were also required to continue smooth pursuit of a sinusoidally moving target while it was blanked for about half of a cycle at 0.5 Hz. This blanking was applied before cell activity normally increased and before the target changed direction. Normalized mean gain of the cells' responses (re control value without blanking) decreased to 0.81(+/-0.67 SD), whereas normalized mean gain of the eye movement (eye gain) decreased to 0.65 (+/-0.16 SD). A majority (75%) of pursuit neurons discharged appropriately up to 500 ms after target blanking even though eye velocity decreased sharply, suggesting a dissociation of the activity of those pursuit neurons and eye velocity. To examine whether pursuit cell responses contain a predictive component that anticipates visual input, the monkeys were required to fixate a stationary target while a second test laser spot was moved sinusoidally. A majority (68%) of pursuit cells tested responded to the second target motion. When the second spot moved abruptly along the preferred direction, the response delays clearly seen at the onset of sinusoidal target motion were compensated in succeeding cycles. Blanking (400-600 ms) was also applied during sinusoidal motion at 1 Hz before the test spot changed its direction and before pursuit neurons normally increased their activity. Preferred directions were similar to those calculated for target motion (normalized mean gain=0.72). Similar responses were also evoked even if the second spot was flashed as it moved. Since the monkeys fixated the stationary spot well, such flashed stimuli should not induce significant retinal slip. These results taken together suggest that the prediction-related activity of periarcuate pursuit neurons contains extracted visual components that reflect direction and speed of the reconstructed target image, signals sufficient for estimating target motion. We suggest that many periarcuate pursuit neurons convey this information to generate appropriate smooth pursuit eye movements.

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

“…11B of Fukushima et al 2002a) and were confirmed to be within the caudal FEF in the fundus of the arcuate sulcus. Two other monkeys are still being used for other experiments.…”

“…The inter-aural midpoint of the animals' heads was positioned close to the axis of horizontal rotation. The target was a laser spot that was back-projected onto the tangent screen 75 cm in front of the animals' eyes (monkey C, Fukushima et al 2000Fukushima et al , 2002a and a 22-inch computer display (Sony) positioned 60 cm in front of the animals' eyes (monkeys SI and SH; e.g., Kasahara et al 2006). Once pursuit-responsive single neurons were encountered, smooth pursuit responses were tested in 4 planes (vertical, horizontal and two oblique planes at 45° angles) to determine the preferred direction.…”

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

“…Traces that contained saccades or slow eye movement were removed since they were indicative of the monkeys' failure to fixate the stationary target, and only those traces with eye position changes of less than 1° during each cycle were analyzed as described previously (Fukushima et al 2000(Fukushima et al , 2002aAkao et al 2005). …”

“…Recording locations were histologically confirmed to be within the fundus of the arcuate sulcus by making electrolytic lesions through the recording electrodes as previously described (Tanaka and Fukushima 1998;Fukushima et al 2000Fukushima et al , 2002aJ Fukushima et al 2004).…”

“…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. Moreover, the majority of them also responded to otolith inputs induced by horizontal whole-body translation .…”