Elsevier

Neuroscience Research

Volume 54, Issue 2, February 2006, Pages 112-123
Neuroscience Research

Anterior and superior lateral occipito-temporal cortex responsible for target motion prediction during overt and covert visual pursuit

https://doi.org/10.1016/j.neures.2005.10.015Get rights and content

Abstract

In smooth-pursuit eye movements (SPEM) with gain close to one, SPEM should be controlled mainly by prediction of target motion because retinal slip is nearly zero. We investigated the neural mechanisms of visual-target prediction by the three fMRI experiments. (1) Overt pursuit task: subjects pursued a sinusoidally moving target which blinked (blink condition) or did not blink (continuous condition). (2) Covert pursuit task: subjects covertly pursued the same target with eyes gazed at fixation point. (3) Attend-to-stationary target task: subjects brought attention on a stationary target with eyes gazed at fixation point. In the overt pursuit task, the SPEM gain and the delay in the blink condition were not very different from the continuous condition, indicating good prediction of the blinking target motion. Activities in the dorsolateral prefrontal, precentral, medial superior frontal, intraparietal, and lateral occipito-temporal cortexes increased in the blink-continuous subtraction. The V1 activity decreased for this contrast. In the covert pursuit task, only the anterior/superior LOTC activity remained in the blink-continuous subtraction. In the attend-to-stationary target task, the blink-continuous subtraction elicited no activation. Consequently, the a/sLOTC activity is responsible for target prediction rather than motor commands for eye movements or just target blinking such as visual saliency.

Introduction

High acuity fovea in primates requires smooth pursuit eye movements to continue looking at a target moving slowly and smoothly. The purpose of smooth pursuit eye movements is to minimize retinal slip, i.e. target velocity projected onto the retina. Retinal slip disappears once eye velocity catches up to target velocity in smooth pursuit eye movements. Nevertheless, eye movements are maintained. As a model for smooth pursuit eye movements to a target moving at constant velocity, Robinson et al. (1986) extended the positive feedback model proposed by Yasui and Young (1975) and proposed that smooth pursuit eye movements were maintained by the integration of a retinal slip velocity and the efference copy of eye velocity. This model (Robinson et al., 1986) attempted to cancel out the feedback signal in order to enable high velocity gain (i.e. the ratio of eye velocity to target velocity), and their model works as a feedforward controller. However, their feedforward pathway still contains a significant delay that prevents this model from achieving zero-lag tracking of a sinusoidal signal. For instance, the eye movement lags behind the target motion of a 1-Hz sinusoidal signal by more than 200 ms (Shibata et al., 2005). According to computational theory, target motion prediction is essential in smooth pursuit eye movements at least for sinusoidally moving targets.

Neurophysiological experiments have been conducted on monkeys to investigate the mechanisms related to an internal representation of target velocity Sakata et al., 1983, Newsome et al., 1988, Kawano et al., 1994, Tanaka and Fukushima, 1998, Fukushima et al., 2002a, Fukushima et al., 2002b. The task of these studies had monkey subjects perform smooth pursuit eye movements to a target that suddenly disappeared for a moment, and the results revealed that neurons in the frontal eye field (FEF) (Tanaka and Fukushima, 1998) and the medial superior temporal (MST) Newsome et al., 1988, Sakata et al., 1983, Kawano et al., 1994 successively discharged when a target was blanked as well as when the target was not blanked. These results suggest that the discharges of FEF and MST neurons, referred to as corollary discharges or extraretinal signals, represent information for maintaining smooth-pursuit eye movements. Especially in the task of (Fukushima et al., 2002b), the results showed that discharges of some FEF neurons of a monkey subject increased despite the eye velocity decreasing when the target was blanked compared to when the target was not blanked, indicating that discharges of some FEF neurons represent predictive information of target velocity.

There have been some neuroanatomical studies in humans using functional magnetic resonance imaging (fMRI). Barton et al. (1996) found greater activities in the lateral occipito-temporal cortex (LOTC) of human subjects when the subjects pursued a smoothly moving target on a fixed background than when they gazed at a fixed target on a smoothly moving background, despite the fact that the visual inputs from the retina was almost the same in both conditions. Dukelow et al. (2001) found that the monkey MST homologue of human subjects that lies in the LOTC was activated when the subjects performed non-visual smooth-pursuit eye movements induced by smooth finger movements in comparison with the rest condition. Lencer et al. (2004) showed that activities in the precentral cortex (PreCC; including the monkey FEF homologue), medial superior frontal cortex (MSFC), intraparietal cortex (IPC), and dorsolateral prefrontal cortex (DLPFC) in humans, increased when the subject pursued the target at constant velocity with blanking compared to when they pursued the target without blanking. These studies suggest that activity in these regions reflects an internal representation of the estimated target motion for maintaining smooth-pursuit eye movements. However, since constant velocity motion rather than sinusoidal motion was used in these experiments, their results cannot be used to assess whether brain activities reflected prediction of a target motion or just maintained the last eye velocity. Furthermore, to our knowledge, there has been no study in which the brain activity induced by saccadic eye movements was properly eliminated.

The aim of this study was to identify the human cortical regions involved in a predictive representation of target motion. For our aim, we conducted a series of fMRI tasks with simultaneous recording of eye movements. The result of recording the eye movements showed that our subjects performed predictive smooth pursuit eye movements even if the target was blinking. Furthermore, we confirmed that target motion prediction was important for smooth pursuit to sinusoidal motion by a simulation experiment based on the model proposed in Shibata et al. (2005). The fMRI result indicated that the PreCC, MSFC, IPC, LOTC, and DLPFC increased their activities when the target was blinking during smooth-pursuit eye movements compared to when the target was presented continuously. In the series of tasks, we analyzed the effect of saccades on their activities and conducted control tasks, such as a covert pursuit task and an attend-to-stationary target task, to eliminate the possibilities of contributions by other factors than the prediction of the target. The results of our fMRI experiments suggested that the LOTC activity represented the target motion prediction during smooth-pursuit eye movements.

Section snippets

Subjects

Thirty-two healthy human volunteers (29 males and 3 females) with normal vision participated in this study. All subjects gave informed consent in writing and the study was approved by the Ethics and Safety Committee of Advanced Telecommunications Research Institute International (ATR). Twenty-five subjects (23 males and 2 females) participated in the overt pursuit task. Twelve subjects (9 males and 3 females) participated in the covert pursuit task and the attend-to-stationary target task. Five

Behavioral analysis

Fig. 1A shows a sample time series of eye and target velocity in a test block (including the continuous condition and the blink condition). Fig. 1B shows the averaged eye velocity (thick red line) over all eye velocities (thin green lines) acquired in all of the test blocks of this subject and the target velocity (thick black line). Saccadic components were eliminated in the eye velocities. The dark shaded blocks show that the target was vanishing at that time.

Further detailed analyses of eye

Prediction of the target motion

There has been much interest in how humans model and make use of the external world in the brain. To approach this question, we conducted fMRI studies mainly focusing on the maintenance phase of smooth pursuit eye movements to a sinusoidal moving target. According to the theoretical argument in Shibata et al. (2005), pursuit to a target moving at constant velocity does not require a model of target motion, but pursuit to a sinusoidally moving target without delay does require knowledge of the

Acknowledgment

This research was conducted as part of ‘Research on Human Communication’, with funding from the National Institute of Information and Communications Technology (NICT) and from the Inamori grant program.

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