Bilateral dorsal fronto-parietal areas are associated with integration of visual motion information and timed motor action

Abstract

Interaction with the environment often involves situations requiring visuomotor integration. For instance, in fast interceptive actions, the brain must integrate visual information of motion with the appropriate motor action. In such dynamic situation, the brain may control movement based on predictions of where the object will be in the future and when it will arrive there. Although previous studies have analyzed brain regions associated with processing visual information of motion, motor control and visuomotor integration with static objects, less is known about visuomotor integration with moving objects. In the present study we used an event-related fMRI experiment to investigate brain areas integrating visual information of motion with motor action in response to moving objects. Twenty healthy volunteers performed an interceptive task where they had to press a button in synchrony with the arrival of a horizontally moving target at a predefined location. They also performed two control tasks—simple reaction and attention to visual motion—in order to identify and exclude brain areas that would be involved in motor or visual motion processing components that are inherent to interceptive tasks. Through a conjunction analysis, we show greater BOLD signal in a bilateral dorsal fronto-parietal network, as well as the intraparietal sulcus, angular gyrus, and human visual motion area hV5+. We discuss these results with respect to their previously identified functions, and suggest they play a role in visuomotor integration with moving objects.

Introduction

Interaction with the environment often involves situations requiring visuomotor integration. For instance, to reach for and grasp a cup of coffee, the brain transforms the visual information of the position of the cup into appropriate motor commands [1], [2]. Visuomotor integration is even more complicated when we interact with the environment in dynamic situations. We also have to estimate an objects changing position over time, such as catching a flying ball coming towards us, or avoiding to be hit by a car while crossing the street. Many studies have investigated possible optical variables involved in visuomotor integration (see [3], [4], for reviews) and the neural basis for the integration of static visual information with reaching and grasping movements (see [5], [2], for reviews). However, less attention has been given to the neural underpinnings of the integration of visual information and motor actions in dynamic scenarios.

Dynamic situations with high temporal constraints, such as fast interceptive actions, may be controlled using predictions of where the object will be in the future and when it will arrive there [6], [7], [8], [4]. The building blocks for estimating when an object will be intercepted, such as distance between two objects, velocity and direction of motion, have been thoroughly investigated in primates and humans [9], [10], [11]. Only few neuroimaging studies have tried to understand how and in which areas of the brain these elements are integrated to perform temporal prediction of moving objects. For instance, Indovina and collegues [12] have shown that a network comprising bilateral fronto-parietal areas is associated with intercepting moving targets (see also [13], [14], [15]). However, these studies fail to precisely identify which regions are associated with visuomotor integration per se because control conditions lack either similar low-level visual or motor information, such as same motor output or visual stimuli [14], or high-level attentional aspects of the task [12], [13], such as attending target motion. Another issue is the lack of spatial specificity of the recording method (MEG: [15]). In contrast to interceptive tasks, temporal estimation in perceptual tasks involve a left lateralized network comprising the supramarginal gyrus and the ventral premotor cortex [16], [17], [18], [19]. Therefore, it remains to be shown whether the central nervous system relies on a bilateral or left lateralized fronto-parietal network to integrate temporal information extracted from target motion in an interceptive task.

In the present study we sought to identify which brain regions are associated with integrating visual information of a moving target and a timed motor action in a coincident anticipation task using fMRI. Coincident anticipation tasks are a class of interceptive actions in which the participant presses a button in synchrony with the arrival of the target at a predetermined position [20]. We hypothesized that the supramarginal gyrus and ventral premotor cortex on the left hemisphere would be associated with this type of visuomotor integration task because it was previously associated with temporal prediction in perceptual tasks [17], [18]. We also hypothesized that the borders of the intraparietal sulcus would be involved in the visuomotor integration given that it has been previously associated with visuomotor integration with static visual information [1], [2] and given that it has connections with premotor cortex [21], [22], [23]. In order to control for low-level—general motor or visual motion processes—and high-level—motor preparation and attention to visual motion—activations, we compared the activation in the coincident anticipation task to reaction time and attention to visual motion conditions. Whenever our initial hypotheses were not met, we explored possible explanations for activity in other brain areas. The comparison of these conditions showed a bilateral dorsal fronto-parietal network, as well as activity in the ascending limb of the inferior temporal sulcus (hV5+ complex; [24], [25]) and the angular gyrus.