High field functional magnetic resonance imaging in the awake, behaving primate: Cortical networks involved in vergence eye movements

Abstract

Animals with eyes positioned towards the front of the head are capable of making saccadic and smooth pursuit eye movements to fixate an object at a given distance. These eye movements are conjugate (i.e. both eyes move the same amount in the same direction). To fixate objects at different distances, such animals are also capable of making vergence eye movements in which both eyes move the same amount in opposite directions i.e. disconjugately. While purely conjugate or vergence eye movements rarely occur in daily life, it is useful to study these types of eye movements separately due to the relative simplicity of addressing a single system. Further, the neural networks responsible for these eye movements represent an ideal model for sensory processing, sensorimotor integration/transformation and motor output in that all of the components are contained within one localized area: the head. While much is known about the subcortical networks involved in both types of eye movements and about the cortical networks involved in conjugate eye movements, the cortical areas involved in vergence eye movements remain to be fully elucidated.

To delineate the cortical areas involved in the initiation and execution of vergence eye movements, we trained a rhesus macaque monkey (Macaca mulatta) to perform visually-guided vergence eye movements during functional magnetic resonance imaging (fMRI). As the entire system responsible for these movements is contained within the head and the possible cortical candidates underlying these movements were many, fMRI provided an ideal tool by which to identify vergence-related areas.

We found that there was a distributed cortical network involved in the stimulus processing and/or production of a motor signal for vergence movements including the superior temporal sulcus, the arcuate sulcus, the intraparietal sulcus and the principle sulcus. We also found a dissociation of function for these areas in that some were more strongly related to the processing of the vergence-eliciting stimuli whereas others were more strongly related to the motor component of the eye movement.

The rapidity with which these data were acquired and the spatial/functional specificity of the resultant statistical maps illustrate the power and versatility of implementing fMRI to investigate brain function, especially when there is relatively little known about the behavior in question.