Ординатура / Офтальмология / Английские материалы / Eye Movements A Window on Mind and Brain_Van Gompel_2007

94 M. F. Land

Initially the subjects found it hard to control vertical and horizontal movements at the same time. Little apparent progress was made, and it took as much as 20 s for each “hit” to be made. Interestingly, gaze tracked the cursor with a lag, implying that vision was being used to provide information to the motor system about its progress. In the next phase learning was rapid and, although diagonal moves were still difficult, the time for each hit came down to about 2 s. Gaze was now level with or even led the cursor. In the final phase diagonal moves were made confidently, and gaze, instead of tracking the cursor, went straight to the next target. All this makes excellent sense. The role of vision changes, during the 20 min it takes to learn the task, from providing feedback to an inexpert motor system to giving feed forward information to a system that is now competent to perform a targeted action.

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PART 2

PHYSIOLOGY AND CLINICAL STUDIES

OF EYE MOVEMENTS

Edited by

MARTIN H. FISCHER

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Abstract

Recording of saccadic eye movements has proved to be a valuable tool for investigation of brain function and dysfunction. Recent neurophysiological studies have revealed that the time from target appearance to saccade initiation can be modeled as an accumulator function in which both baseline and rate of rise of saccade-related activity contribute toward achieving threshold for movement initiation. In this chapter, we review recent saccadic eye-movement studies designed to track abilities across development and in disorders of frontal cortex and basal ganglia. Studies can be designed to probe the ability to initiate automatic vs voluntary saccades or to suppress saccades. The accumulator model can be used to explain normal developmental changes in voluntary saccade control that are present in normal development as well as in attention deficit hyperactivity disorder (ADHD), Parkinson’s disease (PD), and Tourette syndrome (TS).

1. Introduction

One of the most important functions of the central nervous system is the generation of movement in response to sensory stimulation. The visual guidance of saccadic eye movements represents one form of sensory-to-motor transformation that has provided significant insight into our understanding of motor control and sensorimotor processing. The eyes have a simple and well-defined repertoire of movements, and the neural circuitry regulating the production of saccadic eye movements is now understood at a level that is sufficient to now link activation in cortical and subcortical areas with behavior and dysfunction. As a result, deficits in eye-movement control of various patient groups can now provide greater insight into the neural substrate underlying the pathophysiology. To properly interpret these insights one must have an understanding of the entire visuomotor loop involved in saccade control, from the visual input on the eye, through the many cortical and subcortical regions of the brain, to the motor output of the brain stem on the muscles that move the eyes, creating behaviors we can measure.

The primate retina has a specialized region in its center, the fovea, which serves the central 1 of the visual field and provides the greatest visual acuity (Perry and Cowey, 1985). In most visual areas of the primate brain, the fovea has the greatest representation, emphasizing the importance of foveal vision in many aspects of visual processing and visually guided behavior (Dow, Snyder, Vautin, & Bauer, 1981; Van Essen, Newsome, & Maunsell, 1984). To maximize the efficiency of foveal vision, we must have the ability to align the fovea rapidly upon objects in the visual world and then keep the fovea aligned upon these objects for a sufficient period of time for the visual system to perform a detailed analysis of the image. Saccadic eye movements are used to redirect the fovea from one point of interest to another and a fixation mechanism is used to keep the fovea aligned on the target during subsequent image analysis. This alternating behavior of saccade–fixation is repeated several hundred thousand times a day and is critical for complex acts such as reading or driving an automobile.

Saccades can be triggered by the appearance of a visual stimulus in the periphery (e.g., the sudden appearance or motion of a novel visual stimulus), or initiated voluntarily, in the absence of any overt sensory stimuli, motivated by the goals of the individual. They can also be suppressed during periods of visual fixation. In special situations where visually guided saccade plans and internally motivated saccade plans compete, the brain must inhibit the automatic response and instead promote the internally motivated saccade in order to perform the desired behavior. Several experimental paradigms have been devised to investigate the control of saccades in these different behavioral situations (see below).

Our understanding of the neural circuitry controlling saccades has increased dramatically in the past 30 years as a result of human behavioral, imaging, and clinical studies as well as animal behavioral, physiological, anatomical, and pharmacological studies. Figure 1 highlights some of the important brain areas that have been identified. Critical nodes in the network include regions of the parietal and frontal cortices, basal ganglia, thalamus, superior colliculus (SC), cerebellum, and brainstem reticular formation (see Hikosaka, Nakamura, & Nakahara, 2000; Leigh and Zee, 1999; Moschovakis,

saccades in a specific direction. Other neurons located in the brainstem reticular formation control the discharge of EBN and IBN. Long-lead burst neurons (LLBN) discharge a high-frequency burst of action potentials for saccades and they also have a low-frequency buildup of activity before the burst. It is believed that LLBN project to the EBN and IBN to provide the burst input. The EBN and IBN are subject to potent inhibition from omnipause neurons (OPN) which discharge tonically during all periods of fixation and pause for saccades in any direction. Thus, in order to generate a saccade, the OPN must be silenced and then the LLBN activate the appropriate pools of EBN and IBN to produce the saccade command that is sent to the MN. Following completion of the saccade, the OPN reactivate and inhibit the EBN and IBN, thus preventing the eyes from moving any further. The tonic activity of the OPN ensures that any early, presaccadic activity among other premotor elements cannot lead to spurious activity among EBN and IBN, which would disrupt fixation.

Inputs to the brainstem premotor circuitry arise from several structures including the frontal cortex, SC, and cerebellum. Although our understanding of how these inputs are coordinated to control the actions of the brainstem premotor circuit precisely are incomplete, significant progress has been made in recent years.

The SC plays a critical role in the control of visual fixation and saccadic eye movements. The superficial layers of the SC (SCs) contain neurons that receive direct retinal inputs as well as inputs from other visual areas (Robinson & McClurkin, 1989). These visual neurons are organized into a visual map of the contralateral visual hemifield.

The intermediate layers of the SC (SCi) contain neurons whose discharges are modulated by saccadic eye movements and visual fixation (see Munoz et al., 2000; Munoz & Fecteau, 2002 for review). These neurons are organized into a retinotopically coded motor map specifying saccades into the contralateral visual field. Neurons that increase their discharge before and during saccades, referred to as saccade neurons, are distributed throughout the SCi. Neurons that are tonically active during visual fixation and pause during saccades, referred to as fixation neurons, are located in the rostrolateral pole of the SC where the fovea is represented. These saccade and fixation neurons in the SC project directly to the brainstem premotor circuitry in the reticular formation to influence behavior.

The (SCi) receives inputs from posterior parietal cortices, frontal cortices, and basal ganglia which all play a role in the voluntary selection of potential saccadic targets to ultimately influence behavior. Visual inputs that are crucial for maintaining visual fixation or generating saccades are directed from visual cortex, through the parietal lobe, to the (SCi). One area in particular that lies at the sensory-motor interface is the lateral intraparietal area (LIP). Projections from LIP to the (SCi) are involved in sensory-motor transformations and attentional processing (see Andersen et al., 1997; Colby & Goldberg, 1999; Glimcher, 2001 for detailed reviews).

The frontal cortex receives direct projections from the visual cortex but areas like the frontal eye fields (FEF) are strongly interconnected with parietal visual areas (see Schall, 1997; Schall & Thompson, 1999 for reviews). This is a vital point as FEF may act as a central hub connecting several frontal areas such as supplementary eye fields (SEF), and the dorsolateral prefrontal cortex (DLPFC) with the parietal cortex, the (SCi) and also the