Saccades: Fundamentals and Neural Mechanisms

Abstract

Saccadic eye movements allow humans to explore the visual environment, quickly moving the fovea and attention to points of interest for detailed visual processing. Despite these rapid changes in visual input, the brain maintains a stable visual representation through saccadic suppression of blurred input and predictive remapping of receptive fields. In the laboratory, visually-guided saccades are driven primarily by the onset of new stimuli, while volitional saccades are driven by instructions or internal motivation. The distinction between these two classes of saccades is not definitive, but used to illustrate different cognitive loads that fall upon a spectrum based on the balance of visual input and cognitive control processes required to perform simple behavioral tasks. Visually-guided prosaccades depend upon a simple stimulus-response mapping whereby the eye movement is directed toward the peripheral stimulus quickly and accurately. Decision-making processes nonetheless slow the latencies of these basic visual-motor responses to ensure selection of an appropriate saccade target. To dissect the time course of saccade programming, researchers can include a secondary stimulus step or distractor stimulus in the saccade paradigm that alters response characteristics based on additional cognitive processes that occur. Attentional processes, for example, have a strong influence on the way in which participants respond: A pre-trial location cue attracts attention and reduces saccade latencies at that location and increases latencies at uncued locations. If attention is re-directed to central fixation, however, latencies to the originally cued location will be slower than other parts of the visual field, an effect known as inhibition of return. Furthermore, attentional preparation may contribute to the production of fast latency “express” saccades that occur in gap paradigms. The offset of fixation warns the participant of the upcoming stimulus appearance and disengages fixation neurons, allowing saccade-related activity to increase in expectation of the peripheral stimulus. On the other end of the spectrum, “volitional” forms of saccades are elicited via instructional manipulations that require participants to suppress an immediate saccade to a visual stimulus or otherwise rely upon endogenous goals to produce a saccade at a certain time. Antisaccades, ocular motor delayed response saccades, and predictive saccades all fall into this category. Antisaccade tasks require a saccade to the mirror image location of a visual stimulus, depending upon suppression of the visually-driven saccade tendency and a sensorimotor transformation of spatial coordinates to generate the volitional saccade successfully. In this task, the internal saccade programs representing the antisaccade and visually-guided saccade responses are modelled as competing activations racing toward a threshold for motor generation. An ocular motor delayed response task includes a delay period between the presentation of the peripheral stimulus and the time when participants are instructed to respond. Spatial memory processes thus are needed to maintain the target location after the visual stimulus itself is extinguished. Typically, both tasks result in slower latencies, more errors, and poorer spatial accuracy than their visually-guided counterparts. Finally, a predictive saccade task consists of a visual stimulus alternating between two locations at regular intervals. After a few trials, participants learn the spatiotemporal pattern and begin to anticipate the movement, generating saccades to the target location based on internal timing mechanisms before the visual stimulus appears. The aforementioned saccade tasks are supported by a well characterized and widespread neural saccade circuitry. This circuitry includes occipital cortex, posterior parietal cortex, frontal and supplementary eye fields, thalamus, basal ganglia, cerebellum, and the superior colliculus. Visual input initiates neural activation in occipital cortex which spreads to parietal and frontal regions for attentional processing, visuospatial calculations, and saccade motor preparation. Volitional saccade tasks show greater strength and/or extent of activation in this circuitry, and recruitment of new regions, including prefrontal cortex and anterior cingulate cortex, to support additional cognitive control requirements, such as inhibition, working memory, and motor learning. Along with input from the cerebellum, thalamus, and basal ganglia, cortical signals ultimately are integrated within the retinotopic maps of the superior colliculus where a single target location is selected and a motor program triggered via the brainstem ocular motor nuclei. Numerous neuroimaging studies in healthy humans using fMRI, EEG, MEG, and PET report activations in these brain areas during saccades and support findings from lesion studies and intracranial recordings in non-human primates. This consistency makes the saccade network a valuable model for studying cognitive control and understanding how the visual system integrates sensory input with internal goals to create a stable visual representation that guides efficient ocular motor behavior.