Infantile strabismus is characterized by numerous visual and oculomotor abnormalities. Recently nonhuman primate models of infantile strabismus have been established, with characteristics that closely match those observed in human patients. This has made it possible to study the neural basis for visual and oculomotor symptoms in infantile strabismus. In this review, we consider the available evidence for neural abnormalities in structures related to oculomotor pathways ranging from visual cortex to oculomotor nuclei. These studies provide compelling evidence that a disturbance of binocular vision during a sensitive period early in life, whatever the cause, results in a cascade of abnormalities through numerous brain areas involved in visual functions and eye movements.
Combined saccade-vergence movements allow humans and other primates to align their eyes with objects of interest in three-dimensions. In the absence of saccades, vergence movements are typically slow, symmetrical movements of the two eyes in opposite directions. However, combined saccade-vergence movements produce vergence velocities that exceed values observed during vergence alone. This phenomenon is often called "vergence enhancement", or "saccade-facilitated vergence," though it is important to consider that rapid vergence changes, known as "vergence transients," are also observed during conjugate saccades. We developed a visual target array that allows monkeys to make saccades in all directions between targets spaced at distances that correspond to ~1° intervals of vergence angle relative to the monkey. We recorded the activity of vergence-sensitive neurons in the supra-oculomotor area (SOA), located dorsal and lateral to the oculomotor nucleus while monkeys made saccades with vergence amplitudes ranging from 0 to 10°. The primary focus of this study was to test the hypothesis that neurons in the SOA fire a high frequency burst of spikes during saccades that could generate the enhanced vergence. We found that individual neurons encode vergence velocity during both saccadic and non-saccadic vergence, yet firing rates were insufficient to produce the observed enhancement of vergence velocity. Our results are consistent with the hypothesis that slow vergence changes are encoded by the SOA while fast vergence movements require an additional contribution from the saccadic system. NEW & NOTEWORTHY Research into combined saccade-vergence movements has so far focused on exploring the saccadic neural circuitry, leading to diverging hypotheses regarding the role of the vergence system in this behavior. In this study, we report the first quantitative analysis of the discharge of individual neurons that encode vergence velocity in the monkey brain stem during combined saccade-vergence movements.
Motion in the visual periphery of lizards, and other animals, often causes a shift of visual attention toward the moving object. This behavioral response must be more responsive to relevant motion (predators, prey, conspecifics) than to irrelevant motion (windblown vegetation). Early stages of visual motion detection rely on simple local circuits known as elementary motion detectors (EMDs). We presented a computer model consisting of a grid of correlation-type EMDs, with videos of natural motion patterns, including prey, predators and windblown vegetation. We systematically varied the model parameters and quantified the relative response to the different classes of motion. We carried out behavioral experiments with the lizard Anolis sagrei and determined that their visual response could be modeled with a grid of correlation-type EMDs with a spacing parameter of 0.3 degrees visual angle, and a time constant of 0.1 s. The model with these parameters gave substantially stronger responses to relevant motion patterns than to windblown vegetation under equivalent conditions. However, the model is sensitive to local contrast and viewer-object distance. Therefore, additional neural processing is probably required for the visual system to reliably distinguish relevant from irrelevant motion under a full range of natural conditions.
Anolis lizards communicate with displays consisting of motion of the head and body. Early portions of long-distance displays require movements that are effective at eliciting the attention of potential receivers. We studied signal-motion efficacy using a two-dimensional visual-motion detection (2DMD) model consisting of a grid of correlation-type elementary motion detectors. This 2DMD model has been shown to accurately predict Anolis lizard behavioural response. We tested different patterns of artificially generated motion and found that an abrupt 0.38 shift of position in less than 100 ms is optimal. We quantified motion in displays of 25 individuals from five species. Four species employ near-optimal movement patterns. We tested displays of these species using the 2DMD model on scenes with and without moderate wind. Display movements can easily be detected, even in the presence of windblown vegetation. The fifth species does not typically use the most effective display movements and display movements cannot be discerned by the 2DMD model in the presence of windblown vegetation. A number of Anolis species use abrupt up-and-down head movements approximately 10 mm in amplitude in displays, and these movements appear to be extremely effective for stimulating the receiver visual system.
PurposePattern strabismus is characterized by a cross-axis pattern of horizontal and vertical misalignments. In A-pattern strabismus, for example, a divergent change in the horizontal misalignment occurs on downgaze. Work with nonhuman primate models has provided evidence that this disorder is associated with abnormal cross-talk between brainstem pathways that normally encode horizontal and vertical eye position and velocity. Neurons in the interstitial nucleus of Cajal (INC) are normally sensitive to vertical eye position; in the present study, we test the hypothesis that, in monkeys with pattern strabismus, some INC neurons will show an abnormal sensitivity to horizontal eye position.MethodsMonkeys were rewarded for fixating a visual target that stepped to various locations on a tangent screen. Single neurons were recorded from INC in one normal monkey, and two with A-pattern strabismus. Multiple linear regression analysis was used to estimate the preferred direction for each neuron.ResultsIn the normal monkey, all INC neurons had preferred directions within 20° of pure vertical (either up or down). The preferred directions were significantly more variable in the monkeys with pattern strabismus, with a minority being more sensitive to horizontal eye position than vertical eye position. In addition, the vertical eye position sensitivity was significantly less in the monkeys with strabismus.ConclusionsIn pattern strabismus, neurons in INC show neurophysiological abnormalities consistent with a failure to develop normal tuning properties. Results were consistent with the hypothesis that, in pattern strabismus, INC receives an abnormally strong signal related to horizontal eye position.
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