Takanobu Yamanobe

Coding of smooth eye movements in three-dimensional space by frontal cortex

Through the development of a high-acuity fovea, primates with frontal eyes have acquired the ability to use binocular eye movements to track small objects moving in space. The smooth-pursuit system moves both eyes in the same direction to track movement in the frontal plane (frontal pursuit), whereas the vergence system moves left and right eyes in opposite directions to track targets moving towards or away from the observer (vergence tracking). In the cerebral cortex and brainstem, signals related to vergence eye movements—and the retinal disparity and blur signals that elicit them—are coded independently of signals related to frontal pursuit. Here we show that these types of signal are represented in a completely different way in the smooth-pursuit region of the frontal eye fields. Neurons of the frontal eye field modulate strongly during both frontal pursuit and vergence tracking, which results in three-dimensional cartesian representations of eye movements. We propose that the brain creates this distinctly different intermediate representation to allow these neurons to function as part of a system that enables primates to track and manipulate objects moving in three-dimensional space.

Directional asymmetry in smooth ocular tracking in the presence of visual background in young and adult primates

The smooth pursuit system moves the eyes in space accurately while compensating for visual inputs from the moving background and/or vestibular inputs during head movements. To understand the mechanisms underlying such interactions, we examined the influence of a stationary textured visual background on smooth pursuit tracking and compared the results in young and adult humans and monkeys. Six humans (three children, three adults) and six macaque monkeys (five young, one adult) were used. Human eye movements were recorded using infrared oculography and evoked by a sinusoidally moving target presented on a computer monitor. Scleral search coils were used for monkeys while they tracked a target presented on a tangent screen. The target moved in a sinusoidal or trapezoidal fashion with or without whole body rotation in the same plane. Two kinds of backgrounds, homogeneous and stationary textured, were used. Eye velocity gains (eye velocity/target velocity) were calculated in each condition to compare the influence of the textured background. Children showed asymmetric eye movements during vertical pursuit across the textured (but not the homogeneous) background; upward pursuit was severely impaired, and consisted mostly of catch-up saccades. In contrast, adults showed no asymmetry during pursuit across the different backgrounds. Monkeys behaved similarly; only slight effects were observed with the textured background in a mature monkey, whereas upward pursuit was severely impaired in young monkeys. In addition, VOR cancellation was severely impaired during upward eye and head movements, resulting in residual downward VOR in young monkeys. From these results, we conclude that the directional asymmetry observed in young primates may reflect a different neural organization of the vertical, particularly upward, pursuit system in the face of conflicting visual and vestibular inputs that can be associated with pursuit eye movements. Apparently, proper compensation matures later.

Role of the frontal eye fields in smooth-gaze tracking

Visual and vestibular senses are essential for appropriate motor behavior in three-dimensional (3D) space. Discovery of relevant specific subdivisions in sensory and motor pathways in recent decades has considerably advanced our understanding of the overall neural control of movement. Such subdivisions must eventually be further delineated into functional neural circuits for purposeful motor acts. Two critical questions are where in the brain do such circuits operate, and by what means. In this chapter, these issues are addressed for smooth tracking eye-movement systems in the simian. These results show that contrary to current understanding, synthesis of the functionally similar eye-movement systems, smooth-pursuit and vergence, takes place in the frontal cortex. This processing, which is of higher order than previously supposed, enables primates to track and manipulate objects moving in 3D space with the utmost of efficiency.

Response of a pacemaker neuron model to stochastic pulse trains

Abstract. We investigated the response of a pacemaker neuron model to trains of inhibitory stochastic impulsive perturbations. The model captures the essential aspect of the dynamics of pacemaker neurons. Especially, the model reproduces linearization by stochastic pulse trains, that is, the disappearance of the paradoxical segments in which the output firing rate of pacemaker neurons increases with inhibition rate, as the coefficient of variation of the input pulse train increases. To study the response of the model to stochastic pulse trains, we use a Markov operator governing the phase transition. We show how linearization occurs based on the spectral analysis of the Markov operator. Moreover, using Lyapunov exponents, we show that variable inputs evoke reliable firing, even in situations where periodic stimulation with the same mean rate does not.

Adaptive eye movements induced by cross-axis pursuit--vestibular interactions in trained monkeys.

We showed previously that smooth pursuit training combined with whole-body rotation in the orthogonal plane induces adaptive cross-axis vestibulo-ocular reflex (VOR). To gain an insight into the possible pathways and the nature of error signals for cross-axis VOR adaptation, we examined further properties of adaptive responses. In the first series, we trained monkeys for vertical pursuit during sinusoidal yaw rotation at 0.5 Hz ( - 10°) by presenting a target spot either in phase with, or with phase shifts (lead or lag) of 90° to, the chair for 1 h. After training, sinusoidal or trapezoidal yaw rotation was tested in complete darkness without a target. Different training conditions resulted in different amounts of phase shift in cross-axis VOR. Trapezoidal yaw rotation (peak acceleration , 780°/s 2 ) revealed further differences in the direction, latency and time course of the adaptive responses depending on the conditions of the pursuit task. At least two (fast and slow) components with different latencies were induced in the cross-axis VOR by trapezoidal rotation after in-phase and phase-shift training. Adaptive responses were accurately simulated by the weighted sum of these two components. In the second series, we examined the effects of sequentially flashed (10 w s) targets in the horizontal plane during pitch rotation. The monkeys learned to track such targets by smooth pursuit, and cross-axis VOR was also induced after such apparent motion stimuli without retinal slip of the target image. These results indicate the importance of eye velocity for cross-axis VOR and suggest that this adaptation occurs most probably in the smooth pursuit pathways.We showed previously that smooth pursuit training combined with whole-body rotation in the orthogonal plane induces adaptive cross-axis vestibulo-ocular reflex (VOR). To gain an insight into the possible pathways and the nature of error signals for cross-axis VOR adaptation, we examined further properties of adaptive responses. In the first series, we trained monkeys for vertical pursuit during sinusoidal yaw rotation at 0.5 Hz (+/- 10 degrees) by presenting a target spot either in phase with, or with phase shifts (lead or lag) of 90 degrees to, the chair for 1 h. After training, sinusoidal or trapezoidal yaw rotation was tested in complete darkness without a target. Different training conditions resulted in different amounts of phase shift in cross-axis VOR. Trapezoidal yaw rotation (peak acceleration approximately 780 degrees/s2) revealed further differences in the direction, latency and time course of the adaptive responses depending on the conditions of the pursuit task. At least two (fast and slow) components with different latencies were induced in the cross-axis VOR by trapezoidal rotation after in-phase and phase-shift training. Adaptive responses were accurately simulated by the weighted sum of these two components. In the second series, we examined the effects of sequentially flashed (10 microseconds) targets in the horizontal plane during pitch rotation. The monkeys learned to track such targets by smooth pursuit, and cross-axis VOR was also induced after such apparent motion stimuli without retinal slip of the target image. These results indicate the importance of eye velocity for cross-axis VOR and suggest that this adaptation occurs most probably in the smooth pursuit pathways.

Analysis of models for crustacean stretch receptors

Abstract. The mechanisms underlying the diverse responses to step current stimuli of models [Edman et al. (1987) J Physiol (Lond) 384: 649–669] of lobster slowly adapting stretch receptor organs (SAO) and fast-adapting stretch receptor organs (FAO) are analyzed. In response to a step current, the models display three distinct types of firing reflecting the level of adaptation to the stimulation. Low-amplitude currents evoke transient firing containing one to several action potentials before the system stabilizes to a resting state. Conversely, high-amplitude stimulations induce a high frequency transient burst that can last several seconds before the model returns to its quiescent state. In the SAO model, the transition between the two regimes is characterized by a sustained pacemaker firing at an intermediate stimulation amplitude. The FAO model does not exhibit such a maintained firing; rather, the duration of the transient firing increases at first with the stimulus intensity, goes through a maximum and then decreases at larger intensities. Both models comprise seven variables representing the membrane potential, the sodium fast activation, fast inactivation, slow inactivation, the potassium fast activation, slow inactivation gating variables, and the intra cellular sodium concentration. To elucidate the mechanisms of the firing adaptations, the seven-variable model for the lobster stretch receptor neuron is first reduced to a three-dimensional system by regrouping variables with similar time scales. More precisely, we substituted the membrane potential V for the sodium fast activation equivalent potential Vm, the potassium fast inactivation Vn for the sodium fast inactivation Vh, and the sodium slow inactivation Vl for the potassium slow inactivation Vr. Comparison of the responses of the reduced models to those of the original models revealed that the main behaviors of the system were preserved in the reduction process. We classified the different types of responses of the reduced SAO and FAO models to constant current stimulation. We analyzed the transient and stationary responses of the reduced models by constructing bifurcation diagrams representing the qualitatively distinct dynamics of the models and the transitions between them. These revealed that (1) the transient firings prior to reaching the stationary state can be accounted for by the sodium slow inactivation evolving more slowly than the other two variables, so that the changes during the transient firings reflect the bifurcations that the two-dimensional system undergoes when the sodium slow inactivation, considered as a parameter, is varied; and (2) the stationary behaviors of the models are captured by the standard bifurcations of a two-dimensional system formed by the membrane potential and the potassium fast inactivation. We found that each type of firing and the transitions between them is due to the interplay between essentially three variables: two fast ones accounting for the action potential generation and the post-discharge refractoriness, and a third slow one representing the adaptation.