scholarly journals Oculomotor plant and neural dynamics suggest gaze control requires integration on distributed timescales

2021 ◽  
Author(s):  
Andrew Miri ◽  
Brandon J. Bhasin ◽  
Emre R. F. Aksay ◽  
David W. Tank ◽  
Mark S. Goldman

A fundamental principle of biological motor control is that the neural commands driving movement must conform to the response properties of the motor plants they control. In the oculomotor system, characterizations of oculomotor plant dynamics traditionally supported models in which the plant responds to neural drive to extraocular muscles on exclusively short, subsecond timescales. These models predict that the stabilization of gaze during fixations between saccades requires neural drive that approximates eye position on longer timescales and is generated through the temporal integration of brief eye velocity-encoding signals that cause saccades. However, recent measurements of oculomotor plant behaviour have revealed responses on longer timescales, and measurements of firing patterns in the oculomotor integrator have revealed a more complex encoding of eye movement dynamics. Here we use measurements from new and published experiments in the larval zebrafish to link dynamics in the oculomotor plant to dynamics in the neural integrator. The oculomotor plant in both anaesthetized and awake larval zebrafish was characterized by a broad distribution of response timescales, including those much longer than one second. Analysis of the firing patterns of oculomotor integrator neurons, which exhibited a broadly distributed range of decay time constants, demonstrates the sufficiency of this activity for stabilizing gaze given an oculomotor plant with distributed response timescales. This work suggests that leaky integration on multiple, distributed timescales by the oculomotor integrator reflects an inverse model for generating oculomotor commands, and that multi-timescale dynamics may be a general feature of motor circuitry.

1987 ◽  
Vol 58 (4) ◽  
pp. 832-849 ◽  
Author(s):  
D. Tweed ◽  
T. Vilis

1. This paper develops three-dimensional models for the vestibuloocular reflex (VOR) and the internal feedback loop of the saccadic system. The models differ qualitatively from previous, one-dimensional versions, because the commutative algebra used in previous models does not apply to the three-dimensional rotations of the eye. 2. The hypothesis that eye position signals are generated by an eye velocity integrator in the indirect path of the VOR must be rejected because in three dimensions the integral of angular velocity does not specify angular position. Computer simulations using eye velocity integrators show large, cumulative gaze errors and post-VOR drift. We describe a simple velocity to position transformation that works in three dimensions. 3. In the feedback control of saccades, eye position error is not the vector difference between actual and desired eye positions. Subtractive feedback models must continuously adjust the axis of rotation throughout a saccade, and they generate meandering, dysmetric gaze saccades. We describe a multiplicative feedback system that solves these problems and generates fixed-axis saccades that accord with Listing's law. 4. We show that Listing's law requires that most saccades have their axes out of Listing's plane. A corollary is that if three pools of short-lead burst neurons code the eye velocity command during saccades, the three pools are not yoked, but function independently during visually triggered saccades. 5. In our three-dimensional models, we represent eye position using four-component rotational operators called quaternions. This is not the only algebraic system for describing rotations, but it is the one that best fits the needs of the oculomotor system, and it yields much simpler models than do rotation matrix or other representations. 6. Quaternion models predict that eye position is represented on four channels in the oculomotor system: three for the vector components of eye position and one inversely related to gaze eccentricity and torsion. 7. Many testable predictions made by quaternion models also turn up in models based on other mathematics. These predictions are therefore more fundamental than the specific models that generate them. Among these predictions are 1) to compute eye position in the indirect path of the VOR, eye or head velocity signals are multiplied by eye position feedback and then integrated; consequently 2) eye position signals and eye or head velocity signals converge on vestibular neurons, and their interaction is multiplicative.(ABSTRACT TRUNCATED AT 400 WORDS)


Author(s):  
Sharon Dixon ◽  
Sophie Roberts

An orthotic is a custom-made insole which fits inside a shoe with the purpose of changing the way in which the foot functions during both standing and dynamic gait. There are many theories regarding the influence of these devices on the foot and lower limb. It is widely accepted that the fundamental principle is that an orthotic encourages a change in the movement pattern of the foot, aiming to alleviate stress to musculoskeletal structures, and produce changes in muscle firing patterns. An example of how an orthotic works is when one is used to change the functioning position of the medial longitudinal arch of the foot by altering the orientation of the calcaneus and potentially reducing the demand on the tibialis posterior tendon....


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Ting-Feng Lin ◽  
Mohammad Mohammadi ◽  
Ahmed M. Fathalla ◽  
Duygu Pul ◽  
Dennis Lüthi ◽  
...  

AbstractMotor learning is essential to maintain accurate behavioral responses. We used a larval zebrafish model to study ocular motor learning behaviors. During a sustained period of optokinetic stimulation in 5-day-old wild-type zebrafish larvae the slow-phase eye velocity decreased over time. Then interestingly, a long-lasting and robust negative optokinetic afternystagmus (OKAN) was evoked upon light extinction. The slow-phase velocity, the quick-phase frequency, and the decay time constant of the negative OKAN were dependent on the stimulus duration and the adaptation to the preceding optokinetic stimulation. Based on these results, we propose a sensory adaptation process during continued optokinetic stimulation, which, when the stimulus is removed, leads to a negative OKAN as the result of a changed retinal slip velocity set point, and thus, a sensorimotor memory. The pronounced negative OKAN in larval zebrafish not only provides a practical solution to the hitherto unsolved problems of observing negative OKAN, but also, and most importantly, can be readily applied as a powerful model for studying sensorimotor learning and memory in vertebrates.


Neuroreport ◽  
1994 ◽  
Vol 5 (11) ◽  
pp. 1333-1336
Author(s):  
Philippe Mettens ◽  
Guy Cheron ◽  
Emile Godaux

1997 ◽  
Vol 78 (6) ◽  
pp. 3283-3306 ◽  
Author(s):  
Kathleen E. Cullen ◽  
Daniel Guitton

Cullen, Kathleen E. and Daniel Guitton. Analysis of primate IBN spike trains using system identification techniques. II. Relationship to gaze, eye, and head movement dynamics during head-free gaze shifts. J. Neurophysiol. 78: 3283–3306, 1997. We have investigated the relationships among the firing frequency B( t) of inhibitory burst neurons (IBNs) and the metrics and dynamics of the eye, head, and gaze (eye + head) movements generated during voluntary combined eye-head gaze shifts in monkey. The same IBNs were characterized during head-fixed saccades in our first of three companion papers. In head-free gaze shifts, the number of spikes (NOS) in a burst was, for 82% of the neurons, better correlated with gaze amplitude than with the amplitude of either the eye or head components of the gaze shift. A multiple regression analysis confirmed that NOS was well correlated to the sum of head and eye amplitudes during head-free gaze shifts. Furthermore, the mean slope of the relationship between NOS and gaze amplitude was significantly less for head-free gaze shifts than for head-fixed saccades. NOS is a global parameter. To refine we used system identification techniques to evaluate a series of dynamic models in which IBN spike trains were related to gaze or eye movements. We found that gaze- and eye-based models predicted the discharges of IBNs equally well. However, the bias values required by gaze-based models were comparable to those required in our head-fixed models whereas those required by eye-based models were significantly larger. The difference in biases between gaze- and eye-based models was very strongly correlated to the mean head velocity ( H˙) during gaze shifts [ R = −0.93 ± 0.15 (SD)]. This result suggested that the increased bias required by the eye-based models reflected an unmodeled H˙ input onto these cells. To pursue this argument further we investigated a series of dynamic models that included both eye velocity ( E˙) and H˙ terms and this confirmed the importance of these two terms. As in our head-fixed analysis of companion paper I, the most valuable model formulation also included an eye saccade amplitude term (Δ E) and was given by B( t) = r 0 + r 1Δ E + b 1 E˙ + g 1 H˙ where r 0, r 1, b 1, and g 1 are constants. The amplitude of the head velocity coefficient was significantly less than that of the eye velocity coefficient. Furthermore, in our population long-lead IBNs tended to have a smaller head velocity coefficients than short-lead IBNs. We conclude that during head-free gaze shifts, the head velocity signal carried to the abducens nucleus by primate excitatory burst neurons (EBNs; if EBNs and IBNs carry similar signals) must be offset by other premotor cells.


2008 ◽  
Vol 99 (1) ◽  
pp. 96-111 ◽  
Author(s):  
Tamara Tchelidze ◽  
Bernhard J. M. Hess

To investigate the role of noncommutative computations in the oculomotor system, three-dimensional (3D) eye movements were measured in seven healthy subjects using a memory-contingent vestibulooculomotor paradigm. Subjects had to fixate a luminous point target that appeared briefly at an eccentricity of 20° in one of four diagonal directions in otherwise complete darkness. After a fixation period of ∼1 s, the subject was moved through a sequence of two rotations about mutually orthogonal axes in one of two orders (30° yaw followed by 30° pitch and vice versa in upright and 30° yaw followed by 20° roll and vice versa in both upright and supine orientations). We found that the change in ocular torsion induced by consecutive rotations about the yaw and the pitch axis depended on the order of rotations as predicted by 3D rotation kinematics. Similarly, after rotations about the yaw and roll axis, torsion depended on the order of rotations but now due to the change in final head orientation relative to gravity. Quantitative analyses of these ocular responses revealed that the rotational vestibuloocular reflexes (VORs) in far vision closely matched the predictions of 3D rotation kinematics. We conclude that the brain uses an optimal VOR strategy with the restriction of a reduced torsional position gain. This restriction implies a limited oculomotor range in torsion and systematic tilts of the angular eye velocity as a function of gaze direction.


Sensors ◽  
2019 ◽  
Vol 19 (3) ◽  
pp. 626 ◽  
Author(s):  
Katarzyna Harezlak ◽  
Pawel Kasprowski

Eye movement is one of the biological signals whose exploration may reveal substantial information, enabling greater understanding of the biology of the brain and its mechanisms. In this research, eye movement dynamics were studied in terms of chaotic behavior and self-similarity assessment to provide a description of young, healthy, oculomotor system characteristics. The first of the investigated features is present and advantageous for many biological objects or physiological phenomena, and its vanishing or diminishment may indicate a system pathology. Similarly, exposed self-similarity may prove useful for indicating a young and healthy system characterized by adaptability. For this research, 24 young people with normal vision were involved. Their eye movements were registered with the usage of a head-mounted eye tracker, using infrared oculography, embedded in the sensor, measuring the rotations of the left and the right eye. The influence of the preprocessing step in the form of the application of various filtering methods on the assessment of the final dynamics was also explored. The obtained results confirmed the existence of chaotic behavior in some parts of eye movement signal; however, its strength turned out to be dependent on the filter used. They also exposed the long-range correlation representing self-similarity, although the influence of the applied filters on these outcomes was not unveiled.


2019 ◽  
Vol 121 (2) ◽  
pp. 513-529 ◽  
Author(s):  
Julianne Skinner ◽  
Antimo Buonocore ◽  
Ziad M. Hafed

Two main types of small eye movements occur during gaze fixation: microsaccades and slow ocular drifts. While microsaccade generation has been relatively well studied, ocular drift control mechanisms are unknown. Here we explored the degree to which monkey smooth eye movements, on the velocity scale of slow ocular drifts, can be generated systematically. Two male rhesus macaque monkeys tracked a spot moving sinusoidally, but slowly, along the horizontal or vertical direction. Maximum target displacement in the motion trajectory was 30 min arc (0.5°), and we varied the temporal frequency of target motion from 0.2 to 5 Hz. We obtained an oculomotor “transfer function” by measuring smooth eye velocity gain (relative to target velocity) as a function of frequency, similar to past work with large-amplitude pursuit. Monkey eye velocities as slow as those observed during slow ocular drifts were clearly target motion driven. Moreover, as with large-amplitude smooth pursuit, eye velocity gain varied with temporal frequency. However, unlike with large-amplitude pursuit, exhibiting low-pass behavior, small-amplitude motion tracking was band pass, with the best ocular movement gain occurring at ~0.8–1 Hz. When oblique directions were tested, we found that the horizontal component of pursuit gain was larger than the vertical component. Our results provide a catalog of the control abilities of the monkey oculomotor system for slow target motions, and they also support the notion that smooth fixational ocular drifts are controllable. This has implications for neural investigations of drift control and the image-motion consequences of drifts on visual coding in early visual areas. NEW & NOTEWORTHY We studied the efficacy of monkey smooth pursuit eye movements for very slow target velocities. Pursuit was impaired for sinusoidal motions of frequency less than ~0.8–1 Hz. Nonetheless, eye trajectory was still sinusoidally modulated, even at velocities lower than those observed during gaze fixation with slow ocular drifts. Our results characterize the slow control capabilities of the monkey oculomotor system and provide a basis for future understanding of the neural mechanisms for slow ocular drifts.


Neuroreport ◽  
1994 ◽  
Vol 5 (11) ◽  
pp. 1333-1336 ◽  
Author(s):  
Philippe Mettens ◽  
Guy Cheron ◽  
Emile Godaux

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