A noninvasive electromagnetic perturbation approach to probe extraocular proprioception.

BACKGROUND: Extraocular proprioception has been shown to participate in spatial perception and binocular alignment. Yet the physiological approaches used to study this sensory signal are limited because proprioceptive signaling takes place at the same time as visuomotor signaling. It is critical to dissociate this sensory signal from other visuomotor events that accompany eye movements. METHODS: We present a novel noninvasive and quantifiable method for probing extraocular proprioception independent of other visuomotor processing by attaching a rare-earth magnet to a real-time model eye and placing an electromagnet <20 mm from the eye. An electromagnet can increase or decrease angular displacements and velocities of the model eye. RESULTS: Electromagnetic activation rapidly affected (<2 ms) the rotation kinematics of the eye, which were correlated linearly with both the current supply and the distance of the electromagnet relative to the eye. CONCLUSIONS: This method circumvented the constraints of conventional physiological manipulation of extraocular proprioception, such as manually or mechanically tugging on the eye ball. It can be applied to produce the discrepancy between the intended and the executed eye movements, so that proprioceptive reafference signals are dissociated from corollary motor discharges and other visuomotor events.

Brain control and information transfer.

In this review, we examine the importance of having a body as essential for the brain to transfer information about the outside world to generate appropriate motor responses. We discuss the context-dependent conditioning of the motor control neural circuits and its dependence on the completion of feedback loops, which is in close agreement with the insights of Hebb and colleagues, who have stressed that for learning to occur the body must be intact and able to interact with the outside world. Finally, we apply information theory to data from published studies to evaluate the robustness of the neuronal signals obtained by bypassing the body (as used for brain-machine interfaces) versus via the body to move in the world. We show that recording from a group of neurons that bypasses the body exhibits a vastly degraded level of transfer of information as compared to that of an entire brain using the body to engage in the normal execution of behaviour. We conclude that body sensations provide more than just feedback for movements; they sustain the necessary transfer of information as animals explore their environment, thereby creating associations through learning. This work has implications for the development of brain-machine interfaces used to move external devices.

Monetary reward speeds up voluntary saccades.

Past studies have shown that reward contingency is critical for sensorimotor learning, and reward expectation speeds up saccades in animals. Whether monetary reward speeds up saccades in human remains unknown. Here we addressed this issue by employing a conditional saccade task, in which human subjects performed a series of non-reflexive, visually-guided horizontal saccades. The subjects were (or were not) financially compensated for making a saccade in response to a centrally-displayed visual congruent (or incongruent) stimulus. Reward modulation of saccadic velocities was quantified independently of the amplitude-velocity coupling. We found that reward expectation significantly sped up voluntary saccades up to 30°/s, and the reward modulation was consistent across tests. These findings suggest that monetary reward speeds up saccades in human in a fashion analogous to how juice reward sped up saccades in monkeys. We further noticed that the idiosyncratic nasal-temporal velocity asymmetry was highly consistent regardless of test order, and its magnitude was not correlated with the magnitude of reward modulation. This suggests that reward modulation and the intrinsic velocity asymmetry may be governed by separate mechanisms that regulate saccade generation.

Cognitive regulation of saccadic velocity by reward prospect.

It is known that expectation of reward speeds up saccades. Past studies have also shown the presence of a saccadic velocity bias in the orbit, resulting from a biomechanical regulation over varying eccentricities. Nevertheless, whether and how reward expectation interacts with the biomechanical regulation of saccadic velocities over varying eccentricities remains unknown. We addressed this question by conducting a visually guided double-step saccade task. The role of reward expectation was tested in monkeys performing two consecutive horizontal saccades, one associated with reward prospect and the other not. To adequately assess saccadic velocity and avoid adaptation, we systematically varied initial eye positions, saccadic directions and amplitudes. Our results confirmed the existence of a velocity bias in the orbit, i.e., saccadic peak velocity decreased linearly as the initial eye position deviated in the direction of the saccade. The slope of this bias increased as saccadic amplitudes increased. Nevertheless, reward prospect facilitated velocity to a greater extent for saccades away from than for saccades toward the orbital centre, rendering an overall reduction in the velocity bias. The rate (slope) and magnitude (intercept) of reward modulation over this velocity bias were linearly correlated with amplitudes, similar to the amplitude-modulated velocity bias without reward prospect, which presumably resulted from a biomechanical regulation. Small-amplitude (≤ 5°) saccades received little modulation. These findings together suggest that reward expectation modulated saccadic velocity not as an additive signal but as a facilitating mechanism that interacted with the biomechanical regulation.

Submovement composition of head movement.

Limb movement is smooth and corrections of movement trajectory and amplitude are barely noticeable midflight. This suggests that skeletomuscular motor commands are smooth in transition, such that the rate of change of acceleration (or jerk) is minimized. Here we applied the methodology of minimum-jerk submovement decomposition to a member of the skeletomuscular family, the head movement. We examined the submovement composition of three types of horizontal head movements generated by nonhuman primates: head-alone tracking, head-gaze pursuit, and eye-head combined gaze shifts. The first two types of head movements tracked a moving target, whereas the last type oriented the head with rapid gaze shifts toward a target fixed in space. During head tracking, the head movement was composed of a series of episodes, each consisting of a distinct, bell-shaped velocity profile (submovement) that rarely overlapped with each other. There was no specific magnitude order in the peak velocities of these submovements. In contrast, during eye-head combined gaze shifts, the head movement was often comprised of overlapping submovements, in which the peak velocity of the primary submovement was always higher than that of the subsequent submovement, consistent with the two-component strategy observed in goal-directed limb movements. These results extend the previous submovement composition studies from limb to head movements, suggesting that submovement composition provides a biologically plausible approach to characterizing the head motor recruitment that can vary depending on task demand.