The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement-based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + r, where FR is firing rate, E and are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or "slide" (FR = b + kE + r + uE - c), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients (r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias (b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.

Burst-tonic (BT) neurons in the prepositus hypoglossi and adjacent medial vestibular nuclei are important elements of the neural integrator for horizontal eye movements. While the metrics of their discharges have been studied during conjugate saccades (where the eyes rotate with similar dynamics), their role during disjunctive saccades (where the eyes rotate with markedly different dynamics to account for differences in depths between saccadic targets) remains completely unexplored. In this report, we provide the first detailed quantification of the discharge dynamics of BT neurons during conjugate saccades, disjunctive saccades, and disjunctive fixation. We show that these neurons carry both significant eye position and eye velocity-related signals during conjugate saccades as well as smaller, yet important, "slide" and eye acceleration terms. Further, we demonstrate that a majority of BT neurons, during disjunctive fixation and disjunctive saccades, preferentially encode the position and the velocity of a single eye; only few BT neurons equally encode the movements of both eyes (i.e., have conjugate sensitivities). We argue that BT neurons in the nucleus prepositus hypoglossi/medial vestibular nucleus play an important role in the generation of unequal eye movements during disjunctive saccades, and carry appropriate information to shape the saccadic discharges of the abducens nucleus neurons to which they project.

Although numerous investigations have probed the status of the vestibuloocular (VOR) during gaze shifts, its exact status remains strangely elusive. The goal of the present study was to precisely evaluate the dynamics of VOR suppression immediately before, throughout, and just after gaze shifts. A torque motor was used to apply rapid (100 degrees/s), short-duration (20-30 ms) horizontal head perturbations in three Rhesus monkeys. The status of the VOR elicited by this transient head perturbation was first compared during 15, 40, and 60 degrees gaze shifts. The level of VOR suppression just after gaze-shift onset (40 ms) increased with gaze-shift amplitude in two monkeys, approaching values of 80 and 35%. In contrast, in the third monkey, the VOR was not significantly attenuated for all gaze-shift amplitudes. The time course of VOR attenuation was then studied in greater detail for all three monkeys by imposing the same short-duration head perturbations 40, 100, and 150 ms after the onset of 60 degrees gaze shifts. Overall we found a consistent trend, in which VOR suppression was maximal early in the gaze shift and progressively recovered to reach normal values near gaze-shift end. However, the high variability across subjects prevented establishing a unifying description of the absolute level and time course of VOR suppression during gaze shifts. We propose that differences in behavioral strategies may account, at least in part, for these differences between subjects.

In this report, we provide the first characterization of abducens nucleus neuron (ABN) discharge dynamics during horizontal disjunctive saccades. These movements function to rapidly transfer the visual axes between targets located at different eccentricities and depths. Our primary objective was to determine whether the signals carried by ABNs during these movements are appropriate to drive the motion of the eye to which they project. We also asked whether ABNs encode eye movements similarly during disjunctive saccades and disjunctive fixation. To address the first objective we 1) assessed whether we could predict the discharge dynamics of individual neurons during disjunctive saccades based on their discharge properties during conjugate saccades and 2) directly estimated the sensitivity of individual neurons to either the ipsilateral/contralateral eye or the conjugate/vergence position and velocity using bootstrap statistics. Our main finding was that during disjunctive saccades in the direction ipsilateral to the recording site (ON-direction), the majority of ABNs preferentially encoded the velocity and the position of the ipsilateral eye. The remaining neurons predominantly encoded the conjugate motion of the eyes (i.e., were equally sensitive to the motion of both eyes). Generally, ipsilateral/contralateral eye based models better described neuronal discharges than conjugate/vergence based models, yet both model structures yielded similar conclusions. Moreover, the preferred eye of individual neurons based on their position and velocity sensitivities were generally well matched. We also found that for saccades in the OFF-direction, the pausing behavior of ABNs was similar during conjugate and disjunctive saccades, with the exception that for movements of small amplitudes, more ABNs paused during conjugate saccades. Finally, we found that putative motoneurons and internuclear neurons encoded ON- and OFF-direction disjunctive saccades in a similar manner. To address our second objective, we compared the discharge properties of individual ABNs during disjunctive saccades and disjunctive fixation. Good coherence was observed between the preferred eye of individual ABNs during the two behaviors. Taken together, our results indicate that although individual ABNs can encode the motion of both eyes to various degrees, the population drive of ABNs accounts for most of the movement of the ipsilateral eye during disjunctive saccades and disjunctive fixation.

Simple activities like picking up the morning newspaper or catching a ball require finely coordinated movements of multiple body segments. How our brain readily achieves such kinematically complex yet remarkably precise multijoint movements remains a fundamental and unresolved question in neuroscience. Many prevailing theoretical frameworks ensure multijoint coordination by means of integrative feedback control. However, to date, it has proven both technically and conceptually difficult to determine whether the activity of motor circuits is consistent with integrated feedback coding. Here, we tested this proposal using coordinated eye-head gaze shifts as an example behavior. Individual neurons in the premotor network that command saccadic eye movements were recorded in monkeys trained to make voluntary eye-head gaze shifts. Head-movement feedback was experimentally controlled by unexpectedly and transiently altering the head trajectory midflight during a subset of movements. We found that the duration and dynamics of neuronal responses were appropriately updated following head perturbations to preserve global movement accuracy. Perturbation-induced increases in gaze shift durations were accompanied by equivalent changes in response durations so that neuronal activity remained tightly synchronized to gaze shift offset. In addition, the saccadic command signal was updated on-line in response to head perturbations applied during gaze shifts. Nearly instantaneous updating of responses, coupled with longer latency changes in overall discharge durations, indicated the convergence of at least two levels of feedback. We propose that this strategy is likely to have analogs in other motor systems and provides the flexibility required for fine-tuning goal-directed movements.