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We recently developed a biomimetic robotic eye with six independent tendons, each controlled by their own rotatory motor, and with insertions on the eye ball that faithfully mimic the biomechanics of the human eye. We constructed an accurate physical computational model of this system, and learned to control its nonlinear dynamics by optimising a cost that penalised saccade inaccuracy, movement duration, and total energy expenditure of the motors. To speed up the calculations, the physical simulator was approximated by a recurrent neural network (NARX). We showed that the system can produce realistic eye movements that closely resemble human saccades in all directions: their nonlinear main-sequence dynamics (amplitude-peak eye velocity and duration relationships), cross-coupling of the horizontal and vertical movement components leading to approximately straight saccade trajectories, and the 3D kinematics that restrict 3D eye orientations to a plane (Listing’s law). Interestingly, the control algorithm had organised the motors into appropriate agonist-antagonist muscle pairs, and the motor signals for the eye resembled the well-known pulse-step characteristics that have been reported for monkey motoneuronal activity. We here fully analyse the eye-movement properties produced by the computational model across the entire oculomotor range and the underlying control signals. We argue that our system may shed new light on the neural control signals and their couplings within the final neural pathways of the primate oculomotor system, and that an optimal control principle may account for a wide variety of oculomotor behaviours. The generated data are publicly available at https://data.ru.nl/collections/di/dcn/DSC_626870_0003_600.

Abstract The midbrain superior colliculus is a crucial sensorimotor stage for programming and generating saccadic eye-head gaze shifts. Although it is well established that superior colliculus cells encode a neural command that specifies the amplitude and direction of the upcoming gaze-shift vector, there is controversy about the role of the firing-rate dynamics of these neurons during saccades. In our earlier work, we proposed a simple quantitative model that explains how the recruited superior colliculus population may specify the detailed kinematics (trajectories and velocity profiles) of head-restrained saccadic eye movements. We here show that the same principles may apply to a wide range of saccadic eye-head gaze shifts with strongly varying kinematics, despite the substantial nonlinearities and redundancy in programming and execute rapid goal-directed eye-head gaze shifts to peripheral targets. Our findings could provide additional evidence for an important role of the superior colliculus in the optimal control of saccades.

A cochlear implant (CI) is a neurotechnological device that restores total sensorineural hearing loss. It contains a sophisticated speech processor that analyzes and transforms the acoustic input. It distributes its time-enveloped spectral content to the auditory nerve as electrical pulsed stimulation trains of selected frequency channels on a multi-contact electrode that is surgically inserted in the cochlear duct. This remarkable brain interface enables the deaf to regain hearing and understand speech. However, tuning of the large (>50) number of parameters of the speech processor, so-called “device fitting,” is a tedious and complex process, which is mainly carried out in the clinic through ‘one-size-fits-all’ procedures. Current fitting typically relies on limited and often subjective data that must be collected in limited time. Despite the success of the CI as a hearing-restoration device, variability in speech-recognition scores among users is still very large, and mostly unexplained. The major factors that underly this variability incorporate three levels: (i) variability in auditory-system malfunction of CI-users, (ii) variability in the selectivity of electrode-to-auditory nerve (EL-AN) activation, and (iii) lack of objective perceptual measures to optimize the fitting. We argue that variability in speech recognition can only be alleviated by using objective patient-specific data for an individualized fitting procedure, which incorporates knowledge from all three levels. In this paper, we propose a series of experiments, aimed at collecting a large amount of objective (i.e., quantitative, reproducible, and reliable) data that characterize the three processing levels of the user’s auditory system. Machine-learning algorithms that process these data will eventually enable the clinician to derive reliable and personalized characteristics of the user’s auditory system, the quality of EL-AN signal transfer, and predictions of the perceptual effects of changes in the current fitting.

Abstract Previous studies have indicated that the location of a large neural population in the Superior Colliculus (SC) motor map specifies the amplitude and direction of the saccadic eye-movement vector, while the saccade trajectory and velocity profile are encoded by the population firing rates. We recently proposed a simple spiking neural network model of the SC motor map, based on linear summation of individual spike effects of each recruited neuron, which accounts for many of the observed properties of SC cells in relation to the ensuing eye movement. However, in the model, the cortical input was kept invariant across different saccades. Electrical microstimulation and reversible lesion studies have demonstrated that the saccade properties are quite robust against large changes in supra-threshold SC activation, but that saccade amplitude and peak eye-velocity systematically decrease at low input strengths. These features were not accounted for by the linear spike-vector summation model. Here we show that the model’s input projection strengths and intra-collicular lateral connections can be tuned to generate saccades and neural spiking patterns that closely follow the experimental results.

Abstract Several studies have proposed that an optimal speed-accuracy tradeoff underlies the stereotyped relationship between amplitude, duration and peak velocity of saccades (main sequence). To test this theory, we asked 8 participants to make saccades to Gaussian-blurred spots and manipulated the task’s accuracy constraints by varying target size (1, 3, and 5°). The largest targets indeed yielded more endpoint scatter (and lower gains) than the smallest targets, although this effect subsided with target eccentricity. The main sequence depended on several interacting factors: saccade latency, saccade gain and target size. Early saccades, which were faster than amplitude-matched late saccades, followed the target-size dependency one would expect from a speed-accuracy tradeoff process. They had higher peak velocities and shorter durations for larger targets than for smaller targets. For late saccades, however, the opposite was found. Deviations from the main sequence also covaried with saccade gain, in line with the idea that motor noise underlies part of the endpoint variability. Thus, our data provide partial evidence that the saccadic system weighs the detrimental effects of motor noise on saccade accuracy against movement duration and speed, but other factors also modulate the kinematics. We discuss the possible involvement of parallel saccade pathways to account for our findings.

IntroductionTo reorient gaze (the eye’s direction in space) towards a target is an overdetermined problem, as infinitely many combinations of eye- and head movements can specify the same gaze-displacement vector. Yet, behavioral measurements show that the primate gaze-control system selects a specific contribution of eye- and head movements to the saccade, which depends on the initial eye-in-head orientation. Single-unit recordings in the primate superior colliculus (SC) during head-unrestrained gaze shifts have further suggested that cells may encode the instantaneous trajectory of a desired straight gaze path in a feedforward way by the total cumulative number of spikes in the neural population, and that the instantaneous gaze kinematics are thus determined by the neural firing rates. The recordings also indicated that the latter is modulated by the initial eye position. We recently proposed a conceptual model that accounts for many of the observed properties of eye-head gaze shifts and on the potential role of the SC in gaze control.MethodsHere, we extend and test the model by incorporating a spiking neural network of the SC motor map, the output of which drives the eye-head motor control circuitry by linear cumulative summation of individual spike effects of each recruited SC neuron. We propose a simple neural mechanism on SC cells that explains the modulatory influence of feedback from an initial eye-in-head position signal on their spiking activity. The same signal also determines the onset delay of the head movement with respect to the eye. Moreover, the downstream eye- and head burst generators were taken to be linear, as our earlier work had indicated that much of the non-linear main-sequence kinematics of saccadic eye movements may be due to neural encoding at the collicular level, rather than at the brainstem.Results and discussionWe investigate how the spiking activity of the SC population drives gaze to the intended target location within a dynamic local gaze-velocity feedback circuit that yields realistic eye- and head-movement kinematics and dynamic SC gaze-movement fields.