In addition to their well-known role in skeletal movements, the basal ganglia control saccadic eye movements (saccades) by means of their connection to the superior colliculus (SC). The SC receives convergent inputs from cerebral cortical areas and the basal ganglia. To make a saccade to an object purposefully, appropriate signals must be selected out of the cortical inputs, in which the basal ganglia play a crucial role. This is done by the sustained inhibitory input from the substantia nigra pars reticulata (SNr) to the SC. This inhibition can be removed by another inhibition from the caudate nucleus (CD) to the SNr, which results in a disinhibition of the SC. The basal ganglia have another mechanism, involving the external segment of the globus pallidus and the subthalamic nucleus, with which the SNr-SC inhibition can further be enhanced. The sensorimotor signals carried by the basal ganglia neurons are strongly modulated depending on the behavioral context, which reflects working memory, expectation, and attention. Expectation of reward is a critical determinant in that the saccade that has been rewarded is facilitated subsequently. The interaction between cortical and dopaminergic inputs to CD neurons may underlie the behavioral adaptation toward purposeful saccades.

https://www.physiology.org/doi/pdf/10.1152/physrev.2000.80.3.953

Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements

The modern era of oculomotor research began with the advent of the chronic single-unit recording method in the late 1960s. Research carried out in the intervening years has made it possible to provide a detailed description of the saccadic command signals that are generated by motor neurons and the formation of these signals in premotor brainstem regions. These findings have been assimilated in control-systems models that simulate important behavioural features of saccades. Despite these great advances, key issues, such as the nature of the feedback signal and the location of the comparator, are unresolved and some of the factors that have impeded progress can be identified.

/pdf/the-brainstem-control-of-saccadic-eye-movements-fz5vp6ibpm.pdf

The brainstem control of saccadic eye movements

In the 16 years since we last summarized the behavior of the premotor elements that control saccades, research has revealed shortcomings in previous formulations of the control mechanisms of the brainstem saccadic burst generator. Specifically, complexities in the eye movement plant, a more detailed knowledge of the behaviors of certain bursting neurons, and previously undiscovered anatomical connections have broadened our knowledge but have generated new questions that require rethinking previous concepts. Perhaps the most crucial revelations/insights have come from studies that have implicated the superior colliculus and the midline cerebellum as crucial elements of the burst generator. In summarizing these recent findings here, we have been led to conclude that the superior colliculus issues the saccadic command and receives feedback from the brainstem burst generators, but the feedback does not control saccade size. In addition, the midline cerebellum also contains a feedback path, but only as part of a more generalized circuit that serves multiple functions.

The brainstem burst generator for saccadic eye movements: a modern synthesis.

We present a model for several early stages of the sensorimotor transformations involved in targeted arm movement. In psychophysical experiments, human subjects pointed to the remembered locations of randomly placed targets in three-dimensional space. They made consistent errors in distance, and from these errors stages in the sensorimotor transformation were deduced. When subjects attempted to move the right index finger to a virtual target they consistently undershot the distance of the more distal targets. Other experiments indicated that the error was in the sensorimotor transformation rather than in the perception of distance. The error was most consistent when evaluated using a spherical coordinate system based at the right shoulder, indicating that the neural representation of target parameters is transformed from a retinocentric representation to a shoulder-centered representation. According to the model, the error in distance results from the neural implementation of a linear approximation in the algorithm to transform shoulder-centered target parameters into a set of arm orientations appropriate for placing the finger on the target. The transformation to final arm orientations places visually derived information into a frame of reference where it can readily be combined with kinesthetically derived information about initial arm orientations. The combination of these representations of initial and final arm orientations could give rise to the representation of movement direction recorded in the motor cortex by Georgopoulos and his colleagues. Later stages, such as the transformation from kinematic (position) to dynamic (force) parameters, or to levels of muscle activation, are beyond the scope of the present model.

https://www.cambridge.org/core/services/aop-cambridge-core/content/view/S0140525X00068813

Early stages in a sensorimotor transformation

Sleepiness on the job: continuously measured EEG changes in train drivers.

We have recorded eye, head, and upper arm rotations in five healthy human subjects using the three-dimensional search coil technique. Our measurements show that the coordination of eye and head movements during gaze shifts within ± 25 deg relative to the forward direction is organized by restricting the rotatory trajectories of the two systems to almost parallel planes. These so-called “Listing planes” for eye-in-space and head-in-space rotations are workspace-oriented, not body-fixed. Eye and head trajectories in their respective planes are closely related in direction and amplitude. For pointing or grasping, the rotatory trajectories of the arm are also restricted to a workspace-oriented Listing plane. During visually guided movements, arm follows gaze, and the nine-dimensional rotatory configuration space for eye-head-arm-synergies (three degrees of freedom for each system) is reduced to a two-dimensional plane in the space of quaternion vectors.

Listing's law for eye, head and arm movements and their synergistic control.

The integrity of the paramedian pontine reticular formation (PPRF) is necessary for the generation of rapid eye movements. The main saccade-related population is of the burst type with latencies between 0 and 40 ms preceding a saccade, and they can be divided into medium- and long-lead burst neurons. Burst neurons have predominantly spatially coded movement fields in the rostral PPRF, while in the caudal PPRF they increase their burst strength in temporal coding approximately in the pulling directions of extraocular eye muscles (i.e. almost horizontal or vertical). Both neuronal populations have ipsilateral on-directions and contain long-lead burst neurons. In a quantitative analysis the firing patterns of long-lead burst neurons are compared to those of medium-lead burst neurons, which form the predominant output of the saccadic pulse generator to the motoneurons. The firing patterns of temporally coded long-lead bursters are similar to those of medium-lead bursters, except for earlier on-latencies, larger statistical fluctuations, and specializations for small or large saccades in oblique directions. The spatially coded burst neurons form a motor map of saccadic vectors. The diameter of their movement field is often about the size of the saccade vector, and they encode saccadic onset and duration. These results are consistent with a model for visual saccades in eye displacement coordinates, where the spatio-temporal recording of horizontal eye movements is effected by long-lead burst neurons in the PPRF.

Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation (PPRF)

Eye and head position, EEG, and activity of oculomotor and vestibular neurons in the brain-stem were recorded during alertness and at the transition to light sleep. Characteristic changes of firing patterns were found in many neuronal populations at the sleep-wake transition and could be related to disruption of fixation and rapid and compensatory eye movement generation. Moto-neurons decreased their firing rate by 20 to 50%, and their eye velocity coding deteriorated. Burst neurons had a significant drop in maximum firing rates and often showed continuous activity unrelated to rapid eye movements, but responded to vestibular stimuli. Pause neurons went completely silent. Neurons in the vestibular nuclei often reduced their level of activity, but still responded qualitatively unchanged to semicircular canal stimulation. In the framework of current models of oculomotor organization, the sleep-wake transition can be interpreted as a non-equilibrium phase transition which is driven by specific inputs and nonspecific activating systems.

The sleep-wake transition in the oculomotor system

The role of the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) in generating the vertical and torsional components of rapid eye movements was examined. The on-directions of burst neurons in the riMLF of alert Rhesus monkeys were obtained during quick phase nystagmus in three dimensions. The distinguishing feature of these burst neurons was the torsional component of their on-directions; neurons on the right side exhibited a clockwise component, from the point of view of the subject, while those on the left had a counterclockwise component. Vertical components could have up or down directions. This organization was verified by means of unilateral reversible inactivation of the riMLF using Muscimol. An injection in the right riMLF impaired the generation of quick phases with clockwise components while one on the left impaired counterclockwise components.

On the generation of vertical and torsional rapid eye movements in the monkey.

We have tested Listing's law in the monkey using the dual search coil technique to record 3-dimensional eye positions during smooth pursuit and during spontaneous eye movements in the light. Our results indicate that during smooth pursuit the eye positions obey Listing's law with a least the same accuracy as during spontaneous eye movements or during periods of fixations.

K. Hepp

Papers

Listing's law for eye, head and arm movements and their synergistic control.

Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation (PPRF)

The sleep-wake transition in the oculomotor system

On the generation of vertical and torsional rapid eye movements in the monkey.

Smooth pursuit eye movements obey Listing's law in the monkey.