Modeling eye-head gaze shifts in multiple contexts without motor planning

Abstract

During gaze shifts, the eyes and head collaborate to rapidly capture a target (saccade) and fixate it. Accordingly, models of gaze shift control should embed both saccadic and fixation modes and a mechanism for switching between them. We demonstrate a model in which the eye and head platforms are driven by a shared gaze error signal. To limit the number of free parameters, we implement a model reduction approach in which steady-state cerebellar effects at each of their projection sites are lumped with the parameter of that site. The model topology is consistent with anatomy and neurophysiology, and can replicate eye-head responses observed in multiple experimental contexts: 1) observed gaze characteristics across species and subjects can emerge from this structure with minor parametric changes; 2) gaze can move to a goal while in the fixation mode; 3) ocular compensation for head perturbations during saccades could rely on vestibular-only cells in the vestibular nuclei with postulated projections to burst neurons; 4) two nonlinearities suffice, i.e., the experimentally-determined mapping of tectoreticular cells onto brain stem targets and the increased recruitment of the head for larger target eccentricities; 5) the effects of initial conditions on eye/head trajectories are due to neural circuit dynamics, not planning; and 6) "compensatory" ocular slow phases exist even after semicircular canal plugging, because of interconnections linking eye-head circuits. Our model structure also simulates classical vestibulo-ocular reflex and pursuit nystagmus, and provides novel neural circuit and behavioral predictions, notably that both eye-head coordination and segmental limb coordination are possible without trajectory planning.

Two Distinct Types of Eye-Head Coupling in Freely Moving Mice

“…The vestibular pathways conveying information about head tilt and head rotation are known to be crucial for gaze stabilization (see [62] for a recent review), while the superior colliculus is a key structure for controlling head and eye movements in primates [63,64] and rodents [21,65,66]. Previous experimental and computational work has shown how the vestibular system and superior colliculus are part of an extensive network, including areas in the brainstem and cerebellum, that enables coordinated head and eye movements (e.g., [36,[67][68][69]).…”

Do postural constraints affect eye, head, and arm coordination?

“…These signals can be utilized for postural control (Strupp et al 2003) with the maintenance of eye position (and visual stability) occurring via VOR. However, if postural instability is present in addition to an active head movement (much like during activities of daily living), eye-head stabilizing mechanisms such as the VOR are likely to interfere with the production of a correct gaze response (Daye et al 2014;Haji-Abolhassani et al 2016). Therefore, integration of whole body posture with active eye and head movements must be required to ensure that the timing of individual segment rotations provides accurate gaze shifts.…”

“…Further downstream, supraspinal centers within the brainstem integrate both descending and ascending signals during voluntary reaching (Schepens et al 2008;Stapley et al 2010) and other postural activities (Inglis et al 1994;Stapley and Drew 2009). In fact, specific nuclei of the reticular formation (pontine nucleus pars caudalis and pars oralis) are known to house neurons of the saccadic burst generators (e.g., short latency excitatory burst neurons; Haji-Abolhassani et al 2016) and those that are modulated in the control of posture and movement (Schepens et al 2008). These neuronal populations are responsible for the initiation of gaze shifts and are heavily linked to the production of feed-forward-driven APAs (Sakai et al 2009;Schepens and Drew 2004).…”

Eye-Head Coordination in 31 Space Shuttle Astronauts during Visual Target Acquisition

“…Our subjects’ eye and head movements before spaceflight were comparable to eye movements that were measured in ground-based subjects using EOG and eye coil techniques 9 , 22 , 23 . Current models of eye-head coordination postulate that a vestibular signal serves as an integral component of saccadic spatial programming during head-free gaze shifts 22 – 26 . In these models, the desired gaze position is compared to an internal representation of the actual gaze position.…”