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

• Published in: Journal of neurophysiology Vol. 116; no. 4; pp. 1956 - 1985
• Main Authors: Haji-Abolhassani, Iman, Guitton, Daniel, Galiana, Henrietta L
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01.10.2016
• Subjects: Action Potentials; Animals; Brain Stem - anatomy & histology; Brain Stem - physiology; Cats; Cerebellum - anatomy & histology; Cerebellum - physiology; Control of Movement; Eye Movements - physiology; Haplorhini; Head Movements - physiology; Humans; Models, Neurological; Neural Networks (Computer); Neural Pathways - anatomy & histology; Neural Pathways - physiology; Neurons - physiology; Nonlinear Dynamics; saccade and fixation; eye-head coordination; vestibular compensation; network modeling; common error feedback; gaze shifts
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00605.2015

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.