As animals forage for food and water or evade predators, they must rapidly decide what visual features in the environment deserve attention. In vertebrates, this visuomotor computation is implemented within the neural circuits of the optic tectum (superior colliculus in mammals). However, the mechanisms by which tectum decides whether to approach or evade remain unclear, and also which neural mechanisms underlie this behavioral choice. To address this problem, we used an eye–brain–spinal cord preparation to evaluate how the lamprey responds to visual inputs with distinct stimulus-dependent motor patterns. Using ventral root activity as a behavioral readout, we classified 2 main types of fictive motor responses: (i) a unilateral burst response corresponding to orientation of the head toward slowly expanding or moving stimuli, particularly within the anterior visual field, and (ii) a unilateral or bilateral burst response triggering fictive avoidance in response to rapidly expanding looming stimuli or moving bars. A selective pharmacological blockade revealed that the brainstem-projecting neurons in the deep layer of the tectum in interaction with local inhibitory interneurons are responsible for selecting between these 2 visually triggered motor actions conveyed through downstream reticulospinal circuits. We suggest that these visual decision-making circuits had evolved in the common ancestor of vertebrates and have been conserved throughout vertebrate phylogeny.

Citation: Wibble T, Pansell T. Vestibular eye movements are heavily impacted by visual motion and are sensitive to changes in visual intensities.

Gaze stabilization compensates for movements of the head or external environment to minimize image blurring. Multisensory information stabilizes the scene on the retina via the vestibulo-ocular (VOR) and optokinetic (OKR) reflexes. While the organization of neuronal circuits underlying VOR is well-described across vertebrates, less is known about the contribution and evolution of the OKR and the basic structures allowing visuo-vestibular integration. To analyze these neuronal pathways underlying visuo-vestibular integration, we developed a setup using a lamprey eye-brain-labyrinth preparation, which allowed coordinating electrophysiological recordings, vestibular stimulation with a moving platform, and visual stimulation via screens. Lampreys exhibit robust visuo-vestibular integration, with optokinetic information processed in the pretectum that can be downregulated from tectum. Visual and vestibular inputs are integrated at several subcortical levels. Additionally, saccades are present in the form of nystagmus. Thus, all basic components of the visuo-vestibular control of gaze were present already at the dawn of vertebrate evolution.

Purpose Acceleration plays a great impact on the vestibular system, but is attributed little influence over vision. This study aims to explore how visual and vestibular acceleration affect roll-plane oculomotor responses, including their addiative effect. Methods Seated in a mechanical sled, 13 healthy volunteers (7 men, 6 women; mean age 25 years) were exposed to a series of visual (VIS) optokinetic, vestibular (VES) whole-body, and combined (VIS + VES) rotations. This was carried out at two acceleration intensities. Subjects wore a video-based eye tracker, enabling analysis of torsional and skewing eye movement responses, which were used to evaluate the individual response to each trial. The tracker also contained accelerometers allowing head tracking. Results Both ocular torsion and vertical skewing were sensitive to acceleration intensities for VES and VIS + VES. For VIS only, skewing exhibited such a response. An increased acceleration yielded a decreased torsion-skewing ratio for VIS, explained by the change in skewing, but remained unchanged for VES and VIS + VES. Torsion exhibited particularly reliable summative effect, yielding a relative contribution of 32% VIS and 75% VES during low acceleration, and 19% and 85%, respectively, during high acceleration. Conclusions The change in the skewing response to different intensities indicates that the visual system is more sensitive to visual accelerations than previously described. Eye movements showed reliable summative effects, indicating a robust visual-vestibular integration that indicates their integrative priorities for each acceleration, with the visual system being more involved during low accelerations. Such objective quantifications could hold clinical utility when assessing sensory mismatch in vertiginous patients.