Multimodal integration in extraocular motoneurons

• Applicants: Professor Dr.-Ing. Stefan Glasauer; Professor Dr. Hans Straka (†)
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2015 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 274915083

• Final Report Year: 2022

Final Report Abstract

Our project aimed at studying with a combined experimental/computational approach how multimodal signals are integrated by individual sets of extraocular motoneurons to generate functionally appropriate motor commands for all types of eye movements during visuo-vestibular reflexes and locomotion. We were able to considerably advance the knowledge with respect to morpho-physiological properties of extraocular motoneurons such as those responsible for the dynamic bandwidth of neuronal computations. In particular we demonstrated that abducens motoneurons distinguish into two subgroups with respect to differential encoding of motor commands in the acceleration, velocity and position domain. In addition, we were able to characterize the synaptic organization of vestibular inputs to a specific set of extraocular motoneurons known to receive the classical push-pull synaptic signals from the vestibular sensory periphery of the two inner ears. The functional organization of visuo-motor signals mediated by extraocular motoneurons was evaluated in three separate studies where we explored the dynamic range, general sensory structure and color as well as contrast composition of the effective optokinetic stimuli. In particular, we elaborated the role of color and contrast vision for the optokinetic reflex in a cross-species comparison between Xenopus laevis and the Axolotl. In addition, by advanced modeling of recorded electrophysiological and behavioral eye motion data, we were able to demonstrate a likely reason for the rather small eye movements in Xenopus tadpoles. Accordingly, we propose that low VOR gain values reflect an optimal adaptation to sensory and motor signal variability. According to our novel hypothesis, gaze stabilization mechanisms that aim at minimizing the overall retinal image slip must consider the effects of sensory and motor noise as well as dynamic constraints of the peripheral and central components responsible for the sensory-motor processing. The computational model for optimizing retinal image slip in fact predicts gain values in part considerably smaller than unity. This allowed us to hypothesize that the low VOR gain values in e.g., elderly human subjects or recovered patients with a history of vestibular damage may be the sign of an optimization strategy given higher noise levels rather than a direct consequence of the damage. All studies were performed on the simple and tractable nervous system of Xenopus laevis tadpoles and in part also on corresponding preparations of larval Axolotl. Both experimental models offered the possibility to access all relevant sensory-motor structures for electrophysiological and optical recordings as well as behavioral analyses. The expression of locomotor activity in these semiintact preparations along with intact eyes and inner ears allowed the successful application of natural sensory stimuli in the presence and absence of locomotor activity. The previously postulated separation into motoneuronal subdivisions, e.g., of abducens motoneurons with distinct properties could in fact be clearly demonstrated for vestibular inputs and are the likely explanation of how specific computational capabilities influence the cellular decision on spatial and dynamic aspects of the neuronal output. Our project has therefore demonstrated, as initially proposed, how extraocular motoneurons generate appropriate neuronal activity patterns required for adequate gaze stabilization from multimodal signals (visual, vestibular, locomotor efference copies) and how the underlying mechanisms can be formalized in a computational model at the neuronal level.

Publications

• (2016) Prolonged vestibular stimulation induces homeostatic plasticity of the vestibulo-ocular reflex in larval Xenopus laevis. Eur. J. Neurosci. 44: 1787-1796
  Dietrich H. and Straka H.
  
• (2017) Functional organization of vestibulo-ocular responses in abducens motoneurons. J. Neurosci. 37: 4032-4045
  Dietrich H., Glasauer S. and Straka H.
  
• (2017) It’s not all black and white: Visual scene parameters influence optokinetic reflex performance in Xenopus laevis tadpoles. J. Exp. Biol. 220: 4213-4224
  Gravot C.M., Knorr A.G., Glasauer S. and Straka H.
  
• (2018) I spy with my little eye: a simple behavioral assay to test color sensitivity on digital displays. Biol. Open 7: bio035725
  Knorr A.G., Gravot C.M., Gordy C., Glasauer S. and Straka H.
  
• (2018) Pharmacological profile of vestibular inhibitory inputs to superior oblique motoneurons. J. Neurol. 265 (Suppl 1): S18-S25
  Soupiadou P., Branoner F. and Straka H.
  
• (2019) Impact of 4-aminopyridine on vestibulo-ocular reflex performance. J. Neurol. 266 (Suppl 1): S93-S100
  I Gusti Bagus M., Gordy C., Sanchez-Gonzalez R., Strupp M. and Straka H.
  
• (2021) Image motion with color contrast suffices to elicit an optokinetic reflex in Xenopus laevis tadpoles. Sci. Rep. 11: 8445
  Knorr A.G., Gravot C.M., Glasauer S. and Straka H.
  
• (2022) Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuovestibular reflexes. Nat. Comm. 13: 2957
  Bacqué-Cazenave J., Courtand G., Beraneck M., Straka H., Combes D. and Lambert F.M.
  
• (2022) Low gain values of the vestibulo-ocular reflex can optimize retinal image slip. Front. Neurol. 13: 897293
  Glasauer S. and Straka H.