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Ontogenetic development of gaze-stabilizing reflexes in Xenopus laevis

By Haike Dietrich (25.01.2012)

The topic of my current study deals with the neuroscientific investigation of gaze-stabilizing reflexes, which are essential to maintain stable vision during locomotion. During my master thesis I focused on the cellular and network properties of the vestibulo-ocular reflex (VOR) circuitry, which transfers vestibular information of head motion into motor commands to move the eyes in the opposite direction, respectively. The resulting fast eye movements compensate passive head movements, stabilize gaze and thus maintain a stable visual image of the object of interest. The evolutionary conservation of the VOR allows studying basic functional and developmental principles of the organization in relatively simple animal models, such as the african clawed frog (Xenopus laevis).

Accurate perception of the visual world is essential for an animal’s survival and effective motor behavior. All vertebrates have the necessity of stabilizing retinal images in order to perceive the surrounding environment during their own locomotor actions, whether running, swimming or flying. As a consequence of self-generated head and body movements the retinal images are displaced with a resultant degradation of visual information processing. In order to maintain visual acuity, retinal image drift must be counteracted by compensatory eye and/or head-adjustments that are elicited by fast, reflex-like motor programs that originate from sensory-motor transformations of vestibular, visual (optokinetic) and neck proprioceptive signals. The visual system is relatively slow in comparison to the potential velocity of the animal’s movements, while proprioceptive neck signals are spatially imprecise, thus rendering both sensory modalities inadequate for supporting gaze stabilization. In contrast, vestibular signals, which are detected by sets of inner ear organs, cover a wide dynamic spectrum that ranges from tonic to high frequency head movements.

These sensory signals are transformed and integrated in frequency-tuned second-order vestibular neurons and mediated by a short-latency pathway onto evolutionarily conserved sets of extraocular motor nuclei. The extraocular motoneurons thus carry a range of motor commands to the corresponding eye muscles that generate adequate compensatory eye movements. Accordingly, the vestibulo-ocular reflex (VOR) comprises a reliable mechanism for transforming linear as well as angular acceleration of the head into reactive motor commands to stabilize the gaze. The VOR is supplemented by the optokinetic reflex (OKR) that is activated by large-field image motion and helps stabilizing the gaze by compensating the residual image slip after the VOR has been activated. Accordingly, during self-locomotion, both VOR and OKR act together for successful image stabilization. In addition, efference copies of neural signals produced by locomotor pattern-generating circuitry within the spinal cord are conveyed to the brainstem extraocular motor nuclei during rhythmic, stereotyped locomotion such as swimming in frog tadpoles. These intrinsic signals also generate anticipatory counteracting eye movements in response to the predicted head or body movement and thereby contribute to the gaze stabilization during self-motion.

In the framework of my master project, I have started to investigate the functional organization of extraocular motor units as well as the pharmacology of synaptic inputs from the bilateral vestibular nuclei to a subset of motoneurons that innervate a particular eye muscle. The experiments were carried out in different developmental larval stages of the clawed frog Xenopus laevis, which offers the possibility to evaluate potential changes in response dynamics and transmitter activation during ontogeny. Due to changing locomotor behavior and life style that is associated with the amphibian metamorphosis this experimental model is ideally suited for developmental studies that attempt to investigate plastic changes that are correlated with eco-physiological alterations such as different locomotor strategies. Moreover, this model organism allows employing a range of semi-intact and isolated preparations for morpho-physiological in vitro experimentation, thereby facilitating the accessibility that is necessary for probing cellular and network function in vitro, which in other vertebrates is only possible in vivo.

One of the major results of the current study is a clear differentiation of individual extraocular motor units that innervate the lateral rectus eye muscle according to activation threshold, discharge regularity and response dynamics. Thus, a subset of abducens motoneurons is tonically active, with low stimulus thresholds and a phase relation that is aligned with the head position during passive head movements. In contrast, another set of motoneurons has a rather irregular resting rate, high thresholds and an evoked activity that is more aligned with head velocity. Thus, extraocular motoneurons appear to form discrete frequency-tuned signaling pathways for different types of eye motion. In addition, the pharmacological approach has revealed distinct contributions of different glutamate receptor subtypes as well as of glycine in the mediation of a crossed vestibular excitation and uncrossed vestibular inhibition, respectively, compatible with the conserved organization of the VOR in vertebrates. Ongoing experiments in Xenopus laevis will reveal developmental changes in the functional organization of the different motor units that are involved in the mediation of spatio-temporally appropriate eye movements during different types of locomotor strategies and dynamics.

  • Since 10/2011
  • Ph.D. thesis with Prof. Dr. Hans Straka, Graduate School of Systemic Neurosciences, LMU München
  • 10/2009 – 09/2011
  • M.Sc. study of Neuroscience, LMU München
  • Master thesis with Prof. Dr. Hans Straka, Department Biology II, LMU München
  • 10/2006 - 09/2009
  • B.Sc. study of Biology, LMU München

Berufliche Erfahrung
  • 10/2010
  • Tutor of the Neurophysiology practical course for master students, Graduate School of Systemic Neurosciences, LMU München
  • 04/ 2008 – 07/2008
  • Tutor of the Basic Course in Zoology, Department of Zoology, Technische Universität München