Background

Aquatic vertebrates use a mechano-sensory system to decipher currents, obstacles, and active movements of, for instance, predators or prey in the water body. The morphology of peripheral receptors and the central organization of this lateral line system have much in common with the vertebrate auditory system. Therefore, it was hypothesized that the principles of information processing of both systems are closely related. Similar to acoustic objects, for instance, water object representations along the central lateral line pathway must be generated from patterns of particle motion across peripheral receivers. Thus, the lateral line offers insight into key features of neural computation beyond a specific sensory system. However, while vast progress has been made in auditory neuroscience, less is known of both peripheral and central processing of the lateral line system. Notably, the lateral line sensory system permits to apply unique research concepts to investigate neural computation in the vertebrate CNS, and our laboratory aims to tap the specific advantages of the model system.

Animal model

To this end, central processing of water surface waves is explored in the lateral line system of the African clawed frog. Xenopus laevis is a prominent animal model that is established in biomedical research, and it depends on wave signals on the water surface for insect prey discrimination, recognition, and localization. Its lateral line system provides (i) an arrangement of largely accessible superficial receptors. These receptors and their afferents offer good conditions to locally study the nature of stimuli and sensory transduction, as well as peripheral neuroanatomy. The peripheral morphology of the Xenopus lateral line also permits straightforward and selective manipulation of sensory inputs, receptors, and afferents that drive central processing. (ii) Central processing of the lateral line is organized in parallel fashion to the auditory pathway a fact that aids the stereotactic approach on the neurophysiology and neuroanatomy of the system. (iii) Xenopus lateral line system has been subject to computational modelling studies which provide testable predictions for neurophysiology, neuroanatomy, and behavioural research. (iv) Xenopus, unlike other potential models, has successfully been conditioned to distinguish between incoming lateral line stimuli. That is, centrally observed neural processing can also be related to behavioural paradigms. In consequence, advancing neurophysiology and neuroanatomy projects of our laboratory can feed back to, and are inspired by, unfolding modeling and behavioral studies of our collaborators.

Experimental approach

Our laboratory has developed the expertise to approach the proposed model system by studies on the peripheral and central neuroanatomy and neurophysiology. Multielectrode extracellular recordings in a variety of brainstem and midbrain nuclei of the central lateral line pathway serve to establish the neurons response characteristics to water waves in terms of frequency, amplitude, and spatial tuning. Responses to simple and complex surface wave stimuli recorded at different central levels are inter-individually assigned to distinct nuclei in a newly developed brain atlas system of Xenopus. Hydrodynamic wave stimuli are continuously monitored by confocal optical sensors and can be correlated to observed neural activity. With regard to neural filters along the lateral line pathway, two hypotheses are put forward. (i) The midbrain of Xenopus expresses entities that concern feature detection and localisation of wave sources on the water surface like insect prey. (ii) These functional divisions cause a systematic distribution of response properties across neural substructures. So far, our results suggest midbrain subdivisions with respect to processing of wave stimulus timing, frequency and amplitude. Our future research aims to further unlock the rules of processing that govern the formation of neural filter properties along the central lateral line pathway. A main concern is to relate computational principles of the lateral line to codes observed in other sensory systems.

Branoner F, Zhivko Z, Ziehm U & Behrend O (2012) Central representation of spatial and temporal surface wave parameters in the African clawed frog. Journal of Comparative Physiology A, Sensory, Neural, and Behavioural Physiology, 198: 797–815.

Zhivkov Z, Branoner F, Ziehm U, Schuldt C, Behrend O (2009) Neurophysiology and neuroanatomy of the lateral line system in Xenopus laevis. Proceedings of the 8th Göttingen Meeting of the German Neuroscience Society, T17-11C.

Behrend O, Branoner F & Ziehm U (2008) Lateral line units in the amphibian brain could integrate wave curvatures. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioural Physiology, 194, 8, 777 783.

Pecka M, Brand A, Behrend O & Grothe B (2008) Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. Journal of Neuroscience, 28, 6914 6925.

Branoner F, Ziehm U, Zhivkov Z, Schuldt C & Behrend O (2008) Central lateral line responses to concentric water surface waves propagating over 3 test distances effects of deviating wave curvatures. 6th Forum of European Neuroscience, FENS Abstracts, 4, 223.2.

Branoner F, Ziehm U, Zhivkov Z & Behrend O (2008) Lateral line responses integrate the wave curvature. Abstracts of the Berlin Neuroscience Forum, 33, 12.

Zhivkov Z, Schuldt C, Branoner F, Behrend O (2008) Peripheral and central organization of the lateral line pathway in Xenopus laevis. Abstracts of the Berlin Neuroscience Forum, 68, 107.

Behrend O & Grothe B (2007) Auditory processing in the bat medial superior olive. In The Senses: A Comprehensive Reference, Volume 3, Audition. Dallos P, Oertel D (eds). Academic Press, Oxford, pp. 701 718.

Ziehm U, Branoner F & Behrend O (2007) Water wave curvatures and amplitudes affect lateral line responses: a source distance code. Abstracts of the 8th International Congress of Neuroethology, 142 143, 178.

Branoner F, Ziehm U & Behrend O (2007) Lateral line responses to distant objects on the water surface integrate the wave front curvature and amplitude. 7th IBRO World Congress of Neuroscience, 144, 201.

Behrend O**, Branoner F, Zhivkov Z & Ziehm U (2006) Neural responses to water surface waves in the midbrain of the aquatic predator Xenopus laevis laevis. European Journal of Neuroscience, 23, 729 744.

Ziehm U, Branoner F, Zhivkov Z & Behrend O (2006) Neural representation of surface wave parameters in the aquatic predator Xenopus laevis. Abstracts of the Berlin Neuroscience Forum, 74, 114.

Behrend O, Branoner F, Zhivkov Z & Ziehm U (2006) Central processing of water surface waves in the aquatic predator Xenopus laevis laevis. 5th Forum of European Neuroscience, FENS Abstracts, 444, 180.

Behrend O, Branoner F, Zhivkov Z & Ziehm U (2005) Central processing of water surface waves in the African clawed frog. Abstracts of the 3rd Symposium Juniorprofessur.

Branoner F, Zhivkov Z, Ziehm U & Behrend O (2005) Neural responses to water surface waves in the midbrain of the african clawed frog. Proceedings of the Australian Neuroscience Society, 96, 173.