Nerve cells transmit information by means of rapidly changing electrical signals. Electrophysiological techniques allow for the measurement of these signals with sub-millisecond precision. We perform electrophysiological recordings from single cells and nerve fibers in the fly visual system to measure their neural responses to visual stimuli.
Using Drosophila as a model system we can combine the precision of electrophysiological measurements with the powerful genetic toolbox available for this organism. Thereby we can selectively manipulate neural populations and assess the effect of this manipulation on the neural responses of downstream cells. In particular we use genetic tools to either silence (shibirets, TNT, Kir2.1) or optogenetically activate (ChR2) candidate cells involved in motion detection. We perform in vivo patch clamp recordings from genetically manipulated flies while presenting visual stimuli with a custom built LED arena.
This approach revealed that lamina neurons L1 and L2 are the major input lines to the motion detection circuit. Whereas L1 transmits information about brightness increments (ON pathway) only, L2 signals information about brightness decrements (OFF pathway) to downstream neurons (Joesch et al., 2010). Subsequently, these findings led to the discovery that visual motion is detected by two parallel motion detectors, one within each pathway (Eichner et al., 2011; Maisak et al., 2013). The output elements of the ON and OFF pathways are constituted by the T4 and T5 cells, respectively (Maisak et al., 2013). T4 and T5 cells in turn synapse onto LPTCs which pool information from many of these “elementary motion detectors” to generate complex receptive fields (Joesch et al., 2008; Schnell et al., 2010; Schnell et al., 2012).
Tangential cells in the lobula plate do not work independently but possess multiple chemical and electrical connections with each other to form an intricate neural network (Borst & Weber, 2011). These interactions have been studied by performing dual recordings, dye-coupling and laser ablation experiments in blow flies. A major outcome of these studies is that the receptive fields of LPTCs are not only determined by input from retinotopic motion detectors, but are broadened and shaped by lateral interactions between LPTCs themselves.
How is the information that is extracted by the sensory systems transformed into appropriate motor output? To answer this question with respect to optomotor behavior we perform electrophysiological recordings from descending motor neurons that control head movements. Interestingly, some motor neurons do not only respond to visual stimulation, but also to sensory input e.g. from wind-sensitive organs and halteres (Haag et al., 2010). Thus motor neurons integrate multimodal sensory information to trigger appropriate behavior only when visual information is relevant to the fly.
Borst, A. & Weber, F. Neural action fields for optic flow based navigation: a simulation study of the fly lobula plate network. PLoS ONE 6, e16303 (2011).
Borst, A. & Haag, J. Optic flow processing in the cockpit of the fly. in Invertebrate neurobiology (eds. North, G. & Greenspan, R. J.) (CSHL-Press, 2007).
Eichner, H., Joesch, M., Schnell, B., Reiff, D. F. & Borst, A. Internal structure of the fly elementary motion detector. Neuron 70, 1155–1164 (2011).
Haag, J., Wertz, A. & Borst, A. Central gating of fly optomotor response. Proc. Natl. Acad. Sci. USA (2010). doi:10.1073/pnas.1009381107
Joesch, M., Weber, F., Eichner, H. & Borst, A. Functional specialization of parallel motion detection circuits in the fly. J. Neurosci. 33, 902–905 (2013).
Joesch, M., Schnell, B., Raghu, S. V., Reiff, D. F. & Borst, A. ON and OFF pathways in Drosophila motion vision. Nature 468 , 300–304 (2010).
Joesch, M., Plett, J., Borst, A. & Reiff, D. F. Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster. Curr. Biol. 18, 368–374 (2008).
Maisak, M. S. et al. A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212–216 (2013).
Schnell, B., Raghu, S. V., Nern, A. & Borst, A. Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J. Comp. Physiol. A 198, 389–395 (2012).
Schnell, B. et al. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103, 1646–1657 (2010).