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1 Department of Biology, Carl von Ossietzky University, Oldenburg, Germany
2 Department of Biology, Carl von Ossietzky University, Oldenburg, Germany; Systems Neuroscience Lab E, The Salk Institute, La Jolla, California, United States
3 Theoretical Neurophysics, University of Bremen, Bremen, Germany
* To whom correspondence should be addressed. E-mail: andreas.thiel{at}uni-oldenburg.de.
We investigate the capability of turtle retinal ganglion cell (RGC) ensembles to simultaneously encode multiple aspects of visual motion, namely speed, direction, and acceleration of moving patterns. Bayesian stimulus reconstruction reveals that the instantaneous firing rates of RGCs contain information about all of these stimulus properties. Stimulus velocity is mainly encoded by steady-state firing rates, while acceleration can be reconstructed from transient components in RGC activity induced by abrupt velocity changes. Therefore, neurons in higher brain areas may in principle extract information about changing velocity from the instantaneous firing activity of RGCs, without the need to compare responses to present velocities to previous ones. However, reconstruction requires the estimation of a combined acceleration and velocity signal, indicating that RGC ensembles signal both properties simultaneously. In accordance with this conclusion, combined velocity/acceleration sensitivity enhances the similarity of artificial spike trains to experimental data by 50% compared to the case of pure velocity tuning. Decoding of motion direction in addition to speed and acceleration requires direction sensitive cells, which generate higher firing rates for one of the motion directions and therefore show asymmetric velocity tuning. By dividing the entire ensemble of simultaneously recorded cells into one group of direction-sensitive cells and one group with symmetric tuning, we demonstrate that the population of these direction-sensitive cells encodes a combination of motion speed, acceleration and direction. However, estimation of velocity and acceleration is improved by including the larger group of RGC responses that are sensitive to speed but not to motion direction.
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