Processing properties of ON and OFF pathways for Drosophila motion detection

Abstract

The algorithms and neural circuits that process spatiotemporal changes in luminance to extract visual motion cues have been the focus of intense research. An influential model, the Hassenstein-Reichardt correlator1 (HRC), relies on differential temporal filtering of two spatially separated input channels, delaying one input signal with respect to the other. Motion in a particular direction causes these delayed and non-delayed luminance signals to arrive simultaneously at a subsequent processing step in the brain; these signals are then nonlinearly amplified to produce a direction-selective response (Figure 1A). Recent work in Drosophila has identified two parallel pathways that selectively respond to either moving light or dark edges2,3. Each of these pathways requires two critical processing steps to be applied to incoming signals: differential delay between the spatial input channels, and distinct processing of brightness increment and decrement signals. Using in vivo patch-clamp recordings, we demonstrate that four medulla neurons implement these two processing steps. The neurons Mi1 and Tm3 respond selectively to brightness increments, with the response of Mi1 delayed relative to Tm3. Conversely, Tm1 and Tm2 respond selectively to brightness decrements, with the response of Tm1 delayed compared to Tm2. Remarkably, constraining HRC models using these measurements produces outputs consistent with previously measured properties of motion detectors, including temporal frequency tuning and specificity for light vs. dark edges. We propose that Mi1 and Tm3 perform critical processing of the delayed and non-delayed input channels of the correlator responsible for the detection of light edges, while Tm1 and Tm2 play analogous roles in the detection of moving dark edges. Our data shows that specific medulla neurons possess response properties that allow them to implement the algorithmic steps that precede the correlative operation in the HRC, revealing elements of the long-sought neural substrates of motion detection in the fly.

Direction Selectivity in Drosophila Emerges from Preferred-Direction Enhancement and Null-Direction Suppression

“…Model-fitting code was implemented in Python using Theano and the Lasagne deep-learning framework (Bergstra et al, 2010;Bastien et al, 2012). Models were fit using minibatch optimization with the Adam optimization algorithm (Kingma and Ba, 2014) with a learning rate optimized through cross-validation, ␤ 1 ϭ 0.9, ␤ 2 ϭ 0.999, and ⑀ ϭ 10 Ϫ8 .…”

“…In the fly motion-processing stream, third-order medulla neurons are contrast selective to either light or dark increments but are not direction selective (Behnia et al, 2014;Strother et al, 2014;Serbe et al, 2016;Yang et al, 2016). Directly postsynaptic to these medulla neurons, T4, which is selective for moving light edges, and T5, which is selective for moving dark edges, exhibit direction selectivity (Maisak et al, 2013;Fisher et al, 2015b).…”

Subcellular mapping of dendritic activity in optic flow processing neurons

“…Accordingly, the response of Tm1 is delayed relative to Tm2. Although this offset is rather small, the authors of this study suggest that it represents the temporal delay between the two arms of a Reichardt detector, and Mi1/Tm3 and Tm1/Tm2 form two elementary motion detectors for ON and OFF stimuli, respectively [61].…”

The use of computational modeling to link sensory processing with behavior in Drosophila

“…(Schwartz et al 2006;Aljadeff et al 2016)). In the context of Drosophila systems neuroscience, LN models have provided insight into the dynamical stimulus features driving neuronal responses in the olfactory system (Nagel and Wilson 2011;Martelli et al 2013), visual system (de Vries and Clandinin 2012; Seelig and Jayaraman 2013; Behnia et al 2014)), and auditory system (Clemens et al 2015a). These LN models provide information about what sensory information is available to the brain for driving behaviors and in which format it is represented.…”