A Class of Visual Neurons with Wide-Field Properties Is Required for Local Motion Detection

Abstract

Visual motion cues are used by many animals to guide navigation across a wide range of environments. Long-standing theoretical models have made predictions about the computations that compare light signals across space and time to detect motion. Using connectomic and physiological approaches, candidate circuits that can implement various algorithmic steps have been proposed in the Drosophila visual system. These pathways connect photoreceptors, via interneurons in the lamina and the medulla, to direction-selective cells in the lobula and lobula plate. However, the functional architecture of these circuits remains incompletely understood. Here, we use a forward genetic approach to identify the medulla neuron Tm9 as critical for motion-evoked behavioral responses. Using in vivo calcium imaging combined with genetic silencing, we place Tm9 within motion-detecting circuitry. Tm9 receives functional inputs from the lamina neurons L3 and, unexpectedly, L1 and passes information onto the direction-selective T5 neuron. Whereas the morphology of Tm9 suggested that this cell would inform circuits about local points in space, we found that the Tm9 spatial receptive field is large. Thus, this circuit informs elementary motion detectors about a wide region of the visual scene. In addition, Tm9 exhibits sustained responses that provide a tonic signal about incoming light patterns. Silencing Tm9 dramatically reduces the response amplitude of T5 neurons under a broad range of different motion conditions. Thus, our data demonstrate that sustained and wide-field signals are essential for elementary motion processing.

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

“…1A) (Fischbach and Dittrich, 1989;Maisak et al, 2013). To study the algorithm for direction selectivity in T4 and T5, we recorded the visually evoked calcium dynamics of T4 and T5 using in vivo two-photon microscopy of the genetically encoded calcium indicator GCaMP6f, which we targeted to these cells using the R42F06 driver line (Maisak et al, 2013;Fisher et al, 2015b). R42F06 drives strong expression in most T4 and T5 neurons, revealing strongly contrast-and direction-selective responses in T4 and T5 axon terminals in the lobula plate (Maisak et al, 2013).…”

“…To achieve single-neuron resolution of T4 and T5, we first isolated single-cell clones using a stochastic Flpout method, which limited expression of GCaMP6f to a sparse subset of the R42F06 expression pattern (Fig. 1C) (Gordon and Scott, 2009;Chen et al, 2013;Gruntman and Turner, 2013;Fisher et al, 2015b). From the sparsened R42F06 expression pattern, we identified visually responsive single-cell clones by their periodic responses to moving sinusoidal gratings.…”

“…Because T5 responds poorly to full-field contrast excursions (Maisak et al, 2013;Fisher et al, 2015a), ROIs were excluded from further analysis if they were responsive ( p Ͻ 0.01) to this stimulus. Clustering pixels in a space of response properties guarantees that each cluster is defined by a response profile that is shared by all constituent pixels, but it does not guarantee that this response profile corresponds to a single unit.…”

“…Multiplication nonlinearly enhances the PD response. Indeed, calcium imaging of the most upstream direction-selective neurons in Drosophila, T4 and T5, has demonstrated precisely this functional signature: nonlinear enhancement of responses to PD motion (Fisher et al, 2015b).…”

“…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). What neural circuit configuration transforms nondirection-selective inputs into direction-selective outputs?…”