The physiological basis for contrast opponency in motion computation in Drosophila

In Drosophila, direction-selective neurons implement a mechanism of motion computation similar to cortical neurons, using contrast-opponent receptive fields with ON and OFF subfields. It is not clear how the presynaptic circuitry of direction-selective neurons in the OFF pathway supports this computation if all major inputs are OFF-rectified neurons. Here, we reveal the biological substrate for motion computation in the OFF pathway. Three interneurons, Tm2, Tm9 and CT1, provide information about ON stimuli to the OFF direction-selective neuron T5 across its receptive field, supporting a contrast-opponent receptive field organization. Consistent with its prominent role in motion detection, variability in Tm9 receptive field properties transfers to T5, and calcium decrements in Tm9 in response to ON stimuli persist across behavioral states, while spatial tuning is sharpened by active behavior. Together, our work shows how a key neuronal computation is implemented by its constituent neuronal circuit elements to ensure direction selectivity.

Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion

Diverse sensory systems, from audition to thermosensation, feature a separation of inputs into ON (increments) and OFF (decrements) signals. In the Drosophila visual system, separate ON and OFF pathways compute the direction of motion, yet anatomical and functional studies have identified some crosstalk between these channels. We used this well-studied circuit to ask whether the motion computation depends on ON-OFF pathway crosstalk. Using whole-cell electrophysiology we recorded visual responses of T4 (ON) and T5 (OFF) cells and discovered that both cell types are also directionally selective in response to non-preferred contrast motion. We mapped T4s' and T5s' composite ON-OFF receptive fields and found they share a similar spatiotemporal structure. We fit a biophysical model to these receptive fields that accurately predicts directionally selective T4 and T5 responses to both ON and OFF moving stimuli. This model also provides a detailed mechanistic explanation for the directional-preference inversion in response to a prominent visual illusion, a result we corroborate with electrophysiological recordings and behavioral responses of flying flies.

The physiological basis for the computation of direction selectivity in the Drosophila OFF pathway

In Drosophila, direction-selective neurons implement a mechanism of motion computation similar to cortical neurons, using contrast-opponent receptive fields with ON and OFF subunits. It is not clear how the presynaptic circuitry of direction-selective neurons in the OFF pathway supports this computation, because all major inputs are OFF-rectified neurons. Here, we reveal the biological substrate for motion computation in the OFF pathway. Three interneurons, Tm2, Tm9 and CT1, also provide information about ON stimuli to the OFF direction-selective neuron T5 across its receptive field, supporting a contrast-opponent receptive field organization. Consistent with its prominent role in motion detection, variability in Tm9 receptive field properties is passed on to T5, and calcium decrements in Tm9 in response to ON stimuli are maintained across behavioral states, while spatial tuning is sharpened by active behavior. Together, our work shows how a key neuronal computation is implemented by its constituent neuronal circuit elements to ensure direction selectivity.

State and stimulus dependence reconcile motion computation and the Drosophila connectome

Sensory systems dynamically optimize their processing properties in order to process a wide range of environmental and behavioral conditions. However, attempts to infer the function of these systems via modeling often treat system components as having static processing properties. This is particularly evident in the Drosophila motion detection circuit, where the core algorithm for motion detection is still debated, and where inputs to motion detecting neurons remain underdescribed. Using whole-cell patch clamp electrophysiology, we measured the state- and stimulus-dependent filtering properties of inputs to the OFF motion-detecting T5 cell in Drosophila. Simply summing these inputs within the framework of a connectomic-constrained model of the circuit demonstrates that changes in the shape of input temporal filters are sufficient to explain conflicting theories of T5 function. Therefore, with our measurements and our model, we reconcile motion computation with the anatomy of the circuit.

Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes

Animals detect motion using a variety of visual cues that reflect regularities in the natural world. Experiments in animals across phyla have shown that motion percepts incorporate both pairwise and triplet spatiotemporal correlations that could theoretically benefit motion computation. However, it remains unclear how visual systems assemble these cues to build accurate motion estimates. Here, we used systematic behavioral measurements of fruit fly motion perception to show how flies combine local pairwise and triplet correlations to reduce variability in motion estimates across natural scenes. By generating synthetic images with statistics controlled by maximum entropy distributions, we show that the triplet correlations are useful only when images have light-dark asymmetries that mimic natural ones. This suggests that asymmetric ON-OFF processing is tuned to the particular statistics of natural scenes. Since all animals encounter the world’s light-dark asymmetries, many visual systems are likely to use asymmetric ON-OFF processing to improve motion estimation.