Input organization of motion-sensitive interneurons in the fly.

Abstract

The network of tangential cells in the lobula plate (LPTCs) of the fly receives retinotopic input from excitatory and inhibitory columnar elements encoding local motion information. This work uses both experimental and computational methods to address the question of how local inputs and network interactions within the LPTC system affect the responses of LPTCs to visual motion stimulation. First, the excitatory and inhibitory synaptic currents were decomposed analytically, by using current injection measurements. This electrophysiological method was used to test the previous assumption that both inputs, i.e. excitatory and inhibitory, exhibit weak direction selectivity. The excitatory component was strongly directionally selective while the inhibitory component was weakly selective for the same direction, defying the ongoing theory. Excitatory (gexc) and inhibitory (ginh) conductances were proportional to each other for different stimulus conditions used. Similar gexc:ginh balancing in the vertebrate cortex is associated with synaptic gain control, suggesting that a form of gain control may govern the input to this system. The following two types of LPTCs represented an exception to the above scheme: CH cells are believed to receive their input not from elementary motion detector cells but from HS cells dendritically via electrical synapses. Furthermore, they transmit this information to other LPTCs via their dendrite. I showed by realistic compartmental modeling that the assumptions for this type of connectivity are founded. Linear electrical synapses between HS and CH without current rectification or temporal filtering characteristics fitted best the experimental results. This dendritic network implements a convolution, one of the most common operations in image processing. In a first step, dendritic electrical coupling spatially blurs the original motion input of the HS cell in the CH cell. The blurred motion image is then passed onto another LPTC via inhibitory dendritic synapses resulting in a sharpening of the signal. This enhancement of motion contrast may be the central element of figure- ground discrimination based on relative motion in the fly. Among the VS cells, the VS1 exhibited a similar input decomposition signature as the CH cell. The impact of recently observed network connections among LPTCs is discussed.