Dendritic Computation of Direction Selectivity and Gain Control in Visual Interneurons

Abstract

The extraction of motion information from time varying retinal images is a fundamental task of visual systems. Accordingly, neurons that selectively respond to visual motion are found in almost all species investigated so far. Despite its general importance, the cellular mechanisms underlying direction selectivity are not yet understood in most systems. Blocking inhibitory input to fly visual interneurons by picrotoxinin (PTX), we demonstrate that their direction selectivity arises largely from interactions between postsynaptic signals elicited by excitatory and inhibitory input elements, which are themselves only weakly tuned to opposite directions of motion. Their joint activation by preferred as well as null direction motion leads to a mixed reversal potential at which the postsynaptic response settles for large field stimuli. Assuming the activation ratio of these opponent inputs to be a function of pattern velocity can explain how the postsynaptic membrane potential saturates with increasing pattern size at different levels for different pattern velocities ("gain control"). Accordingly, we find that after blocking the inhibitory input by PTX, gain control is abolished.Key words: direction selectivity; motion detection; membrane parameters; compartmental model; synaptic conductance; neural computation; gain control; flyThe fly has for long been a model system to study the processing and extraction of motion information from the time varying retinal images. In the third visual neuropile of the fly optic lobes a group of individually identifiable, motion-sensitive interneurons has been found. They are called lobula plate tangential cells (LP TC s) and are involved in visual course control (Hausen, 1984). In the blowfly Calliphora er ythrocephala this group comprises about 60 different cells. Via large dendritic arbors, these neurons spatially pool the signals of thousands of retinotopically arranged columnar elements . Most LP TC s studied so far display a directionally selective response: When the pattern is moving in the preferred direction (PD) of the cell, the cells become excited; when the pattern is moving in the anti-preferred or null direction (N D) of the cell, they become inhibited. Many L P TC s are nonspiking neurons. Rather than producing regular action potentials, they respond to visual motion by a graded shift of their membrane potential. Their directional selective responses are driven by at least two kinds of input elements, one being excitatory and the other inhibitory Borst et al., 1995) (Fig. 1a). As was revealed by in vitro studies (Brotz et al., 1995), the underlying dendritic receptors exhibit a pharmacological profile typical for insect nicotinic ACh receptors and picrotoxinin (P TX)-sensitive GABA receptors, respectively (Brotz and Borst, 1996).The computational structure of the fly motion detection system can be well described by a correlation type of elementary motion detector (EMD) Egelhaaf and Borst, 1989). This model for motion detection assumes a delay-andcompare mechanism for ea...

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

“…The membrane conductances introduced a nonlinearity into the model HSE cell, which was partly responsible for the so-called gain control of the HSE cell. By 'gain control' we mean that the responses of the HSE cell are largely invariant against changes in pattern size, while still depending on pattern velocity (Single et al 1997, Borst et al 1995, Hausen 1982b). The specific gain control properties are determined by the relation between the cell's leak conductance (g 0 ) and the membrane conductances (g e , g i ) that are modulated by the visual input.…”

“…This is because TCs such as the HSE cell receive opponent input from excitatory and inhibitory input channels. Since the ratio of activation of both types of input depends on the direction of motion and on stimulus velocity, the HSE cell as well the output neuron of the model approach different saturation levels for different velocities (Single et al 1997, Borst et al 1995, Egelhaaf and Borst 1993a. This gain control might lead to response levels that are independent of textural changes in the environment as may frequently happen to the fly under outdoors conditions.…”

Directional Selectivity in the Simple Eye of an Insect

“…We observed the same inseparabilities in the UV STRFs of L-neurons. This type of directional computation is distinct from that seen in fully opponent directionally selective cells, like lobula plate tangential cells in flies (Hausen, 1982a,b;Single et al, 1997;Borst and Haag, 2002;Egelhaaf et al, 2002) or complex cells in the mammalian visual cortex (Emerson et al, 1992) that encode directionality in the mean of the response.…”

Encoding of motion in real time by the fly visual system

“…As a consequence of the opponent local motion inputs, the response saturates at different levels for different velocities (Figure 1c). Hence, the responses, while still encoding velocity, are almost invariant against changes in pattern size [26,27]. (i) The enlargement illustrates that each point in the visual space is subserved by a pair of input elements of the TCs, one of them being cholinergic (ACh) and excitatory, the other GABAergic and inhibitory [19].…”