The orientation of flies towards visual patterns: On the search for the underlying functional interactions

The average optomotor response of insects to a given visual stimulus (measured in open-loop conditions) can be decomposed into a direction sensitive and a direction insensitive component. This decomposition is conceptual and always possible. The direction sensitive optomotor response represents the “classical” optomotor reflex, already studied in previous investigations; the direction insensitive optomotor response is strictly connected to the orientation and tracking behaviour (see the work of Reichardt and coworkers). Thus a characterization of the direction insensitive response is useful in clarifying the nervous mechanisms underlying the orientation behaviour. For this reason we study in this paper the direction insensitive optomotor (torque) response of fixed flying fliesMusca domestica. Periodic gratings, either moving or flickering, represent our main stimulus, since the dependence of the fly response on the spatial wavelength can unravel the presence and properties of the underlying lateral interactions. In this connection an extension of the Volterra series formalism to multi-input (nervous) networks is first outlined in order to connect our (behavioural) input-output data with the interactive structure of the network. A number of results concerning, for instance, the response of such networks to flickered and moving gratings are derived; they are not restricted to our behavioural results and may be relevant in other fields of neuroscience. These theoretical considerations provide the logical framework of our experimental investigation. The main results are:

1. the direction insensitive optomotor response depends on the spatial frequency of a moving grating, implying the existence of (nonlinear) lateral interactions,
2. its wavelength dependence changes with age, unlike the direction sensitive response,
3. both the direction insensitive response and the (closed loop) orientation behaviour are present only in the lower part of the eye; on the other hand the direction sensitive response is present in every part of the two eyes.

Furthermore the attraction towards a flickered periodic grating shows, as theoretically expected, a wavelength-dependence similar to that of the direction insensitive response, again present only in the lower part of the eye. The interactions which affect the orientation response are selective with respect to the spatiotemporal mapping of the pattern onto the receptor array. It is conjectured that these interactions are the basic mechanisms underlying spontaneous pattern discrimination in flies. Their possible organization is further discussed in terms of our formalism. Moreover our data suggest that two specific nervous circuitries correspond to our conceptual decomposition of the optomotor response.