Klaus Hausen

Motion sensitive interneurons in the optomotor system of the fly

The three horizontal cells of the lobula plate of the blowflyCalliphora erythrocephala were studied anatomically and physiologically by means of cobalt impregnations and intracellular recordings combined with Procion and Lucifer Yellow injections. The cells are termed north, equatorial and south horizontal cell (HSN, HSE, HSS) and are major output neurons of the optic lobe. 1. The dendritic arborizations of the HSN, HSE, HSS reside in a thin anterior layer of the lobula plate and extend over the dorsal, equatorial and ventral parts of this neuropil, respectively. Due to the retinotopic organization of the optic lobe, these parts correspond anatomically to respective regions of the ipsilateral visual field. Homologue horizontal cells in both lobula plates of the same animal and in different animals are highly variable with respect to their individual dendritic branching patterns. They are extraordinarily constant, on the other hand, with regard to the position and size of their dendritic fields as well as their dendritic branching density distributions. Each cell covers about 40% of the total area of the lobula plate and shows the highest dendritic density near the lateral margin of the neuropil which subserves the frontal eye region. The axons of the horizontal cells are relatively short and large in diameter; they terminate in the posterior ventrolateral protocerebrum. 2. The horizontal cells are directionally selective motion sensitive visual interneurons responding preferentially to progressive (front to back) motion in the ipsilateral visual field with graded depolarization of their axons and superimposed action potentials. Stimulation with motion in the reverse direction leads to hyperpolarizing graded responses. The HSE and HSN are additionally activated by regressive motion in the contralateral visual field.

The Lobula-Complex of the Fly: Structure, Function and Significance in Visual Behaviour

The lobula-complex of flies consists of the highest order visual neuropils of the optic lobe, the lobula plate and the lobula. Anatomical and electrophysiological investigations of the lobula plate have revealed that it contains a system of large directionally selective motion sensitive interneurons. The structure, response characteristics and synaptic interactions of these interneurons are described. There is strong evidence that the lobula plate is the main motion computation centre of the optic lobe controlling the optomotor responses of the fly. Additional functions in the visual fixation and tracking behaviour and in the figure-ground discrimination seem likely. The lobula has so far been studied only anatomically but not physiologically. Rather indirect evidence suggests that it computes visual signals initiating escape behaviour. The existence of male specific interneurons in this neuropil indicates that it is additionally involved in the control of chasing behaviour typical of males.

Figure-ground discrimination by relative movement in the visual system of the fly

A moving object can be separated from its surround on the basis of motion information alone. It has been known for some time that various species and especially the housefly can discriminate relative motion of an object and its background, even when the two have an identical texture. An earlier paper (Reichardt and Poggio, 1979) has analyzed on the basis of behavioural experiments the main features of the algorithm used by the fly to separate figure from ground. This paper (a) proposes the basic structure of a neuronal circuitry possibly underlying the detection of discontinuities in the optical flow by the visual system of the houseflyMusca; (b) compares detailed predictions of the model circuitry with old and new behavioural experiments onMusca (measuring its attempts to fixate an object), and (c) studies the neuronal realization of the model circuitry in terms of electrophysiological recordings from the lobula plate horizontal cells of the blowflyCalliphora.

Neural Mechanisms of Visual Course Control in Insects

Visual orientation and course-stabilization of flying insects rely essentially on the evaluation of the retinal motion patterns perceived by the animals during flight. Apparent motions of the entire surrounding indicate the direction and speed of self-motion in space and are used as visual feedback signals during optomotor course-control manoeuvres. Discontinuities in the motion pattern and relative motions between pattern-segments indicate the existence of stationary or moving objects and represent the basic visual cues for flight-orientation during fixation-and tracking-sequences, and possibly also for the avoidance of obstacles, and the selection of landing sites.

The number and structure of giant vertical cells (VS) in the lobula plate of the blowflyCalliphora erythrocephala

Summary1.The structure of one class of giant tangential neurons in the lobula plate ofCalliphora, the ‘Vertical System (VS)’ has been investigated by light microscopy. Different staining and reconstruction procedures were employed to ensure that all existing VS-neurons are revealed.2.There are 11 VS-cells in a characteristic, and constant arrangement (Fig. 2). Each cell covers a particular area of the lobula plate, i.e., a distinct area of the retinotopic input array (Table 2), and therefore has a distinct receptive field.3.Although VS-cells in general tend to occupy the posterior surface of the lobula plate, only three of them (VS 2-VS 5) reside exclusively in this layer. The other cells (VS1 and VS6-VS10) have bistratified dendritic arborizations (Fig. 6), whose dorsal parts are apposed to the anterior surface of the lobula plate.4.The arrangement, territory and stratification of any given VS-cell is largely invariant in different individuals, whereas the branching pattern may vary considerably (Fig. 3).5.The present results provide the framework for physiological studies of the role of individual VS-cells in movement perception, and their involvement in the control of particular locomotor behaviour.

Visual course control in flies relies on neuronal computation of object and background motion

The spatial distribution of light intensity received by the eyes changes continually when an animal moves around in its environment. These retinal activity patterns contain a wealth of information on the structure of the environment, the direction and speed of self-motion, and on the independent motion of objects1,2. If evaluated properly by the nervous system this information can be used in visual orientation. In a combination of both behavioural and electrophysiological analysis and modelling, this article establishes the neural mechanisms by which the visual system of the fly evaluates two types of basic retinal motion patterns: coherent retinal large-field motion as induced by self-motion of the animal, and relative motion between objects and their background. Separate neuronal networks are specifically tuned to each of these motion patterns and make use of them in two different visual orientation tasks.

Microsurgical lesion of horizontal cells changes optomotor yaw responses in the blowfly Calliphora erythrocephala

The horizontal cells of flies are giant output neurons of the otpic lobes that respond selectively to horizontal motion in the visual environment. The effect of microsurgical lesion of the cells on visually induced flight behaviour was investigated in blowflies (Calliphora erythrocephala). The results indicate that the horizontal cells are the parts of the neural circuitry that control the generation of optomotor yaw torque.

A neuronal circuitry for relative movement discrimination by the visual system of the fly

We propose the basic structure of a neuronal circuitry possibly underlying the detection of discontinuities in the optical flow by the visual system of the housefly. The main features of the circuitry are: binocular cells summate elementary movement detectors over a large visual field and inhibit each one of them; inhibition is of the shunting type, with an inhibitory equilibrium potential very near the resting potential. A specific model implementing our proposal accounts for all the behavioral data on relative movement discrimination, including the characteristic dynamics of the response.

How is tracking and fixation accomplished in the nervous system of the fly

The optomotor yaw torque response of fixed flying female houseflies, Musca domestica to three different types of visual stimuli is analyzed. In contrast to most previous investigations, the stimuli were displayed for short time intervals only in order to approximate transiently occuring visual stimuli, which mainly govern the torque generation during free flight. Monocular stimulation with a periodic pattern moving in different positions in the equatorial plane of the compound eyes reveals that (1) flight torque responses are mainly induced by progressive (front to back) motion; regressively moving stimuli are significantly less effective. (2) the strength of the response to motion in the horizontal direction depends on the position of the stimulus and (3) vertical motions do not elicit flight torque responses. Correspondingly the response to a single vertical black stripe moving clockwise in a cylindrical panorama centered around the fly is small if the stripe is in the visual field of the left eye but becomes large and strongly depending on position if the stripe enters the visual field of the right eye. The response to counterclockwise motion of the stripe is small if the stripe is in the visual field of the right eye but becomes large and strongly depending on position if the stripe enters the visual field of the left eye. Torque responses to two adjacent stripes whose intensities are modulated in time with a rectangular function can be elicited if apparent motion is generated by means of a phase difference between the intensity modulations of the two stripes. Apparent progressive motion elicits strong torque responses, apparent regressive motion is less effective. Synchronous flicker of both stripes does not elicit torque responses. The extraction of positional information from the incoming visual signals has been considered to play an important role in the orientation behaviour, and especially in the tracking behaviour of flies. The results of the experiments indicate, that under transient stimulation the evaluation of positional information is in general not mediated by formerly postulated flicker detectors but is bound to the computation of motion. These findings are implemented in a model, describing the free flight tracking behaviour of a female fly on the horizontal plane. It is shown that tracking can be achieved by a mechanism whose sensitivity to motion is parametrized in the stimulus position as outlined above. The results of the behavioural experiments are interpreted in view of electrophysiological and anatomical data on giant interneurons in the third optic ganglion of the fly.

Is the landing response of the housefly (Musca) driven by motion of a flow field

The landing response of tethered flying housefliesMusca domestica elicited by motion of periodic gratings is analysed. The field of view of the compound eyes of a fly can be subdivided into a region of binocular overlap and a monocular region. In the monocular region the landing response is elicited by motion from front to back and suppressed by motion from back to front. The sensitivity to front to back motion in monocular flies (one eye covered with black paint) has a maximum at an angle 60°–80° laterally from the direction of flight in the equatorial plane. The maximum of the landing response to front to back motion as a function of the contrast frequencyw/λ is observed at around 8 Hz. In the region of binocular overlap of monocular flies the landing response can be elicited by back to front motion around the equatorial plane if a laterally positioned pattern is simulataneously moved from front to back. 40° above the equatorial plane in the binocular region the landing response in binocular flies is elicited by upward motion, 40° below the equatorial plane in the binocular region it is elicited by downward motion. The results are interpreted as an adaptation of the visual system of the fly to the perception of a flow field having its pole in the direction of flight.