Eye Movements and Visual Tracking in Flies

The preceding section demonstrated that the visual systems of flies are richly endowed with at least two types of DS visual neuron, and several preferred directions. It is reasonable to assume that these neurons carry information to the complex motor centers that stabilize flight. In the visual systems of other arthropods, e.g., crustaceans, which have movable eyes on eyestalks, visual DS units control eye movements (Burrows and Horridge, 1968; Horridge and Burrows, 1968).

Insect eyes are generally considered to be fixed to their heads, and only move when the head moves, so that rapid scanning or fixation saccades are not possible. The exception to the fixed eye occurs in the eyes of flies and mosquitoes (the Diptera). Figure 5.4-2 shows a schematic of a horizontal section through the middle of a fly's head; the section passing through the eye's "equator." A thin muscle (M. orbito-tentoralis, or MOT) has its origin at the heavy chitin of the tentorium (TT) at the rear of the head. The tentorium lies in line with the mass of the optic ganglia and the center of the CE. The muscle inserts on the inner margin of the orbital ridge, an elastic ring that surrounds the base of the retinular structure and gives it support. The muscle has 14 to 20 tubular fibers, each 7 to 10 |im in diameter, innervated by multiple motor end plates from a single motor nerve fiber, about 6 |im in diameter (Hengtstenberg, 1972). There is one muscle and nerve for each eye; i.e., it is a paired structure. The nerves arise from the sides of the subesophageal ganglion.

The mechanics of the fly's eye muscle system are not clearly understood. Because the muscle inserts at the central medial margin of the orbital ridge, increased muscle tension and shortening presumably move the proximal ends of the medial central ommatidia medially, while the distal ends of the ommatidia remain relatively fixed, anchored by the attachment of the cuticle on the outside of the eye to the heavy head cuticle at the margin of the eye. This medial movement of the proximal ends of the ommatidia appears to swing their optical axes laterally, toward the animal's rear, providing what is in effect a scanning eye movement toward the rear. This eye movement affects the most anterior or medial ommatidia the most, and the lateral ommatidia (on the rear margin of the eye) probably do not move at all.

Early workers on fly vision observed so-called clock spikes from the OLs of flies (Leutscher-Hazelhoff and Kuiper, 1966). In the absence of visual stimuli, or in the dark, these spikes fired very regularly at a mean rate determined by the fly's temperature. From a graph given by Leutscher-Hazelhoff and Kuiper (their Figure 2), the author found that the clock spike frequency in Calliphora was approximately given

FIGURE 5.4-2 Artist's summary of a horizontal section through the middle of a fly's head. A visual object is moving from left to right in front of the fly. When the MOT contracts, the visual axes of the medial ommatidia swing to the right, tracking the object. Ideally, vo = ve = R0. Key: MOT, muscle orbitotentorialis; NMOT, motor nerve to MOT; RET, ommatidia; LAM, lamina ganglionaris; MED, medulla of OL; TT, tentorium; ANT, antenna base; NA, antennal nerve; OE, esophagus; SOG, subesophageal ganglion. (Modified from Qi, 1989. With permission.)

FIGURE 5.4-2 Artist's summary of a horizontal section through the middle of a fly's head. A visual object is moving from left to right in front of the fly. When the MOT contracts, the visual axes of the medial ommatidia swing to the right, tracking the object. Ideally, vo = ve = R0. Key: MOT, muscle orbitotentorialis; NMOT, motor nerve to MOT; RET, ommatidia; LAM, lamina ganglionaris; MED, medulla of OL; TT, tentorium; ANT, antenna base; NA, antennal nerve; OE, esophagus; SOG, subesophageal ganglion. (Modified from Qi, 1989. With permission.)

by f = -40 + 6.25 T pps. T is the Celcius temperature, and no spikes occur for T > 36° or T < 15°. At room temperature, f is about 85 pps. Subsequent workers found that the clock spike was related to (if not actually) the MOT nerve (NMOT) firing in order to maintain a constant state of tension in the MOT. Thus, any increase or decrease in the firing frequency will increase or decrease muscle tension, respectively, and cause the anterior (medial) ommatidia to scan to the rear or forward, respectively.

Burtt and Patterson (1970) and Patterson (1973a,b) reported that the NMOT frequency underwent a transient increase in frequency for OFF or dimming of general illumination. Conversely, ON or brightening caused a transient decrease in the NMOT firing rate. Burtt and Patterson (1970) also reported that when a vertical dark stripe was moved from front to rear around the head, the ipsilateral NMOT firing rate increased during the motion, and decreased when the stripe was moved from rear to front. This suggested that DS visual units may play a role in modulating the frequency of the NMOT mean rate. Burtt and Patterson also observed that puffs of air directed at the head caused transient changes in the frequency of the NMOT. This multimodal behavior suggests that there is a functional connection between the yaw stimulation of aerodynamic mechanoreceptor hairs and the need to scan the medial retinula cells.

The author and graduate student Xiaofeng Qi decided to investigate the dynamics of the clock spike and eye muscle (CSEM) system of the fly Calliphora erythro-cephala. Qi (1989a, b), using fixed, nonflying Calliphora flies, recorded MOT action potentials from both left and right MOTs while presenting the animal with various controlled moving visual stimuli. To characterize better the rapid changes in frequency on the left and right CSEM systems, Qi used two instantaneous pulse frequency demodulators (IPFDs) to convert the instantaneous frequency (IF) of the spike trains to voltage in the following manner: The kth interspike interval (defined by two adjacent spikes), Tk, is by definition, Tk = (tk - tk-1). tk is the time the kth spike in the sequence occurs, tk-1 is the time the previous spike occurs. Since two spikes are needed to define an interval, k = 2, 3, ... x. The kth element of instantaneous frequency is defined as rk = 1/Tk. The analog output voltage of the IPFD is given by

U(t - tk) is a unit step which occurs at t = tk, by definition, it is 0 for t < tk and 1 for t S tk. Vok is thus a stepwise series of voltages, each level of which is the instantaneous frequency of the preceding interspike interval. G is a scaling constant, typically, G = 0.01.

Qi found that when a vertical stripe was moved from side to side in front of the insect, the object motion from left to right (or anterior to posterior at the right eye) caused the IF of the right NMOT spikes to increase, and at the same time, the IF of the left NMOT decreased. When the stripe centered in front of the fly was given a sinusoidal deflection of known frequency, an interesting set of phase relations emerged between the stimulus position and the averaged left and right NMOT IFs. Figure 5.4-3 illustrates the IF changes of the left and right eye MOT spikes. (Note that MOT spikes follow the NMOT spike in a 1:1 manner without appreciable delay.) Stimulus frequency was about 1 Hz, and the amplitude was about ± 15° at the eyes. The black stripe subtended 3.5° in the horizontal plane, and extended 38° vertically. The IFs of the left and right MOTs were 180° out of phase, and each led the stimulus position by about 90°, suggesting that the nerves were responding to object velocity, rather than position. To verify that object velocity was driving the NMOT frequencies, Qi deflected his centered test stripe ±15° with a triangle wave. The results are shown in Figure 5.4-4. Note that the IF responses to object movement are rounded square waves, which would be expected from taking the bandwidth-limited derivative of a triangular position waveform. Only the IF changes are shown; they represent variations in frequency around an average clock spike frequency of about 80 pps.

When both eyes were subjected to a ±15° square-wave lateral displacement of a 0.75° wide stripe centered on the fly, the result was a "impulse function" change in the IF of the right and left MOT spikes, shown in Figure 5.4-5. Note that when the stripe snaps to the left or right, the IF response is different on the k=2

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