Visual position stabilization in the hummingbird hawk moth, Macroglossum stellatarum L. II. Electrophysiological analysis of neurons sensitive to wide-field image motion

Response properties of neurons in the cervical connectives of the hummingbird hawk moth, Macroglossum stellatarum L., were determined. All neurons described in this account respond directionally selectively to motion in large parts of the visual field of either eye. They respond maximally to bilateral stimulation, preferring either motion as induced on the eyes during translatory movements of the animal or when it turns around one of its body axes. Cells most sensitive to rotational motion either respond best to rotation of the patterns around the vertical axis of the animal or around its longitudinal body axis. Neurons most sensitive to translational pattern motion respond best to either simulated translations of the animal along its vertical or along an oblique axis. Most types of neurons respond tonically and do not habituate. The sensitivity to motion stimuli is not evenly distributed within the receptive field of any investigated neuron. Part of these neurons might play a role in visual position and course stabilization. Accepted: 13 August 1997     

A system of insect neurons sensitive to horizontal and vertical image motion connects the medulla and midbrain

Summary The response properties and gross morphologies of neurons that connect the medulla and midbrain in the butterfly Papilio aegeus are described. The neurons presented give direction-selective responses, i.e. they are excited by motion in the preferred direction and the background activity of the cells is inhibited by motion in the opposite, null, direction. The neurons are either maximally sensitive to horizontal motion or to slightly off-axis vertical upward or vertical downward motion, when tested in the frontal visual field. The responses of the cells are dependent on the contrast frequency of the stimulus with peak values at 5–10 Hz. The receptive fields of the medulla neurons are large and are most sensitive in the frontal visual field. Examination of the local and global properties of the receptive fields of the medulla neurons indicates that (1) they are fed by local elementary motion-detectors consistent with the correlation model and (2) there is a non-linear spatial integration mechanism in operation.     

The transmission of translational seat vibration to the head--II. Horizontal seat vibration

The second part of this study of the six axes of head motion caused by translational seat vibration is concerned with the effect of fore-and-aft (x-axis) and lateral (y-axis) seat vibration. Seat-to-head transmissibilities have been determined at frequencies up to 16 Hz for each of the three translational and three rotational axes of the head during exposure to random vibration of the seat. Repeatability measures within a single subject and studies of the variability across a group of twelve subjects have been conducted with two seating conditions: a rigid seat with a backrest, and the same seat with no backrest. Fore-and-aft seat motion mainly resulted in head motion within the mid-sagittal plane (x-z plane). Without the backrest, transmissibilities for the fore-and-aft, vertical and pitch axes of the head were greatest at about 2 Hz. The backrest greatly increased head vibration at frequencies above 4 Hz and caused a second peak in the transmissibility curves at about 6 to 8 Hz. Lateral seat motion mainly caused lateral head motion with a maximum transmissibility at about 2 Hz. The backrest had little effect on the transmission of lateral vibration to the head. For both axes of excitation inter-subject variability was much greater than intra-subject variability.     

Visual processing of moving single objects and wide-field patterns in flies: Behavioural analysis after laser-surgical removal of interneurons

A laser micro-beam unit was used to reproducibly and selectively eliminate the large horizontal and vertical motion sensitive neurons (H- and V-cells) of the lobula plate on one side of the brain of house fliesMusca domestica. This was achieved by ablating the precursors of these cells deep in the larval brain without damaging other cells in the brain or other tissues. The individually reared flies were tested for their behaviour. Three tests were performed: (i) visual fixation of a single stripe, (ii) the optomotor turning and thrust response to a stripe moving clockwise and counterclockwise around the fly, (iii) the monocular turning response to a moving grating. The responses to a moving single object were normal on both sides, the control side and the one lacking the H- and V-cells. However, the responses to a moving grating were reduced on the side lacking H- and V-cells for progressive (front to back) and regressive (back to front) motion. From this we conclude that the response to single objects is controlled mainly by cells other than the H- and V-cells. We also suggest two separate pathways for the processing of single object motion and wide field pattern motion respectively (Fig. 8). Furthermore, the H- and V-cells might function as visual stabilizers and background motion processors.     

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/ 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.     

Neural action fields for optic flow based navigation: a simulation study of the fly lobula plate network

Optic flow based navigation is a fundamental way of visual course control described in many different species including man. In the fly, an essential part of optic flow analysis is performed in the lobula plate, a retinotopic map of motion in the environment. There, the so-called lobula plate tangential cells possess large receptive fields with different preferred directions in different parts of the visual field. Previous studies demonstrated an extensive connectivity between different tangential cells, providing, in principle, the structural basis for their large and complex receptive fields. We present a network simulation of the tangential cells, comprising most of the neurons studied so far (22 on each hemisphere) with all the known connectivity between them. On their dendrite, model neurons receive input from a retinotopic array of Reichardt-type motion detectors. Model neurons exhibit receptive fields much like their natural counterparts, demonstrating that the connectivity between the lobula plate tangential cells indeed can account for their complex receptive field structure. We describe the tuning of a model neuron to particular types of ego-motion (rotation as well as translation around/along a given body axis) by its 'action field'. As we show for model neurons of the vertical system (VS-cells), each of them displays a different type of action field, i.e., responds maximally when the fly is rotating around a particular body axis. However, the tuning width of the rotational action fields is relatively broad, comparable to the one with dendritic input only. The additional intra-lobula-plate connectivity mainly reduces their translational action field amplitude, i.e., their sensitivity to translational movements along any body axis of the fly.     

Motion sensitive interneurons in the optomotor system of the fly

The functional properties of the three horizontal cells (north horizontal cell, HSN; equatorial horizontal cell, HSE; south horizontal cell, HSS) in the lobula plate of the blowflyCalliphora erythrocephala were investigated electrophysiologically. 1. The receptive fields of the HSN, HSE, and HSS cover the dorsal, equatorial and ventral part of the ipsilateral visual field, respectively. In all three cells, the sensitivity to visual stimulation is highest in the frontal visual field and decreases laterally. The receptive fields and spatial sensitivity distributions of the horizontal cells are directly determined by the position and extension of their dendritic fields in the lobula plate and the dendritic density distributions within these fields. 2. The horizontal cells respond mainly to progressive (front to back) motion and are inhibited by motion in the reverse direction, the preferred and null direction being antiparallel. The amplitudes of motion induced excitatory and inhibitory responses decline like a cosine function with increasing deviation of the direction of motion from the preferred direction. Stimulation with motion in directions perpendicular to the preferred direction is ineffective. 3. The preferred directions of the horizontal cells show characteristic gradual orientation changes in different parts of the receptive fields: they are horizontally oriented only in the equatorial region and increasingly tilted vertically towards the dorsofrontal and ventrofrontal margins of the visual field. These orientation changes can be correlated with equivalent changes in the local orientation of the lattice of ommatidial axes in the pertinent compound eye. 4. The response amplitudes of the horizontal cells under stimulation with a moving periodic grating depend strongly on the contrast frequency of the stimulus. Maximal responses were found at contrast frequencies of 2–5 Hz. 5. The spatial integration properties of the horizontal cells (studied in the HSE) are highly nonlinear. Under stimulation with extended moving patterns, their response amplitudes are nearly independent of the size of the stimuli. It is demonstrated that this response behaviour does not result from postsynaptic saturation in the dendrites of the cells. The results indicate that the horizontal system is essentially involved in the neural control of optomotor torque responses performed by the fly in order to minimize unvoluntary deviations from a straight flight course.     

Whole-field integration, not detailed analysis, is used by the crab optokinetic system to separate rotation and translation in optic flow

For optimal visual control of compensatory eye movements during locomotion it is necessary to distinguish the rotational and translational components of the optic flow field. Optokinetic eye movements can reduce the rotational component only, making the information contained in the translational flow readily available to the animal. We investigated optokinetic eye rotation in the marble rock crab, Pachygrapsus marmoratus, during translational movement, either by displacing the animal or its visual surroundings. Any eye movement in response to such stimuli is taken as an indication that the system is unable to separate the translational and the rotational components in the optic flow in a mathematically perfect way. When the crabs are translated within a pseudo-natural environment, eye movements are negligible, especially during sideways translation. When, however, crabs were placed in a gangway between two elongated rectangular sidewalls carrying dotted patterns which were translated back and forth, marked eye movements were elicited, depending on the translational velocity. To resolve this discrepancy, we tested several hypotheses about mechanisms using detailed analysis of the optic flow or whole-field integration. We found that the latter are sufficient to explain the efficient separation of translation and rotation of crabs in quasi-natural situations. Accepted: 6 May 1997     

To keep on track during flight,fruitflies discount the skyward view

When small flying insects go off their intended course, they use the resulting pattern of motion on their eye, or optic flow, to guide corrective steering. A change in heading generates a unique, rotational motion pattern and a change in position generates a translational motion pattern, and each produces corrective responses in the wingbeats. Any image in the flow field can signal rotation, but owing to parallax, only the images of nearby objects can signal translation. Insects that fly near the ground might therefore respond more strongly to translational optic flow that occurs beneath them, as the nearby ground will produce strong optic flow. In these experiments, rigidly tethered fruitflies steered in response to computer-generated flow fields. When correcting for unintended rotations, flies weight the motion in their upper and lower visual fields equally. However, when correcting for unintended translations, flies weight the motion in the lower visual fields more strongly. These results are consistent with the interpretation that fruitflies stabilize by attending to visual areas likely to contain the strongest signals during natural flight conditions.     

Neural population representation hypothesis of visual flow and its illusory after effect in the brain: psychophysics,neurophysiology and computational approaches

The neural representation of motion aftereffects induced by various visual flows (translational, rotational, motion-in-depth, and translational transparent flows) was studied under the hypothesis that the imbalances in discharge activities would occur in favor in the direction opposite to the adapting stimulation in the monkey MST cells (cells in the medial superior temporal area) which can discriminate the mode (i.e., translational, rotational, or motion-in-depth) of the given flow. In single-unit recording experiments conducted on anaesthetized monkeys, we found that the rate of spontaneous discharge and the sensitivity to a test stimulus moving in the preferred direction decreased after receiving an adapting stimulation moving in the preferred direction, whereas they increased after receiving an adapting stimulation moving in the null direction. To consistently explain the bidirectional perception of a transparent visual flow and its unidirectional motion aftereffect by the same hypothesis, we need to assume the existence of two subtypes of MST D cells which show directionally selective responses to a translational flow: component cells and integration cells. Our physiological investigation revealed that the MST D cells could be divided into two types: one responded to a transparent flow by two peaks at the instances when the direction of one of the component flow matched the preferred direction of the cell, and the other responded by a single peak at the instance when the direction of the integrated motion matched the preferred direction. In psychophysical experiments on human subjects, we found evidence for the existence of component and integration representations in the human brain. To explain the different motion perceptions, i.e., two transparent flows during presentation of the flows and a single flow in the opposite direction to the integrated flows after stopping the flow stimuli, we suggest that the pattern-discrimination system can select the motion representation that is consistent with the perception of the pattern from two motion representations. We discuss the computational aspects related to the integration of component motion fields.     

Prey Escape Direction is Influenced by the Pivoting Displays of Flush-Pursuing Birds

Painted redstart, Myioborus pictus, and its congeners in Central and South America, belong to a small fraction of insectivorous flush‐pursuing birds. Unlike most of the small insectivorous birds, which glean prey from substrates, the flush pursuers spread and pivot their conspicuously patterned tails and wings. This display triggers prey escape flights which are hypothesized to occur through visual stimulation of prey escape circuits [giant descending neuron cluster (GDNC) in Diptera] sensitive to the looming motion of an approaching bird, translational motion of a pivoting body with widely spread tail and contrast of the white‐black plumage pattern. In this paper, data from field observations of redstarts and experiments with bird models show an increase in the frequency of prey escapes away from the strong visual stimulation of an open tail, and in the direction opposite to that of the horizontal translational motion present in the pivots. We discuss how the effect on prey escape direction may enhance prey interception capabilities of redstarts during aerial pursuits. Combined with an earlier study the results show that, unlike the movements of typical gleaner–foragers, the flush displays by redstarts affect prey escape direction in a manner that may facilitate prey tracking and capture by birds. Because the GDNs, which mediate escape initiation, are not sensitive to motion direction, we hypothesize that other neurons, in addition to the GDNs, are involved in influencing the direction of escape responses.     

The three-dimensional optomotor torque system ofDrosophila melanogaster

Summary The well known optomotor yaw torque response in flies is part of a 3-dimensional system. Optomotor responses around the longitudinal and transversal body axes (roll and pitch) with strinkingly similar properties to the optomotor yaw response are described here forDrosophila melanogaster. Stimulated by visual motion from a striped drum rotating around an axis aligned with the measuring axis, a fly responds with torque of the same polarity as that of the rotation of the pattern. In this stimulus situation the optomotor responses for yaw, pitch and roll torque have about the same amplitudes and dynamic properties (Fig. 2). Pronounced negative responses are measured with periodic gratings of low pattern wavelengths due to geometrical interference (Fig. 3). The responses depend upon the contrast frequency rather than the angular velocity of the pattern (Fig. 4). Like the optomotor yaw response, roll and pitch responses can be elicited by small field motion in most parts of the visual field; only for motion below and behind the fly roll and pitch responses have low sensitivity.The mutantoptomotor-blind ^H31 (omb ^H31) in which the giant neurones of the lobula plate are missing or severely reduced, is impaired in all 3 optomotor torque responses (Fig. 5) whereas other visual responses like the optomotor lift/thrust response and the landing response (elicited by horizontal front-to-back motion) are not affected (Heisenberg et al. 1978).We propose that the lobula plate giant neurons mediate optomotor torque responses and that the VS-cells in particular are involved in roll and pitch but not in lift/thrust control. This hypothesis accommodates various electrophysiological and anatomical observations about these neurons in large flies.Abbreviation EMD elementary movement detector     

The vertical-horizontal neurone (VH) in the lobula plate of the blowfly,Phaenicia

Summary The anatomy and physiology of a motion-sensitive neurone, the vertical-horizontal (VH-) cell in the third visual neuropil (lobula plate) of the blowfly,Phaenicia was studied by intracellular recordings combined with dye injection. The cell possesses two dendritic fields in different layers of the lobula plate. The axon runs jointly with those of the vertical cells along the caudal surface of the lobula plate and terminates in the central protocerebrum lateral to the esophageal canal. The receptive field of the VH-cell is subdivided into two physiologically different parts which correspond to the two dendritic fields: if the input reaches the dendritic field residing in a more caudal layer (V-layer), the cell responds maximally to vertical pattern motion; whereas if the input reaches the dendritic field residing in a more rostral layer (H-layer), the cell responds maximally to horizontal pattern motion. The VH-neurone responds maximally to a contrast frequency of approximately / 1.8 Hz which coincides with the contrast frequency dependence of optomotor (following) responses. It is, therefore, considered to be a likely candidate mediating the pitch response (Blondeau and Heisenberg 1982) in flies.     

Rotational and translational swimming of human spermatozoa: a dynamic laser light scattering study

The rotational swimming motion of human spermatozoa is evaluated from measurements of depolarized dynamic laser light scattering at zero angle. The analysis is based on a Maxwellian angular velocity distribution and yields a rotational frequency of about 4 Hz that is ascribed to the rotation of the sperm head. From comparison with the translational swimming motion, a propelling efficiency of about 10 micron per turn is deduced. This parameter describes the linkage between the rotational and translational swimming motion and is likely to be discriminatory in the analysis of physiological and pathological sperm motions.     

Saccadic flight strategy facilitates collision avoidance: closed-loop performance of a cyberfly

Behavioural and electrophysiological experiments suggest that blowflies employ an active saccadic strategy of flight and gaze control to separate the rotational from the translational optic flow components. As a consequence, this allows motion sensitive neurons to encode during translatory intersaccadic phases of locomotion information about the spatial layout of the environment. So far, it has not been clear whether and how a motor controller could decode the responses of these neurons to prevent a blowfly from colliding with obstacles. Here we propose a simple model of the blowfly visual course control system, named cyberfly, and investigate its performance and limitations. The sensory input module of the cyberfly emulates a pair of output neurons subserving the two eyes of the blowfly visual motion pathway. We analyse two sensory–motor interfaces (SMI). An SMI coupling the differential signal of the sensory neurons proportionally to the yaw rotation fails to avoid obstacles. A more plausible SMI is based on a saccadic controller. Even with sideward drift after saccades as is characteristic of real blowflies, the cyberfly is able to successfully avoid collisions with obstacles. The relative distance information contained in the optic flow during translatory movements between saccades is provided to the SMI by the responses of the visual output neurons. An obvious limitation of this simple mechanism is its strong dependence on the textural properties of the environment.     

Computer-aided studies of vision in crabs

A system for the back projection of computer-generated visual images onto a screen or screens that cover 240° of the horizontal visual field is described. Its applicability for the study of crab vision is tested by comparing the frequency response of the optokinetic response of the land crab, Cardisoma guanhumi , to sinusoidal oscillation of computer-generated striped patterns and a real striped drum. Significant differences were observed only at the low end of the frequency spectrum. The flexibility of computer-generated visual stimulation and its advantages for the study of optic flow are illustrated by experiments that: (a) demonstrate how well crabs separate the translational and rotational components of optic flow by showing compensatory eye movements to only the latter; (b) show that the ability to compensate for rotation is not impaired by combinations of rotation and translation; (c) show that motion parallax cues are used in addition to previously-described global cues for making the distinction between rotation and translation. Finally, the use of these methods in a successful search for visual interneurones sensitive to optic flow stimuli is demonstrated for the shore crab, Carcinus maenas .     

Computer-aided studies of vision in crabs

A system for the back projection of computer-generated visual images onto a screen or screens that cover 240° of the horizontal visual field is described. Its applicability for the study of crab vision is tested by comparing the frequency response of the optokinetic response of the land crab, Cardisoma guanhumi, to sinusoidal oscillation of computer-generated striped patterns and a real striped drum. Significant differences were observed only at the low end of the frequency spectrum. The flexibility of computer-generated visual stimulation and its advantages for the study of optic flow are illustrated by experiments that: (a) demonstrate how well crabs separate the translational and rotational components of optic flow by showing compensatory eye movements to only the latter; (b) show that the ability to compensate for rotation is not impaired by combinations of rotation and translation; (c) show that motion parallax cues are used in addition to previously-described global cues for making the distinction between rotation and translation. Finally, the use of these methods in a successful search for visual interneurones sensitive to optic flow stimuli is demonstrated for the shore crab, Carcinus maenas.     

Active vision in insects: an analysis of object-directed zig-zag flights in wasps (Odynerus spinipes , Eumenidae)

Ground-nesting wasps (Odynerus spinipes, Eumenidae) perform characteristic zig-zag flight manoeuvres when they encounter a novel object in the vicinity of their nests. We analysed flight parameters and flight control mechanisms and reconstructed the optical flow fields which the wasps generate by these flight manoeuvres. During zig-zag flights, the wasps move sideways and turn to keep the object in their frontal visual field. Their turning speed is controlled by the relative motion between object and background. We find that the wasps adjust their rotational and translational speed in such a way as to produce a specific vortex field of image motion that is centred on the novel object. As a result, differential image motion and changes in the direction of motion vectors are maximal in the vicinity and at the edges of the object. Zig-zag flights thus seem to be a `depth from motion' procedure for the extraction of object-related depth information. Accepted: 31 August 1997     

Motion detection in the presence and absence of background motion in anAnolis lizard

Anolis lizards respond to a moving object viewed in the periphery of their visual field by turning their eye to fixate the object with their central fovea. This paper describes the relative effectiveness of different patterns of motion of a small black lure in eliciting these eye movements and the way motion of a backdrop of vegetation affects the response. The stimulus was positioned 45 degrees from the animal's line of gaze and oscillated in the vertical axis at different frequencies between 0.5 and 10 Hz. At each frequency, the amplitude of the oscillation was increased until the lizard flicked its eye towards the stimulus. The minimum amplitude needed for response (0.22 degrees of visual angle) was independent of frequency and waveform. The probability of any response occurring was, however, lower at higher frequencies (7 and 10 Hz) and a 1.5 Hz square wave evoked the greatest proportion of responses. Sinusoidal oscillation of a background of vegetation at 1.6 Hz during or before motion of the stimulus lure reduced the probability of an eye flick but did not raise the minimum amplitude needed for a response. The suppressive effect was greatest when the lure was oscillated at frequencies close to that of the background. It is concluded that Anolis, which rely upon motion to detect objects in the periphery of the visual field, filter out irrelevant motion such as that of windblown vegetation by responding preferentially to particular patterns of motion and short term habituation to commonly present patterns of motion.