Saccadic head movements of the praying mantis, with particular reference to visual and proprioceptive information

ABSTRACT. Horizontal head movements of the praying mantis, Sphodromantis lineola Burm., were recorded continuously. They responded to the presence of a live blowfly prey in the antero-lateral visual field with a rapid saccadic head movement. The angular movement of a fixation saccade was correlated positively to the displacement of the prey from the prothoracic midline. Saccade magnitude and velocity are related. After the stimulus moved out of the visual field, the mantis made a second saccadic head movement, a return saccade towards the body midline. We observed return saccades in which the head overshot or undershot the body midline, as well as saccades which returned the head exactly to its initial position. In 92% of trials with intact mantids, the return movement succeeded eventually in rotating the head back to its initial position, whereas after removal of the neck hair plates this occurred in only 47% of trials. There is a consistent relation between saccade extent and velocity. Velocities of return saccades were slower than those of fixation saccades. It is suggested that sensory inputs from the neck hair plate proprioceptors modify both the magnitude and the angular velocity of fixation and return saccadic head movements.     

Visual stimuli that elicit visual tracking, approaching and striking behavior from an unusual praying mantis, Euchomenella macrops (Insecta: Mantodea)

In comparison to other similarly sized mantis species examined in previous studies, Euchomenella macrops has a significantly smaller head, shorter foreleg tibia, but longer prothorax which have been interpreted as specializations for the capture of smaller, slower prey. We tested this conjecture by assessing the rates at which computer generated stimuli elicit visual tracking, approaching, and striking behaviors by adult females. When presented with black disks moving erratically against a white background, strike rate rose progressively as disks enlarged up to 44 deg (visual angle) if the disks moved rapidly (e.g., 143 deg/s); at slower speeds (113, 127 deg/s), smaller disks (<27 deg) were preferred. When black moved linearly from the visual periphery to visual field center (at 73 or 143 deg/s) and then stopped, E. macrops struck consistently at disks as small as 5 deg after movement ceased. E. macrops also struck at higher rates in response to 23 deg erratically moving (subjective) red (versus subjective blue or green) disks that were luminance matched to a grey background although they tracked all colors at equally high rates. Unlike some other species, E. macrops did not strike at higher rates in response to elongated rectangular stimuli moving parallel (versus perpendicular) to their long axis, although the former elicited higher rates of approaching. An analysis of tracking behavior revealed that virtually all tracking movements were a result of head (versus) prothorax rotation.     

Tracking of small objects in front of a textured background by insects and vertebrates: phenomena and neuronal basis

To follow visually a small object moving in front of a textured background, insects and vertebrates can employ a similar strategy: saccadic tracking. In the case of vertebrates, the neural components that generate this behavior are not known in detail. The neural substrate of optomotor behavior in Diptera is relatively well understood. Here a model developed from the dipteran data is found to be capable of saccadic tracking. It is characterized by the following components and functions: (1) Two subsystems contribute to the response, a small-field tracking system and a large-field compensatory optomotor system, as suggested previously (Egelhaaf et al. 1988). (2) Both systems need to be suppressed during saccadic rotation. In the small-field system, the suppression, close to the visual input, is mediated by the activity of the large-field system. In the large-field system, suppression, close to the motor output, is due to efferent signals from the saccade generator. A similar model could also apply to vertebrates. Two implications of the present model are that saccadic tracking does not require object identification, and under saccadic tracking it is the background rather than the object that is stabilized on the retina. If objects are identified under these conditions, this must occur even though their image is not stabilized on the retina. Received: 23 July 1993/Accepted in revised form: 8 September 1993     

Simultaneous brightness contrast of foraging Papilio butterflies

This study focuses on the sense of brightness in the foraging Japanese yellow swallowtail butterfly, Papilio xuthus. We presented two red discs of different intensity on a grey background to butterflies, and trained them to select one of the discs. They were successfully trained to select either a high intensity or a low intensity disc. The trained butterflies were tested on their ability to perceive brightness in two different protocols: (i) two orange discs of different intensity presented on the same intensity grey background and (ii) two orange discs of the same intensity separately presented on a grey background that was either higher or lower in intensity than the training background. The butterflies trained to high intensity red selected the orange disc of high intensity in protocol 1, and the disc on the background of low intensity grey in protocol 2. We obtained similar results in another set of experiments with purple discs instead of orange discs. The choices of the butterflies trained to low intensity red were opposite to those just described. Taken together, we conclude that Papilio has the ability to learn brightness and darkness of targets independent of colour, and that they have the so-called simultaneous brightness contrast.     

Shrimps that pay attention: saccadic eye movements in stomatopod crustaceans

Discovering that a shrimp can flick its eyes over to a fish and follow up by tracking it or flicking back to observe something else implies a ‘primate-like’ awareness of the immediate environment that we do not normally associate with crustaceans. For several reasons, stomatopods (mantis shrimp) do not fit the general mould of their subphylum, and here we add saccadic, acquisitional eye movements to their repertoire of unusual visual capabilities. Optically, their apposition compound eyes contain an area of heightened acuity, in some ways similar to the fovea of vertebrate eyes. Using rapid eye movements of up to several hundred degrees per second, objects of interest are placed under the scrutiny of this area. While other arthropod species, including insects and spiders, are known to possess and use acute zones in similar saccadic gaze relocations, stomatopods are the only crustacean known with such abilities. Differences among species exist, generally reflecting both the eye size and lifestyle of the animal, with the larger-eyed more sedentary species producing slower saccades than the smaller-eyed, more active species. Possessing the ability to rapidly look at and assess objects is ecologically important for mantis shrimps, as their lifestyle is, by any standards, fast, furious and deadly.     

Responses to non-locomotive prey models by the praying mantis,Tenodera angustipennis Saussure

Adult females of the praying mantisTenodera angustipennis were presented with computer-generated images, and the attractiveness of “non-locomotive” prey models was examined. Mantises fixated and struck the “body and leg” model (consisting of an immobile black square on a white background with 2 black lines oscillating randomly at its sides) more frequently than the “leg” model (only oscillating lines) or the “body” model (static square only). This indicates that the model consisting of a static object and moving lines effectively elicits mantis strike behavior, although it is “non-locomotive.”     

Investigating saccade programming in the praying mantis Tenodera aridifolia using distracter interference paradigms

To investigate the saccadic system in the mantis, I applied distracter interference paradigms. These involved presenting the mantis with a fixation target and one or several distracters supposed to affect saccades towards the target. When a single target was presented, a medium-sized target located in its lower visual field elicited higher rates of saccade response. This preference for target size and position was also observed when a target and a distracter were presented simultaneously. That is, the mantis chose and fixated the target rather than a distracter that was much smaller or larger than the target, or was located above the target. Furthermore, the mantis' preference was not affected by increasing the number of distracters. However, the presence of the distracter decreased the occurrence rate of saccade and increased the response time to saccade. I conclude that distracter interference paradigms are an effective way of investigating the visual processing underlying saccade generation in the mantis. Possible mechanisms of saccade generation in the mantis are discussed.     

Predatory behavior of the praying mantis,Tenodera aridifolia II. Combined effect of prey size and predator size on the prey recognition

Predatory behavior of the praying mantis,Tenodera aridifolia, as a function of the combined effect of its size and the size of the prey was investigated by using prey models. Behavioral responses were almost identical through the nymphal development in the predator. As the mantis grew, it attacked larger prey models, suggesting that it recognizes the prey's size in accordance with its own body size. Regression analyses demonstrate that the ratio of the prey's volume to the cube and the square of the predator's length is a more important parameter for prey recognition than are the one-dimensional parameters of the prey's and the predator's sizes.     

Behavioral Responses of Adult Deathwatch Beetles,Xestobium rufovillosum de Geer (Coleoptera: Anobiidae), to Light and Dark

Video tracking equipment was used to quantify the behavior of adult deathwatch beetles, Xestobium rufovillosum in a light/dark choice chamber. Effects of insect age, sex, and mating status on this behavior were analysed. The behavior recorded included the initial direction of movement, the time taken to reach the light or dark zone, the time spent in each zone, the time spent moving in each zone and the distance moved in each zone. The results show that both male and female insects 1–12 days old prefer the light zone. Insects more than 12 days old demonstrate sexually differential photoresponsive behavior. Males show a preference for the light. Females show an increasing preference for the dark, mated females more so than unmated females. The implications of these differences in behavior are discussed in relation to control programmes.     

Effects of luminance, size, and angular velocity on the recognition of nonlocomotive prey models by the praying mantis

Adult females of the mantis Tenodera angustipennis were presented with the "nonlocomotive" prey model, a static rectangle with two lines oscillating regularly at its sides, generated on a computer display. The models were varied in rectangle luminance (black, gray, and light gray), rectangle height (0.72, 3.6, and 18 mm), rectangle width (0.72, 3.6, and 18 mm), and angular velocity of oscillating lines (65°, 260°, and 1040°/s) to examine their effects on prey recognition. Before striking the model, the mantis sometimes showed peering movements that involved swaying its body from side to side. The black model of medium size (both height and width) elicited higher rates of fixation, peering, and strike responses than the large, small, or gray model. The model of medium angular velocity elicited a higher strike rate than that of large or small angular velocity, but angular velocity had little effect on fixation and peering. We conclude that mantises respond to a rectangle in deciding whether to fixate, and to both rectangle and lines in deciding whether to strike after fixation. Received: September 2, 1999 / Accepted: March 21, 2000     

The effect of a long stay under microgravity on the vestibular function and tracking eye movements

Pre-and postflight examinations of cosmonauts participating in missions ISS-3 to ISS-9 on the International Space Station were performed using a computer-aided method of integrated assessment of the oculomotor system. The role and significance of the vestibular system in the eye tracking were determined; the individual and general characteristics of spontaneous oculomotor reactions and oculomotor reactions induced by visual and vestibular stimuli after a long-term stay at zero gravity (126–195 days) were determined; and the changes in the indices of oculomotor reactions were monitored. Studies of the vestibular function, intersensory interactions, and the tracking function of the eyes in the crew members were performed on the second, fifth (sixth), and ninth (tenth) days of the readaptation period. The results of the postflight examinations showed a significant change in the accuracy, velocity, and temporal characteristics of eye tracking and an increase in the vestibular reactivity. It was shown that the structure of visual tracking (the accuracy of fixational eye rotations and smooth tracking) was disturbed (the appearance of correcting saccades, the transition of smooth tracking to saccadic tracking) only in those cosmonauts who, in parallel to an increased reactivity of the vestibular input, also had central changes in the oculomotor system (spontaneous nystagmus, gaze nystagmus). With one exception, recovery of the indices of the accuracy of tracking eye movements in cosmonauts to the background level in the selected period of examination was not observed, although a positive trend was recorded.     

Changing the Chevreul illusion by a background luminance ramp: lateral inhibition fails at its traditional stronghold--a psychophysical refutation

The Chevreul illusion is a well-known 19^th century brightness illusion, comprising adjacent homogeneous grey bands of different luminance, which are perceived as inhomogeneous. It is generally explained by lateral inhibition, according to which brighter areas projected to the retina inhibit the sensitivity of neighbouring retinal areas. Lateral inhibition has been considered the foundation-stone of early vision for a century, upon which several computational models of brightness perception are built. One of the last strongholds of lateral inhibition is the Chevreul illusion, which is often illustrated even in current textbooks. Here we prove that lateral inhibition is insufficient to explain the Chevreul illusion. For this aim, we placed the Chevreul staircase in a luminance ramp background, which noticeably changed the illusion. In our psychophysical experiments, all 23 observers reported a strong illusion, when the direction of the ramp was identical to that of the staircase, and all reported homogeneous steps (no illusion) when its direction was the opposite. When the background of the staircase was uniform, 14 saw the illusion, and 9 saw no illusion. To see whether the change of the entire background area or that of the staircase boundary edges were more important, we placed another ramp around the staircase, whose direction was opposite to that of the original, larger ramp. The result is that though the inner ramp is rather narrow (mean = 0.51 deg, SD = 0.48 deg, N = 23), it still dominates perception. Since all conditions of the lateral inhibition account were untouched within the staircase, lateral inhibition fails to model these perceptual changes. Area ratios seem insignificant; the role of boundary edges seems crucial. We suggest that long range interactions between boundary edges and areas enclosed by them, such that diffusion-based models describe, provide a much more plausible account for these brightness phenomena, and local models are insufficient.     

不同质地背景对自由飞行蜜蜂跟踪运动目标的影响

本文研究了不同质地背景对自由飞行蜜蜂跟踪运动目标的影响.质地背景采用了灰度调制度和空间频率均可调整的双正弦波图形构成,其灰度对比幅度为64级,平均灰度为32,运动目标是一个直径3.4厘米,灰度值为32的均匀灰色圆盘.当幅度调制度从小(31%)到大(93%)变化时,蜜蜂目标跟踪系统的水平增益S1也随之增大.这是由于较大的调制度可以给予蜜峰以较大的背景与目标之间的灰度对比.从短(7.6毫米)到长(38毫米)改变质地背景的空间波长,结果显示,在空间波长为30.4毫米处有一个明显的锐起峰值.计算结果表明,质地背景与目标之间在目标边缘的灰度反差,其最大值恰好发生在空间波长等于30.4毫米的情况下.这充分说明,S1的锐起峰值完全是由于形成于此的强烈灰度反差造成的.这一结果表明:无论目标运动与否,无论背景是均匀的还是质地的,背景与目标在目标边缘形成的灰度反差对蜜蜂发现并且跟踪目标起着重要乃至决定性的作用.     

Appetitive Responses to Computer-Generated Visual Stimuli by Female Rhombodera basalis, Deroplatys lobata, Hierodula membranacea, and Miomantis sp. (Insecta: Mantodea)

We used computer-generated stimuli to assess the stimulus parameters eliciting prey-directed behaviors in four mantis species: Rhombodera basalis (60 mm body length), Deroplatys lobata (70 mm), Hierodula membranacea (80 mm), Miomantis sp (38 mm). All responded appetitively to erratically moving disks subtending 10° or more. R. basalis responded more consistently to checkered (versus solid black) disks; only D. lobata displayed a size preference (14–23 deg disks); Miomantis sp. struck at disks as large as did the largest species; only Miomantis sp. displayed approaching behavior. H. membranacea and R. basalis preferred black disks on a white background (versus the reverse), and red disks (versus blue or green) on a brightness-matched grey background. All preferred elongated stimuli moving parallel (versus perpendicular) to their long axes.     

Music for a Brighter World: Brightness Judgment Bias by Musical Emotion

A prevalent conceptual metaphor is the association of the concepts of good and evil with brightness and darkness, respectively. Music cognition, like metaphor, is possibly embodied, yet no study has addressed the question whether musical emotion can modulate brightness judgment in a metaphor consistent fashion. In three separate experiments, participants judged the brightness of a grey square that was presented after a short excerpt of emotional music. The results of Experiment 1 showed that short musical excerpts are effective emotional primes that cross-modally influence brightness judgment of visual stimuli. Grey squares were consistently judged as brighter after listening to music with a positive valence, as compared to music with a negative valence. The results of Experiment 2 revealed that the bias in brightness judgment does not require an active evaluation of the emotional content of the music. By applying a different experimental procedure in Experiment 3, we showed that this brightness judgment bias is indeed a robust effect. Altogether, our findings demonstrate a powerful role of musical emotion in biasing brightness judgment and that this bias is aligned with the metaphor viewpoint.     

The Red‐Fluorescing Marine Fish Tripterygion delaisi can Perceive its Own Red Fluorescent Colour

Many marine fishes show conspicuous red fluorescent body patterns. Recent work suggests that red fluorescence may be used as a visual colour cue in these species. Very few studies, however, have as yet been able to demonstrate that red fluorescent fish can actually perceive their own fluorescence. This is the first study to our knowledge in which a red fluorescent fish is trained to assess whether it can recognize red fluorescence. We used the triplefin Tripterygion delaisi, a species with conspicuous red fluorescent eye rings. Training and testing involved repeated binary choices between grey and red fluorescence cues. The training and testing were carried out under broad spectral illumination. The final testing phase involved cyan light illumination, mimicking natural ambient light at depth. When testing all nine combinations of three grey brightness levels against three red fluorescence brightness levels, individuals made significantly more correct choices than the random expectation under broad as well as cyan illumination. Under cyan illumination, fish trained on red chose the correct cue more often compared to fish trained on grey. An analysis of the effect of the brightness levels suggests that fish did indeed make their choices based on chromatic more than achromatic cues: The three grey levels did not affect the proportion of correct choices. We conclude that T. delaisi can perceive and respond to levels of fluorescence that are similar to its own. We also discuss the difficulties that can arise from using a binary choice design on a fish with a cryptobenthic lifestyle. We argue in favour of using sequential choice designs in future studies of T. delaisi.     

Tests of Models for Saccade–Vergence Interaction using Novel Stimulus Conditions

During natural activities, two types of eye movements - saccades and vergence - are used in concert to point the fovea of each eye at features of interest. Some electrophysiological studies support the concept of independent neurobiological substrates for saccades and vergence, namely saccadic and vergence burst neurons. Discerning the interaction of these two components is complicated by the near-synchronous occurrence of saccadic and vergence components. However, by positioning the far target below the near target, it is possible to induce responses in which the peak velocity of the vertical saccadic component precedes the peak velocity of the horizontal vergence component by approximately 75 ms. When saccade-vergence responses are temporally dissociated in this way, the vergence velocity waveform changes, becoming less skewed. We excluded the possibility that such change in skewing was due to visual feedback by showing that similar behavior occurred in darkness. We then tested a saccade-related vergence burst neuron (SVBN) model proposed by Zee et al. in J Neurophysiol 68:1624-1641 (1992), in which omnipause neurons remove inhibition from both saccadic and vergence burst neurons. The technique of parameter estimation was used to calculate optimal values for responses from human subjects in which saccadic and convergence components of response were either nearly synchronized or temporally dissociated. Although the SVBN model could account for convergence waveforms when saccadic and vergence components were nearly synchronized, it could not when the components were temporally dissociated. We modified the model so that the saccadic pulse changed the parameter values of the convergence burst units if both components were synchronized. The modified model accounted for velocity waveforms of both synchronous and dissociated convergence movements. We conclude that both the saccadic pulse and omnipause neuron inhibition influence the generation of vergence movements when they are made synchronously with saccades.     

Phase shifts in heterochromatic flicker photometry and Bidwell's ghost: A model

A simple model of brightness encoding in the retina is proposed that explains:

1. the differential phase shift needed to minimize brightness flicker in a homogeneous red-green counterphase flickering field.
2. the modulation transfer function at low temporal frequencies for flickering lights of one dominant wavelength against the background of light with another dominant wavelength.
3. the occurrence of the Hering, the Purkinje and the Hess afterimages.
4. the ability of monochromatic light to provoke the Purkinje afterimage (Bidwell's ghost).

It is shown that these effects can be treated as pure brightness effects; or that the signal processing of the opponent system is irrelevant to the results. A physiological substrate for the model is tentatively indicated. Some suggestions are made concerning possible experimental checks of the model.     

Manuo-ocular coordination in target tracking. I. A model simulating human performance

During eye tracking of a self-moved target, human subjects' performance differs from eye-alone tracking of an external target. Typical latency between target and eye motion onsets is shorter, ocular smooth pursuit (SP) saturation velocity increases and the maximum target motion frequency at which the SP system functions correctly is higher. Based on a previous qualitative model, a quantitative model of the coordination control between the arm motor system and the SP system is presented and evaluated here. The model structure maintains a high level of parallelism with the physiological system. It contains three main parts: the eye motor control (containing a SP branch and a saccadic branch), the arm motor control and the coordination control. The coordination control is achieved via an exchange of information between the arm and the eye sensorimotor systems, mediated by sensory signals (vision, proprioception) and motor command copy. This cross-talk results in improved SP system performance. The model has been computer simulated and the results have been compared with human subjects' behavior observed during previous experiments. The model performance is seen to quantitatively fit data on human subjects. Received: 6 March 1997 / Accepted in revised form: 15 July 1997