Orientation by polarized light in the crayfish dorsal light reflex: behavioral and neurophysiological studies

In decapod crustaceans, the dorsal light reflex rotates the eyestalk so that the dorsal retina faces the brightest segment of dorsal visual space. Stepwise displacements of white stripes elicit eyestalk rotations in the same direction as that of the stripe. Conversely, stepwise displacements of black stripes on a white background elicit eyestalk rotations in the opposite direction as that of the stripe. The reversal of the response with contrast inversion distinguishes the dorsal light reflex from an optokinetic reflex. When the visual scene is composed of polarized light, segmented by variations in e-vector orientation, displacement of segments containing near vertical e-vectors elicit responses similar to those elicited by a white stripe. Displacement of polarized stripes containing near horizontal e-vectors elicit eyestalk rotations similar to those elicited by a black stripe. The results are consistent with the use of polarized light in orientation. The stimulus conditions described above were also applied to visual interneurons (sustaining fibers) and oculomotor neurons and the results were generally in accord with the behavior. In the neural studies, it was possible to show that responses to polarized stripe displacements are predictable from the receptive field location and the neuron’s polarization tuning function. John P. Schroeter deceased on September 14, 2006.     

Discriminative responses of squid (Loligo pealeii) photoreceptors to polarized light

Cephalopods behaviorally respond to polarized light. Electrophysiology experiments with the squid, Loligo pealeii, demonstrated that spike responses from individual photoreceptors are a cosine2 function of the e-vector orientation of a polarized stimulus. The discrimination limit to this polarization sensitivity depended upon the difference between the orientation of a polarized stimulus with a preferred e-vector. The limit ranged from 2 degrees to 9.2 degrees with a direct stimulus in the dark or 4.8 degrees -22.1 degrees with non-directed background illumination and the cells were least discriminative at the preferred orientations. This limit can be explained partly by the variability in anatomical alignment of microvilli in the photoreceptors around a dominant axis. A few light-sensitive retinal fibers showed no polarization sensitivity. The coding of polarization information suggests that light intensity is transformed into an average spike rate. This average results from silent periods interspersed between bursts of spikes, each burst possessing a consistent interspike interval. The variations in the length and frequency of silent periods depend upon the difference between the polarization e-vector and a preferred e-vector orientation. The minimal discriminated orientation of a squid photoreceptor agrees well with the minimum behavioral discrimination of polarized light by another cephalopod, the octopus.     

Polarization vision in crayfish motion detectors

Motion detector interneurons were examined to determine their responsiveness to the motion of polarized light images (i.e. images segmented by spatial variations in e-vector angle). Computer generated images were displayed as intensity contrasts or polarization contrasts on a modified LCD projection panel. The stimuli included the motion of a single stripe (45 degrees -55 degrees /s) and the global motion of a square wave grating (3.3 degrees /s). Neurons were impaled in the medulla interna. Of the neurons which exhibited a directional response to the motion of intensity contrast stimuli, about 2/3 were also directional in the response to polarized light images. Transient (nondirectional) stimuli included looming and jittery motions. The responses to the transient motions of the polarized light images were roughly comparable to those elicited by intensity contrast. The results imply that behavioral responses to polarized light images (i.e. optokinetic and defense reflexes) may have a basis in the polarization sensitivity and synaptic organization of the medulla interna.     

Neurobiology of polarization vision in the locust Schistocerca gregaria

The polarization pattern of the blue sky serves as an important reference for spatial orientation in insects. To understand the neural mechanisms involved in sky compass orientation we have analyzed the polarization vision system in the locust Schistocerca gregaria. As in other insects, photoreceptors adapted for the detection of sky polarization are concentrated in a dorsal rim area (DRA) of the compound eye. Stationary flying locusts show polarotactic yaw-torque responses when illuminated through a rotating polarizer from above. This response is abolished after painting the DRAs. Central stages of the polarization vision system, revealed through tracing studies, include dorsal areas in the lamina and medulla, the anterior lobe of the lobula, the anterior optic tubercle, the lateral accessory lobe and the central complex. Physiological analysis of polarization-sensitive (POL) neurons has focussed on the optic tubercle and on the central complex. Each POL neuron was maximally excited at a certain e-vector (phimax) and was maximally inhibited at an e-vector perpendicular to phimax. The neurons had large visual fields, and many neurons received input from both eyes. The neuronal organization of the central complex suggests a role as a spatial compass within the locust brain.     

Cone photoreceptor mechanisms and the detection of polarized light in fish

Summary Although numerous studies have demonstrated the detection of polarized light in vertebrates, little is known of the photoreceptor mechanisms involved. Recent evidence, however, indicates that cyprinid fishes possess both ultraviolet (UV) and polarization sensitivity suggesting that some vertebrates, like many invertebrates, may employ UV-sensitive cone receptors in polarization sensitivity. In this report, we describe experiments that determine which spectral types of receptors participate in the detection of polarized light. We used a heart-rate conditioning technique to measure increment thresholds of immobilized goldfish for plane-polarized, narrow-band (10 nm half max.) spectral stimuli (380 nm, 460 nm, 540 nm, 660 nm). A typical experiment involved isolating the activity of a cone photoreceptor mechanism by chromatic adaptation and measuring increment thresholds for spectral stimuli at e-vector orientations of the polarizer between 0° to 180° in 30° steps. The UV-, green- and red-sensitive cone receptor mechanisms showed clear evidence of polarization sensitivity while the blue-sensitive cone receptor mechanism was polarizationally insensitive. The average amplitude (base to peak height on Fig. 4) of the polarization sensitivity curves (UV-, green- and red-curves) was 0.67 log unit (standard deviation of 0.12 log unit), with the UV-sensitive cone receptor mechanism most sensitive to the vertical e-vector axis and the green- and red-sensitive cone receptor mechanisms most sensitive to the horizontal e-vector axis. The observation that different cone photoreceptor mechanisms have orthogonal polarization sensitivity in fish suggests that the perception of polarized light may enhance the capacity for visual discrimination in lower vertebrates.     

Central neural coding of sky polarization in insects

Many animals rely on a sun compass for spatial orientation and long-range navigation. In addition to the Sun, insects also exploit the polarization pattern and chromatic gradient of the sky for estimating navigational directions. Analysis of polarization-vision pathways in locusts and crickets has shed first light on brain areas involved in sky compass orientation. Detection of sky polarization relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Brain areas involved in polarization processing include parts of the lamina, medulla and lobula of the optic lobe and, in the central brain, the anterior optic tubercle, the lateral accessory lobe and the central complex. In the optic lobe, polarization sensitivity and contrast are enhanced through convergence and opponency. In the anterior optic tubercle, polarized-light signals are integrated with information on the chromatic contrast of the sky. Tubercle neurons combine responses to the UV/green contrast and e-vector orientation of the sky and compensate for diurnal changes of the celestial polarization pattern associated with changes in solar elevation. In the central complex, a topographic representation of e-vector tunings underlies the columnar organization and suggests that this brain area serves as an internal compass coding for spatial directions.     

Polarized-light sensitivity in rainbow trout (Oncorhynchus mykiss): characterization from multi-unit responses in the optic nerve

Integrated spike activity of axons from the optic nerve was measured in an investigation of the e-vector sensitive mechanism underlying the ability of rainbow trout (Oncorhynchus mykiss) for orientation in downwelling, linearly-polarized light. In anaesthetized, immobilized fish, one eye was exposed to incremental light flashes which were superimposed over closely controlled background conditions. Under scotopic and various photopic conditions, intensity/response curves were generated from the on-response of the optic nerve. Relative sensitivity curves were then obtained as a function of e-vector direction for the 5 kinds of receptor cells in this trout's retina: rods, ultraviolet cones (UV), short wavelength cones (S), medium wavelength cones (M), and long wavelength cones (L).Under scotopic conditions, no sensitivity to e-vector was apparent: thus, rods do not mediate polarization sensitivity. Under photopic conditions, parr weighing 8–10 g exhibited e-vector sensitivity in two orthogonal channels. A UV stimulus (380 nm) on a white background evoked a three-peaked response (0°, 90°, and 180°) to the e-vector orientations presented in 30° increments between 0° and 180°. In contrast, when the background was illuminated with appropriate short and long wavelength cut-off filters, M-and L-cones showed maximum responses only to the horizontal (90°) plane whether they were stimulated at their -absorption band or their -absorption band in the near UV. Isolated UV-cones gave maximum responses to the vertical (0° and 180°) e-vector, thus corresponding to a second channel. The blue sensitive, S-cones, did not show evidence of polarization sensitivity. As well, no evidence of the polarization sensitivity was observed under UV isolating background conditions in larger individuals, 50–78 g smolts, although the other cone mechanisms responded as in smaller individuals.     

Polarotaxis and scototaxis in the supratidal amphipod Platorchestia platensis

Talitrid amphipods use many cues for orientation during forays between temporary burrows and feeding areas, and for locating beaches when submerged, with visual cues being particularly important. Little evidence exists for polarized light among these visual cues despite extensive orientation by celestial and underwater polarized light in other crustaceans and in insects. We used electroretinography to assess spectral sensitivity in the eye of the beach flea Platorchestia platensis, and behavioral studies to test whether linearly polarized light serves as an orientation cue. Two spectral classes were present in the P. platensis eye with maxima at 431 and 520 nm. Non-uniform orientation of amphipods in the laboratory arena required either light/dark or polarized cues. Scototactic movements depended on arena conditions (day/night, wet/dry), while orientation under linearly polarized light was wavelength-dependent and parallel to the e-vector. Subsequent tests presented conflicting and additive scototactic and polarotactic cues to differentiate among these responses. In dry conditions, orientation parallel to the polarization e-vector overcame a dominant negative scototaxis, confirming that polarotaxis and scototaxis are separate orientation responses in this species. These behavioral results demonstrate talitrid amphipods can perceive and orient to linearly polarized light, and may use it to orient toward preferred zones on beaches.     

Polarized skylight orientation in the desert antCataglyphis

Summary The desert antCataglyphis bicolor is able to use the pattern of polarized light in the sky as compass. By confronting the ant to single spots of artificially and naturally polarized light it is shown howCataglyphis uses the polarization pattern.When exposed to a horizontal e-vector,Cataglyphis was always oriented correctly. Orientation errors occurred, however, when other e-vector directions were presented. This indicates that the e-vector positions assumed by the ant do not coincide with the e-vector positions actually realized in the sky. From this it is concluded thatCataglyphis has no detailed knowledge of the actual azimuthal positions of the e-vectors. Instead, it is relying on a simplified celestial map of the polarization patterns in the sky (Fig. 7).Usually, the ant did not confuse celestial spots with identical e-vector directions. Even at sunset when the polarization pattern is completely ambiguous, correct orientation occurred. This suggests that the ant uses additional celestial cues such as the degree of polarization, the color or the intensity to find its way home when the sun is obscured.     

Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors

Different classes of photoreceptors (PRs) allow animals to perceive various types of visual information. In the Drosophila eye, the outer PRs of each ommatidium are involved in motion detection while the inner PRs mediate color vision. In addition, flies use a specialized class of inner PRs in the "dorsal rim area" of the eye (DRA) to detect the e-vector of polarized light, allowing them to exploit skylight polarization for orientation. We show that homothorax is both necessary and sufficient for inner PRs to adopt the polarization-sensitive DRA fate instead of the color-sensitive default state. Homothorax increases rhabdomere size and uncouples R7-R8 communication to allow both cells to express the same opsin rather than different ones as required for color vision. Homothorax expression is induced by the iroquois complex and the wingless (wg) pathway. However, crucial wg pathway components are not required, suggesting that additional signals are involved.     

Evidence for true polarization vision based on a two-channel analyzer system in the eye of the water bug,Notonecta glauca

Summary Water bugs (Notonecta glauca) were set into flight in a room with a homogeneously illuminated ceiling and a light-emitting platform on the floor. In these conditions polarized UV light from the platform was more effective in causing the animals to fly down to the surface of the platform than was unpolarized UV light several times as intense. Experiments with an array of baffles that restricted the directions from which the polarization film on the platform could be seen showed that the polarized UV light is effective in eliciting descent only when the e-vector is perpendicular to the median sagittal plane of the animal (horizontal). It can be concluded that polarized UV light with horizontal e-vector is distinguished, as a special sensory quality, from unpolarized UV light.Notonecta thus provides an example of true polarization vision.The special orthogonal arrangement of the microvilli in the rhabdomeres of the UV visual cells in the ventral part of the eye (cf. Schwind 1983 b and Schwind et al., in press) is suggestive with regard to polarization vision. The microvilli of the two UV visual cells in the ommatidia looking forward and down are horizontal and vertical, respectively, and hence could serve as a two-channel analyzer system capable of distinguishing the polarized UV light reflected by a water surface from unpolarized UV light.     

Orientation in pied flycatchers: the relative importance of magnetic and visual information at dusk

We investigated the orientation of juvenile pied flycatchers, Ficedula hypoleuca, during autumn migration in south Sweden using orientation cage experiments, to study the relative importance of visual and magnetic information at sunset. We performed cage tests under 12 experimental conditions that manipulated the geomagnetic and visual sunset cues available for orientation: natural clear skies in the local or a vertical magnetic field; simulated total overcast in the local or a vertical magnetic field; natural pattern of skylight polarization and directional information from stars screened off, with the sun's position as normal or shifted 120 degrees anticlockwise with mirrors; reduced polarization in the local or a vertical magnetic field; directions of polarization (e-vector) NE/SW and NW/SE, respectively, in the local or a vertical magnetic field. The pied flycatchers were significantly oriented towards slightly south of west when they could use a combination of skylight and geomagnetic cues. The mean orientation was significantly shifted along with the deflection of the sunset position by mirrors. Reduced polarization had no significant effect on orientation either in the local, or in a vertical, magnetic field. The birds tended to orient parallel with the axis of polarization, but only when the artificial e-vector was aligned NW/SE. The mean orientation under simulated total overcast in a vertical, and in the local, magnetic field was not significantly different from random. It is difficult to rank either cue as dominant over the other and we conclude that both visual and magnetic cues seem to be important for the birds' orientation when caught and tested during active migration. Copyright 1999 The Association for the Study of Animal Behaviour.     

Evidence for instantaneous e-vector detection in the honeybee using an associative learning paradigm

Many insects use the polarization pattern of the sky for obtaining compass information during orientation or navigation. E-vector information is collected by a specialized area in the dorsal-most part of the compound eye, the dorsal rim area (DRA). We tested honeybees' capability of learning certain e-vector orientations by using a classical conditioning paradigm with the proboscis extension reflex. When one e-vector orientation (CS+) was associated with sugar water, while another orientation (CS-) was not rewarded, the honeybees could discriminate CS+ from CS-. Bees whose DRA was inactivated by painting did not learn CS+. When ultraviolet (UV) polarized light (350 nm) was used for CS, the bees discriminated CS+ from CS-, but no discrimination was observed in blue (442 nm) or green light (546 nm). Our data indicate that honeybees can learn and discriminate between different e-vector orientations, sensed by the UV receptors of the DRA, suggesting that bees can determine their flight direction from polarized UV skylight during foraging. Fixing the bees' heads during the experiments did not prevent learning, indicating that they use an 'instantaneous' algorithm of e-vector detection; that is, the bees do not need to actively scan the sky with their DRAs ('sequential' method) to determine e-vector orientation.     

Spectral and Polarization Sensitivity of the Dipteran Visual System

Spectral and polarization sensitivity measurements were made at several levels (retina, first and third optic ganglion, cervical connective, behavior) of the dipteran visual nervous system. At all levels, it was possible to reveal contributions from the retinular cell subsystem cells 1 to 6 or the retinular cell subsystem cells 7 and 8 or both. Only retinular cells 1 to 6 were directly studied, and all possessed the same spectral sensitivity characterized by two approximately equal sensitivity peaks at 350 and 480 nm. All units of both the sustaining and on-off variety in the first optic ganglion exhibited the same spectral sensitivity as that of retinular cells 1 to 6. It was possible to demonstrate for motion detection and optomotor responses two different spectral sensitivities depending upon the spatial wavelength of the stimulus. For long spatial wavelengths, the spectral sensitivity agreed with retinular cells 1 to 6; however, the spectral sensitivity at short spatial wavelengths was characterized by a single peak at 465 nm reflecting contributions from the (7, 8) subsystem. Although the two subsystems exhibited different spectral sensitivities, the difference was small and no indication of color discrimination mechanisms was observed. Although all retinular cells 1 to 6 exhibited a preferred polarization plane, sustaining and on-off units did not. Likewise, motion detection and optomotor responses were insensitive to the polarization plane for long spatial wavelength stimuli; however, sensitivity to select polarization planes was observed for short spatial wavelengths.     

Reviving a neglected celestial underwater polarization compass for aquatic animals

Substantial in situ measurements on clear days in a variety of marine environments at depths in the water down to 200 m have demonstrated the ubiquitous daytime presence of sun-related e-vector (=plane of polarization) patterns. In most lines of sight the e-vectors tilt from horizontal towards the sun at angles equal to the apparent underwater refracted zenith angle of the sun. A maximum tilt-angle of approximately 48.5 degrees , is reached in horizontal lines of sight at 90 degrees to the sun's bearing (the plane of incidence). This tilt limit is set by Snell's window, when the sun is on the horizon. The biological literature since the 1980s has been pervaded with assumptions that daytime aquatic e-vectors are mainly horizontal. This review attempts to set the record straight concerning the potential use of underwater e-vectors as a visual compass and to reopen the field to productive research on aquatic animals' orientation and navigation.     

Navigation by light polarization in clear and turbid waters

Certain terrestrial animals use sky polarization for navigation. Certain aquatic species have also been shown to orient according to a polarization stimulus, but the correlation between underwater polarization and Sun position and hence the ability to use underwater polarization as a compass for navigation is still under debate. To examine this issue, we use theoretical equations for per cent polarization and electric vector (e-vector) orientation that account for the position of the Sun, refraction at the air-water interface and Rayleigh single scattering. The polarization patterns predicted by these theoretical equations are compared with measurements conducted in clear and semi-turbid coastal sea waters at 2 m and 5 m depth over sea floors of 6 m and 28 m depth. We find that the per cent polarization is correlated with the Sun's elevation only in clear waters. We furthermore find that the maximum value of the e-vector orientation angle equals the angle of refraction only in clear waters, in the horizontal viewing direction, over the deeper sea floor. We conclude that navigation by use of underwater polarization is possible under restricted conditions, i.e. in clear waters, primarily near the horizontal viewing direction, and in locations where the sea floor has limited effects on the light's polarization.     

Behavioural relevance of polarization sensitivity as a target detection mechanism in cephalopods and fishes

Aquatic habitats are rich in polarized patterns that could provide valuable information about the environment to an animal with a visual system sensitive to polarization of light. Both cephalopods and fishes have been shown to behaviourally respond to polarized light cues, suggesting that polarization sensitivity (PS) may play a role in improving target detection and/or navigation/orientation. However, while there is general agreement concerning the presence of PS in cephalopods and some fish species, its functional significance remains uncertain. Testing the role of PS in predator or prey detection seems an excellent paradigm with which to study the contribution of PS to the sensory assets of both groups, because such behaviours are critical to survival. We developed a novel experimental set-up to deliver computer-generated, controllable, polarized stimuli to free-swimming cephalopods and fishes with which we tested the behavioural relevance of PS using stimuli that evoke innate responses (such as an escape response from a looming stimulus and a pursuing behaviour of a small prey-like stimulus). We report consistent responses of cephalopods to looming stimuli presented in polarization and luminance contrast; however, none of the fishes tested responded to either the looming or the prey-like stimuli when presented in polarization contrast.     

Quantification of phase synchronization phenomena and their importance for verbal memory processes

The tangential neurons in the lobula plate region of the flies are known to respond to visual motion across broad receptive fields in visual space.When intracellular recordings are made from tangential neurons while the intact animal is stimulated visually with moving natural imagery,we find that neural response depends upon speed of motion but is nearly invariant with respect to variations in natural scenery. We refer to this invariance as velocity constancy. It is remarkable because natural scenes, in spite of similarities in spatial structure, vary considerably in contrast, and contrast dependence is a feature of neurons in the early visual pathway as well as of most models for the elementary operations of visual motion detection. Thus, we expect that operations must be present in the processing pathway that reduce contrast dependence in order to approximate velocity constancy.We consider models for such operations, including spatial filtering, motion adaptation, saturating nonlinearities, and nonlinear spatial integration by the tangential neurons themselves, and evaluate their effects in simulations of a tangential neuron and precursor processing in response to animated natural imagery. We conclude that all such features reduce interscene variance in response, but that the model system does not approach velocity constancy as closely as the biological tangential cell.     

Modeling and measuring the visual detection of ecologically relevant motion by an Anolis lizard

Motion in the visual periphery of lizards, and other animals, often causes a shift of visual attention toward the moving object. This behavioral response must be more responsive to relevant motion (predators, prey, conspecifics) than to irrelevant motion (windblown vegetation). Early stages of visual motion detection rely on simple local circuits known as elementary motion detectors (EMDs). We presented a computer model consisting of a grid of correlation-type EMDs, with videos of natural motion patterns, including prey, predators and windblown vegetation. We systematically varied the model parameters and quantified the relative response to the different classes of motion. We carried out behavioral experiments with the lizard Anolis sagrei and determined that their visual response could be modeled with a grid of correlation-type EMDs with a spacing parameter of 0.3° visual angle, and a time constant of 0.1 s. The model with these parameters gave substantially stronger responses to relevant motion patterns than to windblown vegetation under equivalent conditions. However, the model is sensitive to local contrast and viewer-object distance. Therefore, additional neural processing is probably required for the visual system to reliably distinguish relevant from irrelevant motion under a full range of natural conditions.