Contrast gain reduction in fly motion adaptation.

In many species, including humans, exposure to high image velocities induces motion adaptation, but the neural mechanisms are unclear. We have isolated two mechanisms that act on directionally selective motion-sensitive neurons in the fly's visual system. Both are driven strongly by movement and weakly, if at all, by flicker. The first mechanism, a subtractive process, is directional and is only activated by stimuli that excite the neuron. The second, a reduction in contrast gain, is strongly recruited by motion in any direction, even if the adapting stimulus does not excite the cell. These mechanisms are well designed to operate effectively within the context of motion coding. They can prevent saturation at susceptible nonlinear stages in processing, cope with rapid changes in direction, and preserve fine structure within receptive fields.

Sexual dimorphism matches photoreceptor performance to behavioural requirements.

Differences in behaviour exist between the sexes of most animal species and are associated with many sex-specific specializations. The visual system of the male housefly is known to be specialized for pursuit behaviour that culminates in mating. Males chase females using a high-acuity region of the fronto-dorsal retina (the 'love spot') that drives sex-specific neural circuitry. We show that love spot photoreceptors of the housefly combine better spatial resolution with a faster electrical response, thereby allowing them to code higher velocities and smaller targets than female photoreceptors. Love spot photoreceptors of males are more than 60% faster than their female counterparts and are among the fastest recorded for any animal. The superior response dynamics of male photoreceptors is achieved by a speeding up of the biochemical processes involved in phototransduction and by a tuned voltage-activated conductance that boosts the membrane frequency response. These results demonstrate that the inherent plasticity of phototransduction facilitates the tuning of the dynamics of visual processing to the requirements of visual ecology.

Afterimages in fly motion vision.

Afterimage-like effects modulate the responses of fly wide-field motion-sensitive cells following adaptation to stationary or slowly moving patterns. The origin of these afterimages is unclear. They have been interpreted as either the result of adaptation in the early visual system or as a direct consequence of the correlation scheme of motion detection. Using a combination of intracellular recording and computer modelling, we find that afterimage-like effects cannot be satisfactorily explained by a simple version of the correlation model previously proposed by Egelhaaf and Borst (J. Opt. Soc. Am. A 6 (1) (1989) 116). We propose a modified variant of the correlation model featuring a short delay filter and temporal high-pass filtering prior to motion correlation. Our model gives superior predictions of afterimage-like effects induced by a range of stimuli. Our model also predicts changes in cells' image step responses following exposure to motion, suggesting that previous experimental evidence for the "shortening delay" theory of motion adaptation (Biol. Cybern. 54 (1986) 223; Visual Neurosci. 14 (4) (1997) 741) should be re-interpreted in terms of afterimage effects.

Adaptation and the temporal delay filter of fly motion detectors.

Recent accounts attribute motion adaptation to a shortening of the delay filter in elementary motion detectors (EMDs). Using computer modelling and recordings from HS neurons in the drone-fly Eristalis tenax, we present evidence that challenges this theory. (i) Previous evidence for a change in the delay filter comes from 'image step' (or 'velocity impulse') experiments. We note a large discrepancy between the temporal frequency tuning predicted from these experiments and the observed tuning of motion sensitive cells. (ii) The results of image step experiments are highly sensitive to the experimental method used. (iii) An apparent motion stimulus reveals a much shorter EMD delay than suggested by previous 'image step' experiments. This short delay agrees with the observed temporal frequency sensitivity of the unadapted cell. (iv) A key prediction of a shortening delay filter is that the temporal frequency optimum of the cell should show a large shift to higher temporal frequencies after motion adaptation. We show little change in the temporal or spatial frequency (and hence velocity) optima following adaptation.

Spatio-temporal properties of motion detectors matched to low image velocities in hovering insects.

Our recent study [O'Carroll et al. (1996). Nature 382, 63-66) described a correlation between the spatio-temporal properties of motion detecting neurons in the optic lobes of flying insects and behaviour. We consider here theoretical properties of insect motion detectors at very low image velocities and measure spatial and temporal sensitivity of neurons in the lobula complex of two specialised hovering insects, the bee-fly Bombylius and the hummingbird hawkmoth, Macroglossum. The spatio-temporal optima of direction-selective neurons in these insects lie at lower velocities than those of other insects which we have studied, including large syrphid flies, which are also excellent hoverers. We argue that spatio-temporal optima reflect a compromise between the demands of diverse behaviour, which can involve prolonged periods of stationary, hovering flight followed by spectacular high speed pursuits of conspecifics. Males of the syrphid Eristalis which engage in such behaviour, have higher temporal frequency optima than females. High contrast sensitivity in these flies nevertheless results in reliable responses at very low image velocities. Neurons of Bombylius have two distinct velocity optima, suggesting that they sum inputs from two classes of motion correlator with different time constants. This also provides sensitivity to a large range of velocities.

Velocity constancy and models for wide-field visual motion detection in insects.

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.

Temperature and the temporal resolving power of fly photoreceptors.

A hot head gives an insect a clearer view of a moving world because warming reduces motion blur by accelerating photoreceptor responses. Over a natural temperature range, 19-34 degrees C, the speed of response of blowfly (Calliphora vicina) photoreceptors more than doubles, to produce the fastest functional responses recorded from an ocular photoreceptor. This acceleration increases temporal resolving power, as indicated by the corner frequency of the response power spectrum. When light adapted, the corner frequency increases from 53 Hz to 119 Hz with a Q10 of 1.9, and when dark adapted from 8 Hz to 32 Hz with a Q10 of 3.0. Temperature sensitivity originates in the phototransduction cascade, and is associated with signal amplification. The temperature sensitivity of photoreceptors must be taken into account when studying the mechanisms, function and ecology of vision, and gives a distinct advantage to insects that thermoregulate.

Polarized light detection in spiders.

We describe here the detection of polarized light by the simple eyes of spiders. Using behavioural, morphological, electrophysiological and optical studies, we show that spiders have evolved two different mechanisms to resolve the e-vector of light. Wolf spiders (Lycosidae), are able to turn in response to rotation of a polarized pattern at the zenith of their visual fields, and we also describe a strip in the ventral retina of the principal (anterio-median) eyes that views this location and has receptors tiered into two layers. This provides each pair of receptors with a similar optical solution to that provided by the 'dorsal rim area' of the insect compound eye. In contrast, gnaphosid spiders have evolved a pair of lensless secondary eyes for the detection of polarized light. These two eyes, each sensitive to orthogonal directions of polarization, are perfectly designed to integrate signals from the larger part of the sky and cooperate to analyse the polarization of light. Built-in polarizers help to improve signal purity. Similar organisation in the eyes of several other spider families suggests that these two mechanisms are not restricted to only a few families.

Accuracy of velocity estimation by Reichardt correlators.

Although a great deal of experimental evidence supports the notion of a Reichardt correlator as a mechanism for biological motion detection, the correlator does not signal true image velocity. This study examines the accuracy with which realistic Reichardt correlators can provide velocity estimates in an organism's natural visual environment. The predictable statistics of natural images imply a consistent correspondence between mean correlator response and velocity, allowing the otherwise ambiguous Reichardt correlator to act as a practical velocity estimator. Analysis and simulations suggest that processes commonly found in visual systems, such as prefiltering, response compression, integration, and adaptation, improve the reliability of velocity estimation and expand the range of velocities coded. Experimental recordings confirm our predictions of correlator response to broadband images.

Insect motion detectors matched to visual ecology.

To detect motion, primates, birds and insects all use local detectors to correlate signals sampled at one location in the image with those sampled after a delay at adjacent locations. These detectors can adapt to high image velocities by shortening the delay. To investigate whether they use long delays for detecting low velocities, we compared motion-sensitive neurons in ten species of fast-flying insects, some of which encounter low velocities while hovering. Neurons of bee-flies and hawkmoths, which hover, are tuned to lower temporal frequencies than those of butterflies and bumblebees, which do not. Tuning to low frequencies indicates longer delays and extends sensitivity to lower velocities. Hoverflies retain fast temporal tuning but use their high spatial acuity for sensing low-velocity motion. Thus an unexpectedly wide range of spatio-temporal tuning matches motion detection to visual ecology.