Limulus vision in the marine environment.

Horseshoe crabs use vision to find mates. They can reliably detect objects resembling potential mates under a variety of lighting conditions. To understand how they achieve this remarkable performance, we constructed a cell based realistic model of the lateral eye to compute the ensembles of optic nerve activity ("neural images") it transmits to the brain. The neural images reveal a robust encocding of mate-like objects that move underwater during the day. The neural images are much less clear at night, even though the eyes undergo large circadian increases of sensitivity that nearly compensate for the millionfold decreasein underwater lighting after sundown. At night the neurral images are noisy, dominated by bursts of nerve impulses from random photon events that occur at low nighttime levels of illumination. Deciphering the eye's input to the brain begins at the first synaptic level with lowpass temporal and spatial filtering. Both neural filtering mechanisms improve the signal-to-noise properties of the eye's input, yielding clearer neural images of potential mates, especiallyat night. Insights about visual processing by the relatively simple visual system of Limulus may aid in the designof robotic sensors for the marine environment.

Cell-based model of the Limulus lateral eye.

We present a cell-based model of the Limulus lateral eye that computes the eye's input to the brain in response to any specified scene. Based on the results of extensive physiological studies, the model simulates the optical sampling of visual space by the array of retinal receptors (ommatidia), the transduction of light into receptor potentials, the integration of excitatory and inhibitory signals into generator potentials, and the conversion of generator potentials into trains of optic nerve impulses. By simulating these processes at the cellular level, model ommatidia can reproduce response variability resulting from noise inherent in the stimulus and the eye itself, and they can adapt to changes in light intensity over a wide operating range. Programmed with these realistic properties, the model eye computes the simultaneous activity of its ensemble of optic nerve fibers, allowing us to explore the retinal code that mediates the visually guided behavior of the animal in its natural habitat. We assess the accuracy of model predictions by comparing the response recorded from a single optic nerve fiber to that computed by the model for the corresponding receptor. Correlation coefficients between recorded and computed responses were typically >95% under laboratory conditions. Parametric analyses of the model together with optic nerve recordings show that animal-to-animal variation in the optical and neural properties of the eye do not alter significantly its response to objects having the size and speed of horseshoe crabs. The eye appears robustly designed for encoding behaviorally important visual stimuli. Simulations with the cell-based model provide insights about the design of the Limulus eye and its encoding of the animal's visual world.

Adapting bump model for ventral photoreceptors of Limulus.

Light-evoked current fluctuations have been recorded from ventral photoreceptors of Limulus for light intensity from threshold up to 10(5) times threshold. These data are analyzed in terms of the adapting bump noise model, which postulates that (a) the response to light is a summation of bumps; and (b) the average size of bump decreases with light intensity, and this is the major mechanism of light adaptation. It is shown here that this model can account for the data well. Furthermore, the model provides a convenient framework to characterize, in terms of bump parameters, the effects of calcium ions, which are known to affect photoreceptor functions. From responses to very dim light, it is found that the average impulse response (average of a large number of responses to dim flashes) can be predicted from knowledge of both the noise characteristics under steady light and the dispersion of latencies of individual bumps. Over the range of light intensities studied, it is shown that (a) the bump rate increases in strict proportionality to light intensity, up to approximately 10(5) bumps per second; and (b) the bump height decreases approximately as the -0.7 power of light intensity; at rates greater than 10(5) bumps per second, the conductance change associated with the single bump seems to reach a minimum value of approximately 10(-11) reciprocal ohms; (c) from the lowest to the highest light intensity, the bump duration decreases approximately by a factor of 2, and the time scale of the dispersion of latencies of individual bumps decreases approximately by a factor of 3; (d) removal of calcium ions from the bath lengthens the latency process and causes an increase in bump height but appears to have no effect on either the bump rate or the bump duration.

Dispersion of latencies in photoreceptors of Limulus and the adapting-bump model.

To light stimuli of very low intensity, Limulus photoreceptors give a voltage response with a fluctuating delay. This phenomenon has been called "latency dispersion." If the generator potential is the superposition of discrete voltage events ("bumps"), and if the effect of light upon bump size is negligible, then the latency dispersion and the bump shape completely characterize the frequency response to sinusoidal flicker. For very low light intensities, the latency dispersion of the bumps, the bump shape, and the frequency response are measured. It is found that for data obtained at 20 degrees C, the frequency response can be accounted for completely by the latency dispersion and by the bump shape derived from steady-state noise characteristics. At 10 degrees C, the time scale of the response of the photoreceptor is lengthened. The dispersion of latencies and the bump shape are found not to have the same temperature dependence. However, just as those measured at 20 degrees C, the bump shape and the dispersion of latencies measured at 10 degrees C can predict the frequency response measured under the same conditions. These results strongly suggest that the major mechanisms involved in the generator potential are the latency process and the bump process. At high light intensities, the time scale of the generator potential shortens. The decrease in time scale of the generator potential can be attributed to the decreases in time scales of the bumps and of the latency dispersion process.

Rapid dark recovery of the invertebrate early receptor potential.

The recovery in the dark of the early receptor potential, as a direct manifestation of the state of the visual pigments, has been studied by intracellular recording in the ventral photoreceptors of Limulus and lateral photoreceptors of Balanus. The recovery is exponential with 1/e time constants of about 80 ms at 24 degrees C for both preparations and 1800 ms at 4 degrees C for Balanus. The 24 degrees C rate extrapolates to total recovery of the pigment within 2 s. The later part of the dark adaptation of the late receptor potential, which may take from seconds to minutes in these preparations, appears thus to be unrelated to the state of the pigment.