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.

Polarization contrast and motion detection.

Form and motion perception rely upon the visual system's capacity to segment the visual scene based upon local differences in luminance or wavelength. It is not clear if polarization contrast is a sufficient basis for motion detection. Here we show that crayfish optomotor responses elicited by the motion of images derived from spatiotemporal variations in e-vector angles are comparable to contrast-elicited responses. Response magnitude increases with the difference in e-vector angles in adjacent segments of the scene and with the degree of polarization but the response is relatively insensitive to the absolute values of e-vector angles that compose the stimulus. The results indicate that polarization contrast can support visual motion detection.

Analysis and simulation of gain control and precision in crayfish visual interneurons.

Impulse trains in sustaining and dimming fibers of crayfish optic lobe (in situ) were elicited with sinusoidal extrinsic current and sine-wave illumination. Extrinsic currents and currents derived from postsynaptic potentials (PSPs) were used to compute the time course of the spike train with an adaptive integrate-and-fire model. The neurons exhibit variations in gain and spike timing precision related to the frequency of stimulation. These phenomena are influenced by spike-frequency adaptation and nonlinearities in the PSP. Dimming fibers exhibit relatively strong spike-frequency adaptation and an associated increase in gain with the frequency of sinusoidal extrinsic current and sine-wave illumination. The dimming fiber IPSP promotes spike train rectification, and rectification contributes to spike timing precision. Sustaining fibers exhibit weaker spike-frequency adaptation and the gain of the current-elicited response is less sensitive to stimulus frequency. The sustaining fiber excitatory PSP, however, exhibits a strong frequency-dependent nonlinearity that influences the frequency response. Spike timing precision is a function of stimulus frequency in all cells and it is enhanced by rectification of the discharge and/or resonance. In rectified responses the jitter in spike times is closely related to the variance in the times the membrane potential reaches spike threshold. These gain and spike timing results are well approximated by the simulated responses. Because the nonlinearity of the sustaining fiber PSP entails a high rate of depolarization, the PSP can increase the precision of spike timing by 10- to 100-fold compared with the response to pure sine-wave stimuli. This enhanced precision has implications for crayfish oculomotor reflexes that are driven by sustaining fibers and highly sensitive to impulse timing during transient excitation.

Encoder adaptation modulates the visual responses of crayfish interneurons.

The responses of sustaining and dimming fibers were characterized by the time varying firing rates elicited by extrinsic current and flashes of light. These data were simulated by an adaptive integrate-and-fire model. A postimpulse shunt conductance simulated spike-frequency adaptation. The correlation between observed and model current-elicited impulse rates was 0.94-0.98. However, except for a difference in input resistance (both measured and simulated), the voltage to impulse encoders of the two cell groups was similar and exhibited comparable degrees of spike-frequency adaptation (40 to 45%). The encoder model derived from current-elicited responses (with fixed parameters) was used to simulate visual responses elicited by light flashes. These simulations included a synaptic current derived from the time course of the postsynaptic potential (PSP). The sustaining fiber visual response consisted of a large excitatory PSP and high-frequency transient burst that adapted (by approximately 80%) to a low-frequency plateau discharge. The simulations indicated that spike-frequency adaptation had no effect on the transient discharge but reduced the plateau firing rate by approximately 60%. Encoder adaptation enhances the sustaining fiber response to the time derivative of the stimulus. In dimming fibers, the light flash elicits an inhibitory PSP that interrupts the "dark discharge" and an off response following the end of the flash. The simulations indicated that spike-frequency adaptation reduces the firing rate of both the dark discharge and the off response. Thus the model suggests that different effects of encoder adaptation on the two cell types arise from the same encoder mechanisms, but different actions are determined by differences in impulse rate and the time course of the discharge.

Visual signals in an optomotor reflex: systems and information theoretic analysis.

Compensatory optomotor reflexes were examined in crayfish (Procambarus clarkii) with oscillating sine wave gratings and step displacements of a single stripe. A capacitance transducer was used to measure the rotation of the eyestalk about its longitudinal axis. System studies reveal a spatial frequency response independent of velocity and stimulus amplitude and linear contrast sensitivity similar to that of neurons in the visual pathway. The reflex operates at low temporal frequencies (<0.002 Hz to 0.5 Hz) and exhibits a low-pass temporal frequency response with cut-off frequency of 0.1 Hz. Eyestalk rotation increases as a saturable function of the angular stimulus displacement. When compared to the oscillatory response, transient responses are faster, and they exhibit a lower gain for large stimulus displacements. These differences may reflect system nonlinearity and/or the presence of at least two classes of afferents in the visual pathway. Our metric for information transmission is the Kullback-Leibler (K-L) distance, which is inversely proportional to the probability of an error in distinguishing two stimuli. K-L distances are related to differences in responsiveness for variations in spatial frequency, contrast, and angular displacement. The results are interpreted in terms of the neural filters that shape the system response and the constraints that the K-L distances place on information transmission in the afferent visual pathway.