Off-axis illumination elicits lateral inhibition at the primary visual synapse in crustacea and insects. The evidence suggests that the inhibitory action is presynaptic (i.e., on the photoreceptor terminal) and that the amacrine neurons of the lamina ganglionaris (the first synaptic layer) may be part of the inhibitory pathway. The neurotransmitters and the synaptic mechanisms are unknown. We show by immunocytochemistry that GABA and a tachykinin-related peptide (TRP) are localized in the amacrine neurons of the crayfish lamina ganglionaris. Indirect evidence suggests that GABA and TRP may be colocalized in these neurons. The extensive processes of the amacrine neurons occupy lamina layers containing the terminals of photoreceptors. Application of exogenous GABA and TRP to photoreceptor terminals produces a short-latency, dose-dependent hyperpolarization with a decay time constant on the order of a few seconds. TRP also exhibits actions that evolve over several minutes. These include a reduction of the receptor potential (and the light-elicited current) by approximately 40% and potentiation of the action of GABA by approximately 100%. The mechanisms of TRP action in crayfish are not known, but a plausible pathway is a TRP-dependent elevation of intracellular Ca(2+) that reduces photoreceptor sensitivity in arthropods. Although the mechanisms are not established, the results indicate that in crayfish photoreceptors TRP displays actions on two time scales and can exert profound modulatory control over cell function.

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.

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Light-evoked synaptic responses of identified visual interneurons, sustaining fibers (SFs), were quantitatively analyzed, and a neuronal cable model was used to calculate voltage attenuations and predict synaptic responses. The cable model is based on morphological measurements of SFs filled with Lucifer yellow and passive membrane properties assessed by current injection in the proximal portion of the dendritic arbor. The morphological and electrophysiological measurements were made in different preparations on homologues of the same identified interneurons. The excitatory postsynaptic potential (EPSP) elicited with high-intensity light consists of a transient phase (mean amplitude 33.1 mV) and a second phase (the plateau) that decays slowly relative to the membrane time constant (mean amplitude 24.4 mV). The mean extrapolated reversal potentials are -19.1 mV for the transient and -22.3 mV during the plateau. The change in input conductance associated with the plateau phase of the response showed a peak of 121% above the resting input conductance and decayed to approximately 50% above resting conductance over several seconds. Compartmental cable models (18, 19) were used to calculate voltage attenuations and local synaptic conductances within the SF dendritic tree. The dendrites are electrotonically compact, and voltage attenuations average 6% for current flowing distally from the recording site (injected) and 45% for current flowing proximally to the recording site. The steady-state EPSP is associated with a calculated 80% decrease in the net dendritic membrane resistivity. The synaptic response, calculated for an EPSP distributed throughout the dentritic tree (using this conductance change and the measured steady-state reversal potential) was 27.0 mV, compared with an observed mean value of 24.4 mV. The calculated relationship between steady-state EPSP amplitude and dendritic membrane resistivity (Rs) is a sigmoidal function that resembles the intensity/response function of the SF. We can therefore correctly predict the transformation from light intensity to compound EPSP amplitude by calculating the intervening synaptic membrane resistivity and voltage values. These functions are affected in a predictable manner by the passive membrane resistivity (Rm) and the EPSP reversal potentials. Tetrodotoxin (TTX) application abolished all SF spiking but left the EPSP essentially unchanged, suggesting that the neuronal pathway from photoreceptors to SFs is mainly or entirely comprised of nonspiking (i.e., TTX-insensitive) elements.

1. The graded, synaptic potentials of first-order visual interneurons (lamina monopolar cells) were examined with intracellular recordings. The spatiotemporal properties were characterized with drifting sine wave gratings and annuli. 2. Annulus-elicited inhibition is maximal for annulus-test pulse intervals of approximately 140 ms and declines exponentially. The inhibition declines with increasing annular internal radii (ri). 3. Grating responses were examined with respect to spatial and temporal frequency. The gratings elicit sinusoidal signals that are approximately linear with contrast. 4. Variations in spatial frequency produce response functions with a low-pass or modest band-pass characteristic, which are described by a difference of Gaussians sensitivity profile. The central Gaussian approximates the sensitivity profile of photoreceptors. The inhibitory Gaussian is similar to the inhibitory field estimated with annulus pulses. The peak of the inhibitory Gaussian is approximately 18% of the peak excitatory Gaussian. 5. Variations in temporal frequency generally produce transfer functions with a band-pass characteristic and a peak at 1.0 Hz. These data were described by a difference of exponentials function convolved with a low-pass filter that approximates the photoreceptor response. The inhibitory time course estimated from these data was similar to that of the annulus measurements. 6. The spatiotemporal properties of lateral inhibition are consistent with inhibitory action by the lamina amacrine neurons. The proposed model is spatiotemporally inseparable and nonrecurrent. 7. Eleven of 20 monopolar cells tested exhibited a strong orientation preference with a bias to the vertical. Photoreceptors exhibit little or no orientation preference.