Transfer of graded potentials at the photoreceptor-interneuron synapse.

Abstract

To characterize the transfer of graded potentials and the properties of the associated noise in the photoreceptor-interneuron synapse of the blowfly (CaUiphora vicina) compound eye, we recorded voltage responses of photoreceptors (R1-6) and large monopolar cells (LMC) evoked by: (a) steps of light presented in the dark; (b) contrast steps; and (c) pseudorandomly modulated contrast stimuli at backgrounds covering 6 log intensity units. Additionally, we made recordings from photoreceptor axon terminals. Increased light adaptation gradually changed the synaptic signal transfer from low-pass to band-pass filtering. This was accompanied by decreased synaptic delay and increased contrast gain, but the overall synaptic gain and the intrinsic noise (i.e., transmission noise) were reduced. Based on these results, we describe a descriptive synaptic model, in which the kinetics of the tonic transmitter (histamine) release from the photoreceptor axon terminals change with mean photoreceptor depolarization. During signal transmission, tonic transmitter release is augmented by voltage-dependent contrast-enhancing mechanisms in the photoreceptor axons that produce fast transients from the rising phases of the photoreceptor responses and add these enhanced voltages to the original photoreceptor responses. The model can predict the experimental findings and it agrees with the recently proposed theory of maximizing sensory information.

Correlation between OFF and ON Channels Underlies Dark Target Selectivity in an Insect Visual System

“…Spatial antagonism of the first-order interneurons (LMCs) was implemented via weighted subtraction of nearest neighbors in the hexagonally sampled inputs to allow transmission of 70% static luminance and thus match the weak lateral inhibition described from LMC recordings in the same dragonfly species (Laughlin, 1974). LMC temporal filters were derived from Juusola et al (1995), implemented with a relaxed high-pass filter (lower corner frequency 8 Hz) and a small DC component (10%).…”

“…Such complex temporal filtering would lead to weak outputs from even a purely multiplicative ESTMD. In addition to varying the term coefficients, we further tested two model variants ( ϭ 200 ms, ϭ 100 ms) that simulate variation in high-pass filtering that could represent differences in the state of light adaptation (Juusola et al, 1995;van Hateren and Snippe, 2001) or even a change in temperature (Tatler et al, 2000). At low contrasts (Fig.…”

TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

“…The oscillations were exacerbated at dim conditions (Fig. 7B), where the gain of both the photoreceptor output synapses and synaptic feedbacks is the highest (Juusola et al, 1995;Zheng et al, 2006), thereby leaving the lamina network most perturbable to intrinsic activity. Longer recordings indicated that the oscillations in mutant LMCs carried different frequencies during and after light adaptation (Fig.…”

The Performance of Synapses That Convey Discrete Graded Potentials in an Insect Visual Pathway

“…The smallest change in presynaptic potential that can be transmitted reliably is a measure of resolution, and, at the inhibitory synapses between L-neurons, unreliability in transmission limits the number of discrete signal levels they can convey to ϳ5 at best. In contrast, in fly compound eyes recordings of responses to light stimuli from photoreceptors or second-order large monopolar cells (LMCs) (Laughlin et al, 1987;Juusola et al, 1995) indicate a performance an order of magnitude better, enabling LMCs to resolve 2% modulations in light intensity (Laughlin, 1989). In daylight, the photoreceptor to LMC synapse contributes 50 -70% of the noise in the LMC, the remainder originating in photoreceptors (Laughlin et al, 1987).…”