Linear information processing in the retina: a study of horizontal cell responses.

Abstract

A basic question about visual perception is whether the retina produces a faithful or a distorted neural representation of the visual image. It is now well known that in some retinal pathways there are significant nonlinear transductions which distort the neural image. The next natural question is, What are the locations of the nonlinear stages within the retinal network? We report here on an investigation of linearity and nonlinearity ofresponses ofhorizontal cells in the turtle retina as an assay of the degree of nonlinearity in the outer plexiform layer of the retina. The visual stimuli were sinusoidal gratings; these patterns were modulated by contrast reversal with a sinusoidal time course. The conclusion from our experiments is that the turtle's horizontal cell responses show evidence only oflinear spatial summation even at moderately high contrasts on moderately high background levels. Our work thus indicates that there is no significant distortion of the visual image by the photoreceptors or by the neural summation of photoreceptor signals by horizontal cells under normal physiological conditions. These results are consistent with the view that the major nonlinearities ofthe retina are proximal to the outer plexiform layer.Horizontal cells in several fish retinas have been reported to be nearly linear in their response to diffuse illumination (1-3). A model based on the concept that the network of electrically coupled horizontal cells behaves as a single flat cell with passive spread of current injected at the synapses works well for horizontal cells ofcatfish (4, 5) and turtles (6). When the membrane conductance changes caused by the light stimulus are not too large, this model implies linear spatial summation. Horizontal cells in the cat respond to sinusoidal modulation of the luminance of spots with significant harmonic distortion only when relatively high modulation depths are used at frequencies below 2-3 Hz (7).We report here that luminosity horizontal cells (which hyperpolarize to all wavelengths of light) in the turtle and their presynaptic receptors act as linear tranducers in response to diffuse illumination and also in response to spatial patterns which test properties of spatial summation. METHODSIntracellular recordings were obtained from horizontal cells in isolated eye-cup preparations ofPseudemys scripta elegans (redeared turtle) and Chelydra serpentina (common snapping turtle) which gave similar results. The eye-cups were maintained in a moist oxygenated chamber at 16-20'C. Fine-tipped microelectrodes filled with 4 M potassium acetate (resistance, 100-300 MI) gave satisfactory results. The visual stimulus was a raster type display produced on a cathode ray tube oscilloscope screen (Tektronix 5103N, P31 phosphor, which has its spectral peak at 525 nm) by a special-purpose microcomputer (8) which also signal-averaged the response. A monochromator was used to test the spectral sensitivity of the neurons. The stimuli in these experiments were like those used in the past for studying...

Dynamics of turtle cones.

“…This minimizes the static compression nonlinearity caused by large response excursions . These two factors have probably contributed to the finding that turtle horizontal cell responses produced by a modulated light were linear (Tranchina et al, 1981 ;Chappell et al, 1985). The findings in horizontal cells substantiate the present observation that turtle receptors produce linear responses to a modulated stimulus because the waveforms of receptor and (field-evoked) horizontal cell responses are very similar (Fig.…”

“…White-noise or similar analysis performed so far on distal neurons in the turtle receptor and cone horizontal cells (Tranchina et al, 1981(Tranchina et al, , 1983Chappell et al, 1985), on catfish cone horizontal and bipolar, cells (Naka et al, 1975;Naka, 1985), and on the ocellar second-order neurons (Mizunami et al, 1986) has produced similar results. (a) The cells' response to white-noise-modulated light is linearly related to the modulation .…”

Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction

“…Ribbon synapses in the visual pathway possess similar properties (33)(34)(35)(36). The presynaptic stimulus pattern is reproduced in the postsynaptic neurons due to the near linear relationships between membrane potential, calcium current, and exocytosis (4,37).…”

Synaptic transmission at retinal ribbon synapses

“…Linearity in the transmission of small signals from rod photoreceptors to their post-synaptic targets has long been known (Tranchina et al, 1981;Sakai and Naka, 1987;Naka et al, 1987;Wu, 1985); it allows a rod to translate a small light-evoked hyperpolarization from the dark potential into a proportional small change in the magnitude of I Ca and exocytosis. These studies of synaptic gain, however, do not establish an underlying linear mechanism because the predictions using models based either on linear or higher-order relations between Ca 2+ influx and transmitter release do not differ greatly for small signals.…”