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Uniformity detector retinal ganglion cells fire complex spikes and receive only light-evoked inhibition - PubMed

  • ️Fri Jan 01 2010

Uniformity detector retinal ganglion cells fire complex spikes and receive only light-evoked inhibition

Benjamin Sivyer et al. Proc Natl Acad Sci U S A. 2010.

Abstract

Retinal ganglion cells convey information by increasing their firing in response to an optimal visual stimulus or "trigger feature." However, one class of ganglion cell responds to changes in the visual scene by decreasing its firing. These cells, termed uniformity detectors in the rabbit retina, are encountered only rarely and the synaptic mechanisms underlying their unusual responses have not been investigated. In this study, patch-clamp recordings of uniformity detectors show that the action potentials underlying the maintained firing arise within "complex spikes." Both ON and OFF visual stimuli elicit only inhibitory synaptic input, the immediate effect of which is to suppress the maintained firing. However, this inhibition also alters the properties of the "renascent" spiking by increasing the amplitude of the spikes within each burst, suggesting that the effect may increase the efficacy of spike propagation and transmission.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Uniformity detectors (UDs) show maintained firing that is suppressed at light ON and light OFF and they have bistratified dendritic trees. (A) Extracellular recording of the spike responses of a UD to a light spot (Upper) and a dark spot (Lower) flashed in the receptive field; the light and dark bars show the 6-s duration of the flash. (B) Spike raster plots from 13 UDs in response to 3–5 trials of a flashing dark spot. (C) Average spike rate (± SD, gray shading) for the 13 raster plots. (D) Tracing of the dendritic morphology of a Neurobiotin-filled UD reconstructed from a confocal z series. (Scale bar: 50 μm.) Characteristically, some of the dendrites in the proximal ON sublamina of the inner plexiform layer (green) arise retroflexively from dendrites in the distal OFF sublamina (magenta). (E) Vertical projection of the same cell (white) showing the dendritic stratification in relation to strata 1–5 of the inner plexiform layer and the populations of starburst amacrine cells, labeled with an antibody against choline actyltransferase (ChAT, blue).

Fig. 2.
Fig. 2.

Visual stimuli evoke transient inhibitory inputs that are mediated by glycinergic amacrine cells. (A) Voltage-clamp recording from a UD that was held at a range potentials from –100 mV to –25 mV while a dark spot was flashed in the receptive field. When the cell was clamped at –70 mV (red trace), close to the calculated inhibitory reversal potential of –73 mV, the large synaptic currents transiently evoked at light OFF and light ON disappeared. (B) Calculated mean (± SD) synaptic inhibitory conductance (Gi) and excitatory conductance (Ge) evoked by a flashing dark spot in 23 UDs. (C) The integrated inhibitory conductance (± SEM) of the OFF response (filled bars) and ON response (open bars) to a flashing dark spot while the retina was superperfused with 10 μM SR-95531 (n = 5), 1 μM strychnine (n = 7; P = 0.019 OFF, P = 0.005 ON), and 20 μM L-AP4 (n = 4; P = 0.5 OFF, P = 0.001 ON).

Fig. 3.
Fig. 3.

UDs produce complex spikes whose burst frequency is modulated by hyperpolarization. (A) The complex spikes of UDs comprise fast spikes riding on a slow depolarization (Control); the spikes are abolished by 100 nM tetrodotoxin (TTX), whereas the slow depolarizations are abolished by a calcium-channel blocker (500 μM Cd2+). (B) A cocktail of synaptic blockers reduces the burst frequency of UDs. (C) Polarization of UDs by current injection modulates the burst frequency and spike amplitude of complex spikes. The mean burst frequency (filled circles) of 4 cells (open circles) is plotted against the injected current in current-clamp mode; Insets show sample voltage traces for 10, –10, and –30 pA current injection. (D) The application of inhibitory blockers produces a net inward current in voltage-clamp mode; coapplication of excitatory blockers results in a transient outward shift in the measured current that exceeds the baseline current, indicating that UDs receive a tonic excitatory input (mean current ± SEM, n = 5).

Fig. 4.
Fig. 4.

Light-evoked hyperpolarization of the UDs increases the amplitude of the renascent spikes, reflecting removal of voltage-gated Na+-channel inactivation. (A) Perforated-patch current-clamp recording from a UD in response to a flashed dark spot. (B) Complex spikes aligned to the peak voltage of the first spike; renascent spikes (blue) are larger, faster, and more likely to produce a third spike than maintained spikes (black). (C–E) The effects of light-evoked hyperpolarization on the properties of complex spikes (n = 4, ± SEM.). (C) The absolute peak voltage of the first spike (black circles) and second spike (red circles) within each burst, and the spike threshold of the first spike (open circles); the spike threshold was measured 1 ms prior to the rate of rise reaching 40 V/s and reflected the initial membrane potential. (D) The maximum rate of rise (dV/dt) of the first spike (black circles) and second spike (red circles). (E) Individual spike amplitudes for the first spike (black symbols) and second spike (red symbols) plotted against the spike threshold; example traces are taken from the cell in A,> illustrating the variability in amplitudes of the first (black) and second (red) spikes. (F) Mean steady-state inactivation (n = 5, ± SEM) of Na+ currents measured by prepulses at different potentials (Inset) and fitted with a Boltzmann function (solid line; Vhalf = –48 mV, k = 6.3 mV); the onset of inactivation mirrors the decline in spike amplitude and increase in spike thresholds mapped in E. Pulse protocol: holding potential at –70 mV, 50 ms prepulse at potentials from –100 mV to –20 mV in 10-mV steps, and 100-ms test pulse at 0 mV.

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