Voltage-Gated Sodium Channels Improve Contrast Sensitivity of a Retinal Ganglion Cell

Abstract

Voltage-gated channels in a retinal ganglion cell are necessary for spike generation. However, they also add noise to the graded potential and spike train of the ganglion cell, which may degrade its contrast sensitivity, and they may also amplify the graded potential signal. We studied the effect of blocking Na ϩ channels in a ganglion cell on its signal and noise amplitudes and its contrast sensitivity. A spot was flashed at 1-4 Hz over the receptive field center of a brisk transient ganglion cell in an intact mammalian retina maintained in vitro. We measured signal and noise amplitudes from its intracellularly recorded graded potential light response and measured its contrast detection thresholds with an "ideal observer." When Na ϩ channels in the ganglion cell were blocked with intracellular lidocaine N-ethyl bromide (QX-314), the signal-to-noise ratio (SNR) decreased ( p Ͻ 0.05) at all tested contrasts (2-100%). Likewise, bath application of tetrodotoxin (TTX) reduced the SNR and contrast sensitivity but only at lower contrasts (Յ50%), whereas at higher contrasts, it increased the SNR and sensitivity. The opposite effect of TTX at high contrasts suggested involvement of an inhibitory surround mechanism in the inner retina. To test this hypothesis, we blocked glycinergic and GABAergic inputs with strychnine and picrotoxin and found that TTX in this case had the same effect as QX-314: a reduction in the SNR at all contrasts. Noise analysis suggested that blocking Na ϩ channels with QX-314 or TTX attenuates the amplitude of quantal synaptic voltages. These results demonstrate that Na ϩ channels in a ganglion cell amplify the synaptic voltage, enhancing the SNR and contrast sensitivity.

Intrinsic physiological properties of rat retinal ganglion cells with a comparative analysis

“…This optimization for speed, however, would decrease the alpha cell's relative sensitivity to an equivalent synaptic input to other RGC types, yet they would appear to be among the most sensitive cells to visual contrast (Kaplan and Shapley 1986). This apparent paradox implies that A2/alpha cells either have increased synaptic input relative to other RGC types or possibly also employ active dendritic conductances to enhance their sensitivity (Dhingra et al 2005;Velte and Masland 1999). Whether retinal cells receive the same number of synapses per linear micrometer of dendrite is a matter of some disagreement in the literature (Eriköz et al 2008;Jakobs et al 2008).…”

Noise Reduction of Coincidence Detector Output by the Inferior Colliculus of the Barn Owl

“…Phase locking in the auditory system improves from the auditory nerve to the anteroventral cochlear nucleus of the cat (Joris et al, 1994a,b), which has been modeled using both a summative mechanism (Kuhlmann et al, 2002) and a coincidence detection mechanism (Carney, 1992); a similar decrease in temporal jitter is seen from the electroreceptors to the midbrain torus of Eigenmannia (Carr et al, 1986). Retinal ganglion cells also improve on photoreceptor noise levels, using mechanisms such as temporal or spatial summation (Aho et al, 1993;Warrant, 1999), lateral inhibition (Srinivasan et al, 1982;Balboa and Grzywacz, 2000), and channel properties (Dhingra et al, 2005;Ichinose et al, 2005). All of these examples occur within two synapses of their respective sensory receptor.…”

Ideal observer analysis of signal quality in retinal circuits

“…Similarly, the number of gray levels in the graded potential was ~2-fold higher. We attribute the difference in performance of graded potential and spikes to 2 factors: ion channels in the ganglion cell which add noise (van Rossum et al, 2003; Dhingra & Smith, 2004, Dhingra et al, 2005; Demb et al, 2004; Margolis & Detwiler, 2007), and the limited sampling (spike) rate (Demb et al, 2004; Dhingra & Smith, 2004). In a similar study, the ideal observer measured the effect of blocking Na + channels on the performance of the ganglion cell (Dhingra et al, 2005).…”

“…To be relevant to survival, the measured signal quality must be a metric that can be related to a behavioral task performed by the organism. A basic measure of the quality of a neural response is its signal-to-noise ratio (SNR), the ratio of the amplitude of a signal to its associated noise (Figure 2) (Fechner, 1851; Hecht et al, 1942; Rose, 1942; Barlow, 1957, 1978, 1982; Green & Swets, 1988; Meister & Berry, 1999; Dhingra et al, 2003, 2005; Cohn, 2004). With accurate measurements of SNR from recordings of the ganglion cell and neurons in its presynaptic circuit, their contribution to signal quality might be determined.…”