A rise in intracellular Ca²⁺ underlies light adaptation in dogfish retinal ‘on’ bipolar cells

Abstract

The rod visual system is extraordinary not only in its great sensitivity in the dark-adapted state, when it is capable of the detection of a few photons, but also in its ability to operate over a range of light intensities about a million times greater than absolute threshold (Aguilar & Stiles, 1954). High sensitivity in the dark-adapted state is achieved by high gain in phototransduction in rods (Pugh & Lamb, 1993) and in synaptic transduction in 'on' bipolar cells (Shiells & Falk, 1994), each involving a cGMP cascade linked to rhodopsin or to a metabotropic glutamate receptor (mGluR), respectively. This mGluR has been cloned and identified as mGluR6 (Nakajima et al. 1993). Psychophysical studies have indicated that the visual threshold rises at background light intensities too weak to induce significant adaptation in rod photoreceptors. Thresholds double at backgrounds when only one out of three rods absorb one photon per second, remarkable given that each rod in the human eye contains about 10Ì rhodopsin molecules (Rushton, 1965). To operate over such a wide range of light intensities there appears to be light-and time-dependent control of gain, or adaptation, in both photoreceptor and 'on' bipolar cell cGMP cascades. Rod photoreceptors are relatively depolarized in the dark, releasing glutamate from their synaptic terminals at a high rate. Glutamate activates the 'on' bipolar cell mGluR6, which in turn activates a G-protein and phosphodiesterase (PDE) leading to the hydrolysis of cGMP and thus a reduction in cGMP-activated conductance. The closure of cGMP-activated cation channels results in a relatively hyperpolarized state in the dark. Light hyperpolarizes rods,

Sodium Channels in Transient Retinal Bipolar Cells Enhance Visual Responses in Ganglion Cells

“…Sodium channels in transient bipolar cells enhanced the peak-tosustained response index, whereas the index of sustained bipolar cells was not affected by TTX, suggesting sodium channels selectively boosted the transient response component. Nawy (2000) and Shiells and Falk (1999) suggested that the calciumdependent desensitization of the mGluR6-gated channels shapes the transient response component of ON bipolar cells. Our observation that sodium currents shape transient responses is probably an independent mechanism, because BAPTA (10 mM), which was present in our intracellular solution, blocks calciumdependent desensitization (Nawy, 2000).…”

Scotopic Visual Signaling in the Mouse Retina Is Modulated by High-Affinity Plasma Membrane Calcium Extrusion

“…Hence, glutamate release and/or mGluR6 signaling could have been affected in dfw 2J retinas. Although the kinetics of exocytosis and synaptic depression appear to be similar in rods and cones (Kreft et al, 2003;Rabl et al, 2006), the neurotransmission at cone synapses is significantly faster (Schnapf and Copenhagen, 1982;Cadetti et al, 2005 (Shiells and Falk, 1999;Berntson et al, 2004;Nawy, 2004). Elevated [Ca 2ϩ ] i would, in turn, "adapt" rod bipolar responses to light stimulation, accounting for the loss of sensitivity observed in ERG and single-cell recordings.…”

Temporal Contrast Adaptation in Salamander Bipolar Cells

“…3) (Sakai et al, 1995;Smirnakis et al, 1997). Second, Ca 2ϩ -dependent mechanisms in the dendrites of ON bipolar cells contribute to mean but not contrast adaptation (Shiells and Falk, 1999) (Fig. 10).…”

“…3) indicates that contrast adaptation is mediated after signals are transferred to the bipolar cell. The experiments described below tested several possible mechanisms: (1) voltageactivated conductances in the bipolar soma (Mao et al, 1998); (2) amacrine feedback to the bipolar synaptic terminal (Maguire et al, 1989); (3) horizontal cell input to the bipolar dendrites (Mangel, 1991); and (4) Ca 2ϩ -dependent mechanisms in the bipolar dendrites (Shiells and Falk, 1999;Nawy, 2000).…”

“…Several studies have identified Ca 2ϩ -dependent gain controls in the dendrites of ON bipolar cells (Shiells and Falk, 1999;Nawy, 2000). To test whether such a mechanism might contribute to contrast adaptation, changes in Ca 2ϩ were suppressed by dialyzing a bipolar cell with a high concentration of Ca 2ϩ buffer and measuring the consequences for contrast adaptation.…”