Sensitivity and Adaptation in the Retina
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1 Sensitivity and Adaptation in the Retina Visual transduction single photon sensitivity dark current rhodopsin Ca ++ vs cgmp as the messenger amplification Operating range of vision saturation, threshold, sensitivity, adaptation Ca ++ role in adaptation Neuronal specialization: rods vs. cones expanding the operating range population encoding of color Single photon detection in humans (Hecht, 1949)
2 Dark Current Photoreceptor Layer of Frog Retina and Dark Current ItpA) Time (sets) 4 5 Fig. 1. Scanning electron micrograph of photoreceptor layer of frog retina (courtesy of W. H. Miller). Superimposed on a rod at right is a schematic diagram of the dark, circulating current. The lower panel show the mean (n = 99) photocurrent response of a toad rod in HEPES Ringers to 20 msec 520 nm flashes of intensity hv.~rn-~. The individual responses of the rod to this flash show quanta1 fluctuations that can be attributed to Poisson fluctuations in photon absorptions, with a Poisson distribution mean of 0.53 events/flash (Baylor e/ al., 1979b). The lower panel can thus be taken to represent, approximately, the single photon response, scaled to about 0.5 of its height. Retinal isomerization and rhodopsin 1615
3 Ca ++ vs cgmp Photoreceptor Layer of Frog Retina and Dark Current Ca ++ is the messenger external Ca ++ suppresses dark current reversal potential close to Ca ++ iontophoretic inj of Ca ++ hyperpolarizes and decreases light sensitivity Ca ++ is not the messenger membrane very permeable to Ca ++ Ca ++ chelator doesnʼt decrease light sensitivity free Ca ++ decreases during light response Photoreceptor Layer of Frog Retina and Dark Current Ca ++ vs cgmp cgmp is the messenger injection induces rapid depolarization recovery from this depolarization speed up by light injection increases latency of light response BUT, could cgmp increase the dark current via Ca ++
4 cgmp-sensitive Conductance of Rod Outer Segment Membrane lomv[ Fig. 6. (A) Scheme use by Fesenko et ui. (1985) in their discovery of a cgmp-gated conductance I the rod outer segment membrane. A small patch of O.S. membrane was excised from the outer segment with the tight-seal technique of Neher and Sakman. (B) Voltages pulses were applied across the membrane patch and voltage-clamp currents measured under various perfusion conditions, one of which is illustrated. Application of cgmp in the perfusate altered the increased the current through the membrane patch. Ca2+ or calcium chelators applied to the patch had little effect. (C) The cgmp-concentration dependence of the membrane currents through patches as determined in (8). The smooth curve drawn through the data was generated with the Hill equation, equation (2) with k, = 30pM and N = I.8. (D) The same data as in (C) are plotted in the form lo&l/(1-1)] vs log[cgmp], where I is clamp current normalized by the maximal current induced by cgmp perfusion: the slope gives.n. the Hill cocilicient. Fesenko et al. 1985
5 in sensitivity and rees. Suction-pipet. reels, filled circles indish in normal Ringer's response to an identied. For both rods and k increases the light nd slows the lime-toerences between rods cales in top and botns (620 run) /im~2 in nm~'2 in lower panel. atani K, Yau K-W. J hether the stimulus rotransmitters, etc. g structural similarembrane receptors, membrane-helix toansduction is so adodel system to shed pathways. n process seems alany complex cellu- components or branches in a complex pathway. Phototransduction cascade T, Rh' Rh GGDP Rh'-P G GDP G*GTP PDEi ACG = 0 PDEi PDE* ACG<0 (CHANNELopen) ( CHANNELcioso) - T4 A CG = 0 (CHANNELopon) FIGURE 17. A schematic representation of the phototransduction cascade (with the Ca a+ feedback not. included) to highlight the importance of the decay time constants of the active intermediates (7,, T 2, and T3) and the basal rate of metabolic flux of cgmp in darkness (r 4 ). G is transducin, and PDl^ ' s l n c inactive form of the phosphodiestera.se. Asterisks indicate the active intermediates. AC = 0 represents the steady basal level of cgmp in darkness, and AG < 0 indicates a decline in cgmp level. Overall gain of the cascade (and hence light sensitivity) depends on the multiplicative product of the various T values. Light Intensities (candelas/m2) Photopic 10 0 Mesotopic 10-5 Scotopic
6 Saturation Threshold Response Stimulus Strength
7 0.9 Range Saturation 0.8 Dark Current Suppression Threshold Single Photon Light Range Saturation Threshold Threshold
8 Ca ++ and rod adaptation (Nakatani and Yau, 1988) Ca ++ and rod adaptation Figure 10. Molecular Schematic of the Reactions of Phototransduction Species and steps are colored red for activation, blue for inactivation, green for regulation. For activation, a photon (h) isomerizes rhodopsin to its active form R*, now identified as metarhodopsin II (M II ). R* catalyzes activation of a G protein to G*, which binds to an effector E protein, activating it to G*E*. The effector is a phosphodiesterase, which hydrolyzes cgmp (cg) in the cytoplasm, leading to closure of ion channels at the plasma membrane (PM). For inactivation, R* binds RK and is phosphorylated to form M II P. Arrestin (Arr) then binds, substantially completing the inactivation of R*. G*E* is inactivated by hydrolysis of the terminal phosphate of GGTP, a reaction accelerated by an RGS protein (regulator of G protein signaling; He et al., 1998) that is probably complexed to the type 5 G protein subunit (G5; Makino et al., 1999). The inactive G and E then separate. cgmp is continually formed by guanylyl cyclase (GC). For regulation, closure of channels causes a drop in cytoplasmic Ca 2 concentration, regulating the cascade in (at least) two locations. GC activity is modulated by an activating protein (AP) (Gorczyca et al., 1994). RK activity is modulated by recoverin (Rec) (Kawamura, 1993; Klenchin et al., 1995; Tanaka et al., 1995). For further discussion of the reactions, see Nikonov et al. (1998).
9 Light Intensities (candelas/m 2 ) Photopic 10 0 Mesotopic 10-5 Scotopic Figure 1. Schematics of Rod and Cone Photoreceptors Photon absorption in the outer segments of a rod and a cone causes adecreaseincgmp-gatedinwardcurrents(toptraces).theouter segment currents of cones are appreciably faster than those of rods and require flashes of higher intensity. The resulting membrane hyperpolarization (bottom traces) is filtered by the electrical properties of the photoreceptor membranes, including voltage-gated conductances located in the inner segments. This hyperpolarization slows neurotransmitter release from the synaptic terminals. All traces are schematic representations of responses to dim (thin) and bright (thick) brief flashes, and although generalizable to many different species, are shown here with scale bars that reflect the average properties of primate photoreceptors (Baylor et al., 1984b; Schneeweis and Schnapf, 1995, 1999), ignoring the effects of photoreceptor coupling. OS, outer segment; IS, inner segment; N, nucleus; ST, synaptic terminal.
10 Rod Adaptation Cone Adaptation (Nakatani and Yau, 1988) Activation, deactivation, regulation Figure 10. Molecular Schematic of the Reactions of Phototransduction Species and steps are colored red for activation, blue for inactivation, green for regulation. For activation, a photon (h) isomerizes rhodopsin to its active form R*, now identified as metarhodopsin II (M II ). R* catalyzes activation of a G protein to G*, which binds to an effector E protein, activating it to G*E*. The effector is a phosphodiesterase, which hydrolyzes cgmp (cg) in the cytoplasm, leading to closure of ion channels at the plasma membrane (PM). For inactivation, R* binds RK and is phosphorylated to form M II P. Arrestin (Arr) then binds, substantially completing the inactivation of R*. G*E* is inactivated by hydrolysis of the terminal phosphate of GGTP, a reaction accelerated by an RGS protein (regulator of G protein signaling; He et al., 1998) that is probably complexed to the type 5 G protein subunit (G5; Makino et al., 1999). The inactive G and E then separate. cgmp is continually formed by guanylyl cyclase (GC). For regulation, closure of channels causes a drop in cytoplasmic Ca 2 concentration, regulating the cascade in (at least) two locations. GC activity is modulated by an activating protein (AP) (Gorczyca et al., 1994). RK activity is modulated by recoverin (Rec) (Kawamura, 1993; Klenchin et al., 1995; Tanaka et al., 1995). For further discussion of the reactions, see Nikonov et al. (1998).
11 Light Intensities (candelas/m 2 ) Cones 10 6 Photopic 10 0 Mesotopic Rods 10-5 Scotopic Stimulus Encoding With Response Response Visual Parameter
12 Stimulus Encoding With Population Responses Response Visual Parameter Human Cone Spectral Sensitivity Relative Response Wavelength (nm)
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