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Calcium Channels at the Photoreceptor Synapse

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B3H 4H7 output synapse and may transduce NO signals from other cells by either directly permitting Ca2+ influx or by providing depolarizing influences that gate voltage-dependent Ca2+ channels.

Presynaptic Ca2+ channels mediate early stages of visual information processing in photoreceptors by facilitating the release of neurotransmitter and by receiving modulatory input that alters transmission. Two types of L-type Ca2+ channels, composed of α1F and α1D subunits and having similar biophysical and pharmacological properties, appear to form the principle voltage-dependent Ca2+ influx pathways in rods and cones, respectively. The role played by these channels in neurotransmitter release at these graded potential, nonspiking synapses, has been well described. The channels mediate sustained glutamate release in darkness where the cells rest at potentials near 40 mV, and signal increases in light intensity as the cells hyperpolarize negative to this value. Synaptic modulation and integration mediated by these channels has not yet been as fully described but appears to involve GABA, nitric oxide (NO), glutamate, and dopamine. Ca2+ permeable, cyclic nucleotide-gated (CNG) channels appear to have supporting roles at the photoreceptor.

Introduction

Animals see when features of the neural image first formed in the photoreceptors are extracted and encoded in the successive and parallel stages of visual information processing. The output synapse of rod and cone photoreceptors is an obvious crucial link between the transduction of light and the neural processing of that signal. At this first synapse there is communication not only from the photoreceptors to second-order bipolar and horizontal cells, but retrograde, feedback communication from second-order cells to photoreceptors in return. Photoreceptor presynaptic Ca2+ channels are key elements in this bidirectional transfer of visual information.

This chapter reviews three fundamental aspects of the photoreceptor presynaptic terminal: 1) the function of voltage-gated Ca2+ channels in transmission of the light response from the rod spherules and cone pedicles, the presynaptic terminals of the photoreceptors, 2) the presynaptic function of nonvoltage-gated Ca2+ permeable channels in the photoreceptor terminals, and 3) the role of Ca2+ and Ca2+ permeable channels in mediating the synaptic signals received from second-order cells.

Physiology of Transmission at the Photoreceptor Synapse

The neurons of the outer retina, e.g., rod and cone photoreceptors, horizontal cells, and bipolar cells, do not generate action potentials (but see Kawai et al, 2001).1 Instead, they signal via graded and relatively small changes in their membrane potentials.1a For photoreceptors, the range of membrane potential excursions is limited to values from around 40 mV in darkness, to 60 or 70 mV in bright light. For rod photoreceptors, clipping of hyperpolarizing signals greater than about 5-10 mV is known to occur at the synapse,2 while for cones, evidence suggests a greater dynamic range for the synapse (up to 30 mV).3 This is surprising, considering that for both types of photoreceptors, biophysically similar but molecularly distinct voltage-gated Ca2+ channels mediate the Ca2+-dependent synaptic release of glutamate.4 The apparent Ca2+ channel activation threshold at about 45 mV suggests a poor alignment between the range of potentials over which the photoreceptors operate and the voltage range over which presynaptic Ca2+ channels activate. However, it must be recalled that there is no true threshold to ion channel activation (such as there is for an action potential), and that at potentials negative to the apparent threshold, the open probability for the channels falls off exponentially to nearly imperceptible levels.

As at most other synapses in the nervous system, glutamate is released when the membrane is depolarized and Ca2+ channels are activated.5,6 Postsynaptic responses in horizontal cells and hyperpolarizing (“off”) bipolar cells are mediated by a diversity of ionotropic glutamate-gated channels. Light-evoked photoreceptor hyperpolarizations become depolarizations in “on” bipolar cells, the inversion being mediated by a metabotropic glutamate receptor (the APB receptor), which affects membrane potential via CNG channels.7

Synaptic transmission is strikingly sensitive to Ca2+ signal modulation at the rod and cone terminals. Since a narrow range of Ca2+ channel activation is utilized for synaptic release, high gain by the processes translating membrane potential into glutamate release is required. The first consequence of this is that a steep exponential relationship between the presynaptic and postsynaptic potentials arises.8 The second consequence is that small changes in Ca2+ channel activation translate into large changes of synaptic efficacy.2,9 The third consequence, especially important considering the likely role of CNG channels at the synapse, is that all processes resulting in Ca2+ influx and/or membrane potential changes alter synaptic function dramatically.10

Receptive Field Formation and Adaptation at the Photoreceptor Synapse

Ganglion cells, which carry the output of the retina, characteristically have center-surround antagonistic receptive fields. In some ganglion cells, light falling in the center of the receptive field evokes excitation, while light falling on concentric surrounding regions evokes a response of opposite polarity due to lateral inhibition. Other ganglion cell receptive fields have inhibitory centers and excitatory surrounds, while for some others, the color of the light determines the sign of the response. These receptive field organizations support some of the basic principles of retinal processing: contrast enhancement and color opponency. It is known that center-surround antagonistic receptive fields are first formed through presynaptic integration at the cone photoreceptor synaptic terminal.

Another major emphasis of research at the photoreceptor synapse derives from the fact that for the visual processing cascade to function optimally, neural signals must be maximized for all levels of light adaptation.1a The visual system operates over an extremely broad range (1010) of stimulus intensities. The system achieves this remarkable operating range by exploiting the dynamic range at numerous, cascaded stages where adaptation occurs. Several adaptation stages have been described in rods and cones, beginning of course in the light-transducing outer segments. Resetting of the operating range of the photoreceptor output synapse is another such stage, but the process occurs via unknown mechanisms.

The relative strength of cone versus rod synaptic input to second-order cells can be modulated.11 By altering the strength of the rod and cone output synapses inversely, an effective means for broadening the operating range of the retina arises. Most vertebrate retinas are duplex: rod photoreceptors and associated circuits mediate photon-sparse night vision, whereas cone photoreceptors and associated circuitry mediate information-rich day vision. Duplex retinas share circuitry for the rod and cone systems wherein some retinal neurons in the pathway, downstream from photoreceptors, may take part in both night and day vision. Thus, during the light-dark switch, retinal signaling pathways undergo reconfiguration to facilitate the rod or cone domination of the duplex system. A major stage of adaptation in this scheme is at the photoreceptor synapse, where bias is applied to cone synaptic function during the day and to rod synaptic function during the night.

Voltage-Gated Ca2+ Channels at the Presynaptic Terminals of the Photoreceptors

Photoreceptors and other nonspiking neurons communicate with graded potentials and their synapses mediate the continuous release of neurotransmitter. A prominent and specialized morphological feature at the presynaptic membrane of such cells, the synaptic ribbon, is responsible for guiding the transport of vesicles to the release site. Voltage-gated Ca2+ channels, as well as other Ca2+ permeable channels such as CNG channels, mediate the influx of Ca2+ required for vesicle fusion. A great deal is known about the pharmacology and biophysics of the rod and cone L-type Ca2+ channels. First recorded in rods, the properties of these channels have been remarkably consistent in all preparations examined and share features with high-voltage-activated, dihydropyridine-sensitive, noninactivating Ca2+ channels described throughout the nervous system.12–19

However, the Ca2+channels of rod and cone photoreceptors can be distinguished from mainstream cardiovascular L-type Ca2+ channels by their relatively weak interactions with dihydropyridines and the partial and reversible block by the N-type blocker ω-conotoxin.18,20 The pharmacological characterization most closely resembling this profile is that of α1D subunit containing Ca2+ channels.21

In humans expressing a mutated L-type Ca2+ channel α1F subtype, there is no visual function of the rod system. Genetic analysis of small populations affected with Congenital Stationary (e.g., nonprogressive) Night Blindness, type 2 (CSNB2), revealed mutations in the gene coding for the α1F L-type Ca2+ channel-forming subunit.22,23 Electroretinography revealed that these individuals had full function of rod photoreceptors in transduction but a complete lack of transmission of this signal to second-order cells. Since CSNB2 is a rod disease, the identification of the gene product responsible suggests that the rod Ca2+ channel is composed of α1F subunits. In support of this, additional evidence suggests that rod Ca2+ channels, which share most biophysical and pharmacological properties with cone Ca2+ channels,18,20 are composed of α1F Ca2+ channel subunits.22,23 In situ hybridization localized α1F subunit mRNA in rod photoreceptors23 and antibodies directed against α1F Ca2+ channel subunits labeled rod synaptic terminals.24

Immunohistochemistry has not yet allowed firm conclusions to be drawn about the molecular identity of the Ca2+ channels in cones. Some cones in mammalian retina label with antibodies directed against α1D subunits,19,25 while cones (and rods) in salamander retina label with antibodies directed against rat brain α1C subunits, although the specificity of these antibodies in salamander was not established.26

Modifiers of Ca2+ Channel Activity

Several models of Ca2+ channel modulation at this synapse have been described. Protons, divalent cations, and anions have each been investigated for their Ca2+ channel-modulating activity and all have been shown to have profound effects upon the gating and permeation of photoreceptor channels. Protons are known to alter ion channel gating via several mechanisms, including direct block of the conducting pore, surface charge effects, and binding to channel proteins. In rods and cones, protons produce changes in Ca2+ channel gating and conductance by all of these mechanisms. Acidic conditions reduce Ca2+ channel activity and basic conditions increase it.27 The consequences to synaptic transmission are that synaptic efficacy is increased as pH is increased.9,28 It has been suggested that protons liberated during vesicular release from photoreceptors produce a rapid autoinhibition of further release via Ca2+ channel inhibition.29

Divalent cations including Ca2+, Mg2+, Cd2+, Co2+, and Ni2+ have all been shown to exert important modulatory effects on photoreceptor presynaptic Ca2+ channels, and to effect synaptic transmission in both expected and unexpected manners. Ca2+ channel-blocking divalent cations (Cd2+, Co2+, and Ni2+), as expected, block synaptic transmission. Surprisingly, the block by low concentrations of these divalents can be reversed by lowering Ca2+ levels, since this action reduces the screening of membrane surface charge and increases Ca2+ channel activation.30,31 Inversely, as Ca2+ concentrations increase, surface charge effects dominate over a narrow range of the foot of activation curve for Ca2+ channels and reduce Ca2+ channel activity.32

Anion modulation of Ca2+ current voltage dependence and amplitude in salamander photoreceptors has also been reported. Reductions of extracellular Cl suppress the activity and conductance of Ca2+ channels and this leads to reduction of synaptic efficacy.33,34

At the cone synapse in particular, the invaginating horizontal cell processes require that extracellular current flow to the dendrite tips must follow a significant and necessarily resistive path to the glutamate-gated channels. Byzov put forward a model of electrical feedback, in which the large extracellular flow of current to postsynaptic glutamate-gated channels in horizontal cell dendrites, which serve as current sinks, produced voltage drops in the extracellular space.35 Extracellular voltage drops affect the voltage-dependent gating of Ca2+ channels equally as much as intracellular voltage changes. Byzov postulated that the postsynaptic horizontal cell response itself modulates presynaptic release via this autoinhibitory feedback loop. His ingenious model of ephaptic interaction has since been modified and stands as the cornerstone of further attempts, described later in this chapter, to describe synaptic feedback to cones.

Other Ca2+ Permeable Channels in the Photoreceptor Terminals

Another type of ion channel that is well known for having significant Ca2+ permeablility is the CNG channel of the outer segments of rods and cones. While mostly permeable to monovalent cations, the Ca2+ permeability of these channels underlies their role in providing a negative feedback on the production of cGMP. In addition to their high-density expression in the outer segments of photoreceptors, the inner segment membranes of rods also contain CNG channels, albeit at a much lower density.36 CNG channels are capable of supporting exocytosis and glutamate release at cone synaptic terminals.4,10 CNG channel activity was also shown to be stimulated by NO, which acts via guanylate cyclase to produce cGMP.10 The preponderance of sites of NO synthesis in the retina, the demonstrated production of NO in the outer retinal layers during darkness, and the strong actions of NO synthase inhibitors on synaptic release from photoreceptors, suggested a role for CNG channels in synaptic signaling at these synapses.

The Role of Ca2+ Permeable Channels in Feedback from Second-Order Cells

Retinal structure is dominated by lateral networks of neurons that mediate processing of the neural image. At the outer plexiform layer, photoreceptor to bipolar cell transmission is modified by laterally interacting horizontal cells. It is known that basic features of the ganglion cell receptive field structure, e.g., simple center-surround antagonism, are present in bipolar cells.37,38 Morphological studies of the outer plexiform layer support electrophysiological data: bipolar cells sample many photoreceptors directly (accounting for the center region) and, via horizontal cells, sample photoreceptors over broad lateral regions (accounting for the surround component of the receptive field). Integration of center and surround signals occurs presynaptic to bipolar cells at the cone presynaptic terminal.39 The first study of cones showed that surround illumination decreases the hyperpolarizing response of a cone to direct illumination.3 The mechanism of inhibitory feedback to cones has remained elusive.40

GABA as a Feedback Transmitter

An early hypothesis offered for the synaptic mechanisms of feedback was based on histochemical and biochemical experiments showing that some classes of horizontal cells synthesize and release GABA.41 Electrophysiological evidence suggested that GABA is a feedback transmitter and acts at cone GABAA receptors42 which form Cl channels.43,44 When cones are hyperpolarized strongly by bright light, the effect of surround inhibition, as recorded in bipolar cells, diminishes.45 Others demonstrated a conductance increase to Cl in cones during surround illumination46,47 later suggested to be secondary to a conductance increase involving Ca2+ ions.48 However, failure to block surround inhibition in cones with GABAA antagonists has been demonstrated.49 These diverse observations complicated the model in which GABA is the sole feedback neurotransmitter acting via GABAA receptors. The results can also be interpreted in terms of a Ca2+ channel modulation that would vanish at hyperpolarized levels simply because the Ca2+ channels are not activated at this negative potential.

Nitric Oxide as a Feedback Transmitter and Adaptation Signal

Evidence from a variety of cells and tissues has demonstrated the important roles of nitric oxide (NO) as both a second messenger and a neurotransmitter, which mediates diverse physiological functions.50 Recent discoveries suggest that NO may not only be integral to visual processing and retinal function, but may also be a contributor to the underlying pathology associated with diseases such as retinal ischemia and glaucoma.51

Three common isoforms of the enzyme nitric oxide synthase (NOS), which converts L-arginine to NO and L-citrulline, are found in the retina and its vasculature: Constitutive isoforms, denoted as cNOS, are Ca2+/calmodulin dependent and include eNOS (endothelial) and nNOS (neural). A third, Ca2+-independent, inducible isoform, iNOS, is up-regulated by immunological signals. NO can activate guanylate cyclase, which produces cGMP as a second messenger, but additional actions include activation of ADP-ribosyl transferase and direct nitrosylation of proteins.

NOS-immunoreactivity or diaphorase staining (histochemical indicator of NOS activity) has been found in every retina examined.52,53 NOS is found commonly in the specialized glia of the retina, the Müller cells, in subpopulations of horizontal and amacrine cells, and with less consistency in a variety of neurons.54,55 Detailed studies of several species find evidence for subcellular distributions of cNOS in rod and cone photoreceptors, bipolar cells, Müller cells, amacrine cells, and ganglion cell axon-ensheathing astrocytes, as well as in both the inner and outer plexiform layers. Prominent sites of NOS localization in the outer plexiform layer are within horizontal cell synaptic processes. Such localization supports a role for NO as a feedback neurotransmitter carrying surround signals, which are integrated in horizontal cells, back to the cone photoreceptors. In addition, NOS is present in the sclerad region of Müller cells that envelop the photoreceptor inner segments, potentially supporting a role for NO as an adaptation molecule in the outer retina.

Demonstrated actions of NO on retinal cells are consistent with a role in light-dark adaptation.51 For example, whereas voltage-gated Ca2+ channels responsible for rod synaptic release are potentiated by NO,56 evidence suggested that those in cones are suppressed.57 If NO were a dark-adaptation messenger in the outer retina, an increase in NO would strengthen rod signaling while decreasing that of cones.

Another broadly recognized action of NO in photoreceptors4 is the activation of cyclic nucleotide-gated (CNG) channels; the voltage-independent, Ca2+-permeable, nonspecific cation channels best known for their role in phototransduction. While CNG channel activation by NO may have ramifications ranging from phototransduction to synaptic modulation at numerous pre- and postsynaptic sites, this mechanism of signaling raises the issue of whether NO signals darkness or light, whether it signals broadly or locally, and whether its actions as a neuromodulator occur on a fast or slow timescale. It has been suggested that this type of mechanism operates to facilitate neurotransmitter release at the photoreceptor terminal.10 These studies have shown that activation of CNG channels in synaptic terminals elicits transmitter release from cones. This model of neuromodulation at the photoreceptor terminals suggests that nitric oxide is the transmitter responsible for increasing or decreasing neurotransmitter release from photoreceptors in response to other retinal stimuli, either by way of modulating voltage-dependent Ca2+ channels56 or activation of Ca2+-permeable CNG channels.10

Synaptic Modulation by Dopamine

Dopamine is a classic neuromodulator with a well-established role in the retina in light-dark adaptation.58,59 Dopamine has specific actions on virtually all types of neurons of the retina including photoreceptors, horizontal cells, and bipolar cells. Release of dopamine from subclasses of amacrine and interplexiform cells of the inner retina results in increased cone input to horizontal cells and decreased rod input.11,60 In salamander, both D1 and D2 dopamine receptor subtypes have been localized to the photoreceptors.11 D2 receptors appear to have a role in decreasing rod synaptic output by suppressing the activity of the primary signal shaping ionic conductance in the rod inner segment, the hyperpolarization-activated, nonselective cation conductance Ih.61 Ih is responsible for shaping the characteristic peak-plateau sag in the hyperpolarizing rod response to light.62 By suppressing Ih, dopamine would have the effect of diminishing rod output since rods would be more strongly hyperpolarized. In modulatory roles of this nature, dopamine seems to mediate retinal adaptation to increasing levels of illumination. However, dopamine acting via D2 receptors can decrease the activity of Ca2+ channels of cones while increasing that in rods.63 Due to the plethora of actions of dopamine on the postsynaptic cells (targets: glutamate receptors, Ca2+ channels, potassium channels, gap junction channels), as well as other effects on the presynaptic photoreceptors (targets: hcurrent, NaK ATPase, gap junctions), the overall actions of dopamine on synaptic transmission may be different than the effect of dopamine on the presynaptic Ca2+ channels alone.

Synaptic Modulation by Glutamate

Both rod and cone photoreceptors release glutamate in a manner graded with their degree of depolarization. Evidence that possible glutamate autoreception inhibits glutamate release, mediated by a type of metabotropic glutamate receptor (mGluR8), has been provided.64 Metabotropic glutamate receptors signal via G-proteins, and in the example described in rod photoreceptors, this signaling couples glutamate reception to reduction of intracellular Ca2+ levels, an apparent inhibitory feedback mechanism that could serve to protect the cells receptive to glutamate at this synapse to damaging levels of the excitotoxic neurotransmitter.

Synaptic Modulation through an Ephaptic Interaction

The electric feedback model of Byzov (section “Modifiers of Ca2+ Channel Activity”) was modified after the identification of putative hemigap junction channels in the dendrites of horizontal cells.65 In this model (shown in Fig. 1), hemigap junction channels serve as the current sinks instead of the postsynaptic glutamate-gated channels in Byzov's model. This simplifies understanding of the model since little or no conductance change need occur in these elements to gate the horizontal cell response. As in the original postulation of Byzov, extracellular current flow to these hemigap junction channel current sinks produces an extracellular voltage drop, and this causes an apparent shift of the presynaptic Ca2+ channel activation curve.

Figure 1. The modified Byzov electric feedback model describing an ephaptic interaction between horizontal cells and photoreceptors.

Figure 1

The modified Byzov electric feedback model describing an ephaptic interaction between horizontal cells and photoreceptors. In a), the hemigap junction channels in the postsynaptic horizontal cell membrane (HC) are juxtaposed with voltage-gated Ca2+ channels (more...)

Conclusion

This chapter reviewed the biophysical and physiological mechanisms of photoreceptor synaptic function and modulation as they pertain to the formation of receptive fields and adaptation. Voltage-gated L-type Ca2+ channels appear to be the principle ion channel type responsible for Ca2+ entry into photoreceptors. Important features of these channels, as well as how signal processing occurs at the photoreceptor synapse, remain intact among all vertebrates studied such that descriptions of retinal function in lower vertebrates and nocturnal mammals can be extrapolated to other species, including humans.

The presynaptic Ca2+ channels are L-type and appear to be composed of 1F subunits in rods and 1D subunits in cones. Modulatory synaptic interactions between photoreceptors and other retinal cells determine the neural image passed on to higher-order neurons in the visual system. Modulation of Ca2+ channels occurs via GABA, NO, dopamine and glutamate. Although information processing occurs at many levels in the vertebrate visual system, the photoreceptor synapse is the first locus at which synaptic integration can mediate the formation of specialized receptive fields and adaptation-specific output. The photoreceptor synapse is also one of the most accessible and well-characterized CNS synapse and will permit further biophysical, molecular and pharmacological manipulation that will enable continued high-resolution physiological investigation.

Acknowledgments

The authors' work was supported with operating funds (SB) and salary awards (SB, MEMK) from the Canadian Institutes of Health Research and a NSERC research grant (MEMK).

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