Visual ecology and voltage-gated ion channels in insect photoreceptors

REVIEW Visual ecology and voltage-gated channels in insect photoreceptors

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Matti Weckstriim and Simon B. Laughlin That

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Trends Newosci. (1995) 18, 17-21

HOTORBCEPTORS can be used to study the ways I? in which neural signalling molecules work together to process and transmit information efficiently ’ - 4. The key signalling components - the phototransduction cascade, the non-transductive membrane and the output synapses - are highly developed and often neatly separated. A photoreceptor’s performance can be quantified using standard measures from opto-electronics: sensitivity, quantum efficiency, signal-to-noise ratio and frequency response’. Thus, the contributions made by individual components to signal coding can be determined6. Although much attention has focused on the processes of phototransduction’,3,7, the linkage of rhodopsin activation to the gating of lightsensitive channels in the photoreceptor membrane, other mechanisms that participate in voltage-signal generation and synaptic transmission are necessarily involved. A variety of conductances, differing in their ionic selectivities, voltage dependencies and kinetics, have been identified in both vertebrate and invertebrate photoreceptors2,4f8,9. These conductances must play important roles in filtering and transmitting the retinal image2s4. Yet, when research is confined to isolated cells, the contributions to the quality of vision made by channels cannot be established. A broader agenda has been set by studies of the isolated salamander retina”. Single-cell physiology, in situ recordings, and modelling show how voltage-sensitive conductances enable the network of electrically coupled rod inner segments to act as a spatiotemporal filter. This network enhances a bioQ 1995, Elsevier Science Ltd

logically relevant feature - the moving boundaries generated by approaching prey. Such a synthetic approach leads to an understanding of ion channel function2 by quantifying the biological advantages of selecting particular channels for expression in particular parts of neurons. Here we review recent work on insect retinas, where coding mechanisms and coding efficiency in both isolated and intact systems can be analysed6, and where a wide variety of eyes and visual capabilities can be examined. New examples of voltage-gated channels that tune photoreceptors to biologically relevant signal components are advancing the study of ion channel function. Blowfly

photoreceptors

and K’ channels

Blowflies share with birds the excellent temporal resolving power required to distinguish fine details in the rapidly moving images encountered in vigorous flight”. Blowflies use the same set of photoreceptors for vision at all light levels”. At absolute threshold, fly photoreceptors act like vertebrate rods, generating clearly resolvable discrete responses to single photons13. In full daylight, the same cells reduce their sensitivity by 3 log units, and easily outperform vertebrate cones in terms of signal-to-noise ratioI and frequency response”. As in cones”, this reduction in sensitivity is accompanied by a tenfold acceleration of response dynamics’6,17. The light-adapted blowfly photoreceptors have the fastest known photoreceptor response, with a corner frequency (defined as the -3dB point on the signal power spectrum) of over 1OOH.z(Ref. 11). Regulation of the phototransduction 7iiVS Vol. 18, No. 1, 1995

MattJ Weckstrb;m is at the Dept of Physiology and Biocenter OuJu, University of OuJu, Finland, and Simon B. Laughlin is at the Dept of Zoology, University of Cambridge, Cambridge, UK. 17

REVIEW

M. Weckstriim

and S. Laughlin

- Channels and insect Dhotorecemm

In darkness, the membrane potential is -65 mV, and most of the K’ channels are closed to increase gain. This results in a high input resistance that increases sensitivity - enabling l-2 mV responses to discrete photon absorptions”. Light gates inward current that depolar-20 izes the cell, and depolarization z activates outward K+ currents. Thus, -60 [- the voltage-sensitive delayed recti-60 fier provides a negative feedback I I I I 1’ 1 1’ ” 9” 1 that increases progressively with 150 0 100 200 300 400 500 0 50 100 depolarizationlg. Under daylight ms ms conditions, the K+ conductance (of -lo4 delayed-rectifier channels) approximately equals the light-gated conductance. This reduces sensitivity by almost 1 log unit, and maintains operations in the midrange of receptor potential, where the sensitivity to changes in light level is greatese’. The high signalto-noise ratio of blowfly photoreceptors (-100: 1) is achieved by transducing photons at a rate of lo6 photons s-’ (Ref. 14). This rate is possible only because the powerful K’ conductance enables the -20 0 -2 nA -100 -80 -60 -40 light-gated conductance to be increased nearly lOO-fold (Figs 2B Membrane potential (mv) and C). The role of the voltageFig. 1. The voltage-gated K+ conductance in the photoreceptors of the b/owf/y Calliphora vicinarEfO. (A) The dark- gated conductance in widening the bandwidth of the light-adapted cell adapted photoreceptor’s response to a series of 300 ms light pulses of increasing intensity [baseline, 3.9 x 1 04, 7.8 x is equally profound’g-Z’. An exten1O’, 7.6 x l@, 3.1 x 1 O’, 6.3 x 1 O’, 1.3 x IO’, 2.5 x IO6 and 5 x 1 O6 photonsr’ (Ref. 77)). (B) The voltogedependent currents elicited in sing/e-electrode voltage-clomp. Depolarization from a holding potential of -8OmV sive array of photoreceptive mem(20 mV below the resting potential) activates an outward current with both fast ond slow componentP. (C) The voltbrane is necessary for effective age response of a light-adapted photoreceptor to a series of current pulses. The background of -500 000 photons s-’ photon capture, but creates a large has depolarized the cell by 2OmV to -- 40 mV. The membrane is rectifying in both directions OS (1 result of octivotion capacitative load. The membrane (with further depolarization) and deuctivotion (with hyperpolarizotion) of the voltage-sensitive K’ conductance? time constant is approximately (D) Voltage-activation curves for the two components of K’ conductance derived from single-channel data in isolated 4ms in darkness but this does not patches of blowfly photoreceptors (illustrated in the inset) with c~ holding potential of - 7 00 mV. Solid squares represent affect photoreceptor performance activation in patches expressing mainly the slow component; and open circles represent activation in patches expressbecause the dark-adapted photoing mainly the fast component’9. transduction cascade operates cascade is responsible primarily for changing sensi- slowly. During light-adaptation, the cascade accelertivity and response dynamics. Light adaptation ates tenfold and the large membrane time constant reduces the durations, amplitudes and latency disper- could now limit severely the speed of the voltage sions of the primary conductance events generated response. The large light-gated conductance and the by individual photon hits 14,17S18. To take full advantage voltage-dependent activation of the delayed-rectifier of these changes, a powerful voltage-sensitive K+ con- K+ channels lowers the membrane resistance (Fig. 2B), ductance tunes the membrane to match the gain so reducing the time constant by a factor of -10. This and response dynamics of the phototransduction dramatically increases the 3 dB cut-off frequency of cascadelg. Two subtypes of channel, one activating the membrane (Fig. 2D) and permits the transduction more rapidly than the other, have overlapping acti- of exceptionally fast voltage signals”~‘7~‘g~20. A similar vation ranges that span the normal voltage-operating role in reducing the membrane time constant has range of the cell. The rapidly activating type operates been proposed for K+ channels in cochlear hair at more negative potentials (Fig. 1B and D), leading to cell?. This function has been demonstrated in a K+ current that activates almost instantaneously blowfly photoreceptors. Blockage of K+ channels using upon depolarization close to resting potential. A dis- tetraethylammonium (TEA) reduces the cut-off fretinctive slow component appears with larger depolar- quency of the light response by -40% (Ref. 19). izations (Fig. 1B and D). There is little inactivation The diversity of K’ channels in insects in situ in the physiological response rangelgJO. Measurements, modelling (Fig. 2A) and pharmaThe delayed-rectifier conductance in blowfly cological interventionlg show that these delayed- photoreceptor has two advantageous properties, an rectifier channels have a profound influence on three appropriate voltage-operating range and favourable aspects of coding efficiency: sensitivity, signal-toactivation kinetics. In bright light, the slow componoise ratio and frequency response (Figs 2B, C and D). nent dominates, producing a transient response to 18

TINSVol.

18, No. 1, 1995

M. WeckstrSm

and S. Laughlin

-Channels

REVIEW

and insect photoreceptors

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Fig. 2. A simple membrane model depicts the function of voltage-gated /C channels in blowfly photoreceptorF2’. (A) A lumped conductance mode/ of the photoreceptor membrane is appropriate because the photoreceptor is uniformly polarized in the soma, and the short axon has u high resistonce’9,2’ and, thus, draws negligible current. The mode/ incorporates the relevant components: the measured voltage-gated K+ conductance gK with a reversal potential E, = -85 mV; the light-gated conductance gL with o reversol potential E, = 0 mV; (I passive load conductance g,, (determined as the measured input resistance in the dark at membrane potentials where gK is not activated); and the measured membrane capacitance, C. (B) Activation of the R conductance gn (so/id line), according to its measured voltage dependency, great/y increases the light-gated conductonce, gL, required to depolarize the cell to CI particular membrane potential; gL is plotted either in the absence (broken /ine) or in the presence (dotted /ine) of gr (C) Signal-to-noise ratio (SNR) of the phototransduction with and without gr assumingI one lightgoted channel activuted per absorbed photon at high light /eve/s. (D) The 3 dB cut-off frequency of the cell membrone (IS the cell is depo/arized by activation of the light-gated conductance g,, with and without the uctivation of the voltage-gated K+ conductance, gr The physiological signaling range is shaded..

depolarization (Fig. 1C) that spares high-frequency components from attenuation1g*20. Has this set of K+ channels been selected to suit the blowfly’s visual ecology? A comparative study of photoreceptor K+ conductances in dipteran insects with different visual requirements has addressed this question” (Fig. 3, top). Fifteen rapidly moving diurnal species from eight families have fast photoreceptor responses, and exhibit the prominent delayed-rectifier K+ conductance required for an excellent frequency response. Five species of crane-flies or tipulids are active at dusk or at night, fly weakly, have slow photoreceptors with poor frequency responses, and essentially lack the delayed rectifier that typifies fast cells. Depolarization of these slow receptors elicits a K+current that inactivates rapidly in the physiological response range. Such transient currents were first described in another slow flier, the fruit-fly Drosophila24*25. The lack of a delayed rectifier in slow-moving species is not surprising. It is an unnecessary and metabolically expensive mechanism. The vigorous pumps that counteract the large ion fluxes generated by fast photoreceptors26,27 account for 10% of the oxygen consumption of a resting blowflf*. An inactivating conductance is certainly more efficient for

operating in the steady state”, but what is its function? Locusts migrate at night, and their photoreceptors switch between a day state, with high acuity and low sensitivity, and a night state, with low acuity and high sensitivity2’. There is also a diurnal change in K+ conductance3’. Photoreceptors of the locust Schistocercuhave both transient and sustained K’ currents31. In the day, the sustained currents dominate the physiological response range, giving the membrane fast cell properties. At night, the transient currents dominate3’, as in slow dipteran cells” (Fig. 3, middle). S-Hydroxytryptamine could be the neuromodulator that drives the K+ conductance from the day to the night state30*32(Fig. 3, bottom). The function of the transient currents has not been established but their activation at night, and at low membrane potentials, suggests that they are most useful under dark-adapted conditions when they can suppress large voltage transients generated by highly sensitive cells. Nonetheless, the comparative studies confirm that there are considerable differences in K’ conductance amongst arthropod photoreceptors8,q,33, and the correlation between conductance and visual habitat suggests a matching of K+ channels with an organism’s ecology. TINS Vol. 18, No. 1, 1995

19

light, because sustained depolarization inactivates the voltage-gated Na’ channels35. In these lightadapted cells, not all Na’ channels 2nA are inactivated, consequently small voltage increments and decrements are amplified by activation and deactivation of the voltage-dependent conductance, as demonstrated by blocking the voltage-gated Na’ channels with ITX (Fig. 4B). Pharmacological dissecLocust tion and modelling shows that a Day counter-balancing K’ conductance must be adjusted to prevent instability and oscillations35f36. Does this interesting example of a subthreshold-voltage amplifier really help drones to detect queen bees? The distant queen elicits a small brief hyperpolarizing blip in photoreceptors that survey the sky (a response to negative contrast in . +5-HT a ‘depolarizing’ photoreceptor). On the basis of intracellular recordings and application of ‘ITX, the Na+channel amplifier improves the detectability of small transient hyperpolarizations34. This mechanism operates also under natural conditions, outside the laboratory. Behavioural experiments, in which sexually aroused drones respond to Fig. 3. The visual ecology of voltage-goted /C conductances in insect photoreceptors. This small targets lowered on a string, is illustrated by recordings of outward current elicited in single-electrode voltage-c/amp by step establish the minimum angular depolarizations over the physiological response range. In the Diptera (top), the non-inoctivatsubtense of a detectable target. ing de/ayed rectifier typifies fast cells, which are defined by a high-frequency response, and are From the optics, it is found that a currents are found in slow cells, found in rapidly flying diurnal species I9. The inactivating single photoreceptor registers this defined by a poor frequency response, and are found in slow flying, crepuscular species”. The threshold stimulus as a brief dimphotoreceptors of the locust Schistocerca (middle) switch diurnally between a day state, simiming of contrast (8%). Recordings /or to fast cek, and a night state, similar to slow cells. This change can be induced by extracellular application of 5-l?T to day stote cells (bottom)“. from the intact retina show that the voltage signals of this size are amplified34,35. Finally, some deft photometry shows Signal enhancement by voltage-sensitive that the behaviour of the drones is coupled to the perconductances formance of the Na+-conductance amplifieti6. Drones The elegant series of studies of drone-bee photoreact visually to queens over a restricted range of light receptors by Coles, Vallett and colleagues34-36 draws levels, and this corresponds to the stimulus intensities together bath pharmacology, modelling, receptor at which the photoreceptor’s responses to small decresponses in intact retina, and field measurements of rements are greatest (Fig. 4C). Thus, drone bees have bee mating behaviour. It shows that a particular evolved a unique combination of voltage-gated Na’ combination of conductances amplifies a signal of conductance with a stabilizing K’ conductance, to supreme biological importance, the prospective enhance the image of a well-defined signal, a distant mate. Mating is the fulfillment of a drone’s life, and queen. involves the detection of a distant dark queen Prospects against the blue afternoon sky. This detection task is subject to considerable selection pressure. The It is extremely unlikely that signal enhancement drone’s enlarged dorsal eye shows a number of op- by positive feedback is confined to drone bees. A tical specializations that are not seen in queen and rapid transient is seen on the rising phase of light worker bees, such as larger lenses and a visual pig- responses recorded from the synaptic terminals of ment system that is sensitive to short wavelengths3’. worker-bee34 and blowfly3’ (Fig. 4C) photoreceptors, Sexual dimorphism of the eye’s optics is comp- and small action potentials can be recorded from lemented by electrical specializations of the photothe axons of cockroach photoreceptors4’, suggesting Drone photoreceptors are amplification by Na’ channels. This voltage-sensitive receptor membrane. unusual. Unlike worker bees, they generate TTX- enhancement appears to generate large postsynaptic sensitive action potentials at the onset of the transients, and the Ca2+ channels associated with response to a relatively bright light? (Fig. 4A). These vesicle release could contribute by providing a action potentials are not seen in cells held in bright positive feedback4’. Voltage-gated Ca” and Na’ Diptera Fast

aI

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TIN.5 Vol. 18, No. 1, 1995

M. We&Mm

conductances generate such a feedback in photoreceptors of the horseshoe crab (L&&us), which amplifies bumps?‘. quantum Amplification is greatest at night, and it has been suggested that a diurnal modulation of K+ channels is involved in regulating gain4’. Ingenious combinations of voltage, Ca” and possibly protonsensitive conductances have been implicated in signal filtering and amplification at photoreceptor output synapses2,4,8,41.However, none of these mechanisms is demonstrated conclusively, not even in the most favourable preparation, the enlarged synaptic terminals of photoreceptors from the giant barnacle Balanu.~~~. Given the general importance of synaptic amplification and adaptation, and progress to date, we expect studies of invertebrate and vertebrate photoreceptor terminals to advance our understanding of ion channel ecology. We are confident that insect photoreceptors will continue to contribute. The rich diversity of insect eyes and insect visual behaviour offers many more opportunities to correlate the distribution of channels with biological function. The study of modulation of channels has only just begun30,32, and the development of Drosophila photoreceptor preparations brings molecular genetics to the comparative study of ion channel physiolofl. Selected

references

and S. Laughlin

REVIEW

- Channels and insect photoreceptors

A

40 mV

C

20 ms 1.4 r 1.2

g

1.0

% 0.8 5 $ 0.6

sIf

0.4 : 0.2 1 17

18

19

20

21

22

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Radiance [log photons s-k-‘m-21 Fig. 4. Theamplification of insect photoreceptor responses by voltage-gored (depolarizing) conductonces. (A) In the dark-adopted photoreceptors of the drone bee, Apis mellifera, an action potential (contra/j is initiated on the rising phase of the light response’“, and it can be abolished by opplicotion of 77X. (6) Two sets of depolarizing and hyperpolarizing responses (30 overages) of drone photoreceptors to stimuli of low (8.9%) contrast. The opplicution of 77X reduces the responses by blocking the voltage-gated No+ channels responsible for omp/ification3A36. (C) Photoreceptor signal omplificotion matches drones’ visual behaviour. The voltage response, V, to a stimulus of threshold contrast (8%) increases in amplitude with background light level (continuous line). Maximum response occurs over the range of light levels at which drones f/y towurds queens, as illustrated by the histogram showing the relative frequencies with which drones approached pheromone scented lure?. (D) Signal enhancement in blowfly photoreceptor axons by (I fast voltage-dependent mechanism 39. The intracellulorly recorded response of the RI -6 type photoreceptor to short (10~s) light pulses of logarithmically increasing intensity has a small spike-like depolarization in the rising phase, which is also seen in worker bees”.

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Acknowledgements

The authors thank 7’he British Council in Finland support,

for their

reading various

the paper stages.

and Roger Hardie, Wulf Hews, Eero Kouvalainen, Mikko Juusola and Raimo Uusitalo for

21

in its