Correspondence to: Mikko Juusola, Physiological Laboratory, Downing Street, University of Cambridge, Cambridge CB2 3EG, UK. Fax:44-1223-333-840 E-mail:mj216{at}cus.cam.ac.uk.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
It is known that an increase in both the mean light intensity and temperature can speed up photoreceptor signals, but it is not known whether a simultaneous increase of these physical factors enhances information capacity or leads to coding errors. We studied the voltage responses of light-adapted Drosophila photoreceptors in vivo from 15 to 30°C, and found that an increase in temperature accelerated both the phototransduction cascade and photoreceptor membrane dynamics, broadening the bandwidth of reliable signaling with an effective Q10 for information capacity of 6.5. The increased fidelity and reliability of the voltage responses was a result of four factors: (1) an increased rate of elementary response, i.e., quantum bump production; (2) a temperature-dependent acceleration of the early phototransduction reactions causing a quicker and narrower dispersion of bump latencies; (3) a relatively temperature-insensitive light-adapted bump waveform; and (4) a decrease in the time constant of the light-adapted photoreceptor membrane, whose filtering matched the dynamic properties of the phototransduction noise. Because faster neural processing allows faster behavioral responses, this improved performance of Drosophila photoreceptors suggests that a suitably high body temperature offers significant advantages in visual performance.
Key Words: vision, retina, information, neural coding, graded potential
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Animals live in a noisy and changeable environment with a variety of internal noise sources also present in the nervous system. Yet, with adequate stimulus conditions, their responses are usually both reliable and accurate. How robust is the underlying neural code, and can it be influenced by general physical factors like temperature? In the visual system, the flow of information starts from an intricate network of photoreceptors and interneurons, many of which use graded potentials (analogue signals) for their communication. This communication has its limitations even in its initial stages. If photoreceptors cannot code incoming light information into voltage responses larger than their own intrinsic voltage noise, higher order neurons in the brain cannot usefully process the signals they are receiving, and the action potentials they generate will carry little information. Because of their intrinsic noise and limited dynamic range, photoreceptors also face the problem of gain control. They must have a high gain to respond to small light contrasts and, yet, be able to accommodate large stimulus changes associated with changes in mean illumination. The reliability of this complex gain control, which involves both the phototransduction cascade and the cell membrane (including voltage-sensitive conductances), may also be prone to temperature-sensitive changes in the reaction kinetics (
Most animals, including insects and other invertebrates, cannot thermoregulate, but still are active over a wide range of temperatures. Studies in toads have emphasized how cooling can improve performance at absolute threshold by reducing the rate of thermal isomerization of rhodopsin (
Our previous study of the signaling efficiency in Drosophila photoreceptors (see
Physical chemistry tells us that the speed of chemical reactions can be increased by increasing the number of effective hits between the molecules taking part in the reaction. This can be achieved by increasing the concentration of the reactants or catalysts, or by increasing the thermal energy. The speed of chemical reactions approximately doubles with a 10°C rise in temperature; expressed as a Q10 of 2. Our results from Drosophila photoreceptors at 25°C (see
We have studied the response and membrane properties of light-adapted Drosophila photoreceptors in vivo over a 15°C temperature range using linear signal analysis with natural-like contrast and current stimulation similar to those of our companion paper (see
![]() |
MATERIALS AND METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Flies, wild-type red-eyed Drosophila melanogaster (Oregon), were taken from a laboratory culture and reared at 25°C. Intracellular voltage responses of green-sensitive R1-6 photoreceptors to light and current stimuli were recorded over a range of temperatures from 15 to 30°C. The recording procedures, light and current stimulation, and data analysis are explained in the companion paper (see
Recording Criteria
Only photoreceptors with saturating impulse responses (Vmax) over 40 mV, minimum input resistance of 100 M, and resting potential in the dark below -50 mV were selected for this study. These photoreceptors allowed stable recordings sometimes for several hours and, therefore, were used in a number of different experiments, each of which was repeated with a minimum of three cells, unless stated otherwise. However, we found the recording criteria to be temperature- dependent. In cooler temperatures, the photoreceptors required a significantly longer time to recover from the previous light exposure. Consequently, when a dark recovery period was kept constant, the light responses of a cool photoreceptor were often smaller than those measured in the same cell in warmer temperatures. The impulse responses were largest in a temperature range from 22 to 27°C (50.2 ± 9.3 mV, n = 30). Altogether, the data were collected from 51 photoreceptors. All the statistics are given as mean ± SD.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Impulse Responses of Dark-adapted Photoreceptors at Different Temperatures
The photoreceptor voltage responses to light impulses were first studied after 1030 min of dark adaptation. Fig 1 A shows typical voltage responses to a saturating light flash at different temperatures. Warming accelerated the voltage responses, producing an earlier peak. The responses also terminated more rapidly at higher temperatures.
|
Light Adaptation Is Highly Temperature-sensitive
Fig 1 B shows typical voltage responses of a photoreceptor to a prolonged light pulse at 28 and 18°C, both recorded after a 2-min dark adaptation period. Soon after the onset of the light pulse, the photoreceptor rapidly depolarizes from the dark-adapted resting potential (around -65 mV) to values close to zero, before declining in a multiphasic fashion to a much lower plateau potential. The decline of the responses from the initial transient to the lower steady-state potential, which is reached after 1020 s of continuous illumination, reflects the processes of light adaptation. Not only the timing and the shape of the initial voltage transients, but also the steady-state potential depends on temperature. At the brightest adapting background of 3 x 106 photons/s (BG0) the magnitude of the steady-state potential varies from 515 mV at 16°C to 2040 mV at warmer temperatures.
The temperature also greatly affects the voltage responses to contrast steps of light-adapted photoreceptors. Fig 2 A shows averaged contrast responses of two different photoreceptors recorded at BG0 at 29 and 24°C, respectively. Although light increments (positive contrasts) produce smaller responses than light decrements of the same amplitude, warming increases and accelerates voltage responses to any contrast stimulus. The faster time course of the contrast responses with warming is accompanied by accelerated photoreceptor membrane dynamics. This is shown in Fig 2 B, which compares current-evoked voltage responses of the same cells at the same temperatures. Small depolarizing current pulses (up to 0.3 nA) produce voltage responses showing strong outward rectification because of the activation of voltage-sensitive potassium channels (
|
These findings were confirmed and further characterized in recordings from single light-adapted photoreceptors using more natural, time-dependent light and current stimuli, i.e., white noisemodulated light contrasts and current injections at various temperatures. By applying both signal and shot noise analysis to the data, we could characterize the temperature-induced changes in the photoreceptor signal and noise dynamics and compare the filtering dynamics of the photoreceptor membrane to those of the phototransduction cascade.
In the next paragraph, we show: (I) how the light-adapted signal and noise dynamics of photoreceptor voltage responses change with temperature; (II) how the filtering properties of the photoreceptor membrane are tuned by the temperature; and (III) how the adaptive co-processing by the phototransduction cascade and membrane refines the photoreceptor signaling.
Light Adaptation and Photoreceptor Signaling at Different Temperatures
Light-adapted Drosophila photoreceptors produce slightly variable voltage responses to repeated presentations of an identical light contrast stimulus (
![]() |
(1) |
Voltage Responses to Dynamic Contrast Sequences at Bright Background Light
The signal and noise dynamics of light-adapted photoreceptors were studied using a 10-s-long Gaussian contrast stimulus at BG0. The stimulus was spectrally white up to 200 Hz and had a mean value of 0.32 (
|
The magnitude of the photoreceptor voltage signal, sV(t), increases 415 times (Fig 3 A) when warmed from 18 to 29°C. This is accompanied by an increasing signal mean, µ (or the BG0-induced steady-state depolarization), from
5 mV to 2025 mV above the dark-adapted resting potential (Fig 3 E) and by changes in the signal probability distribution (Fig 3 C, continuous line) from Gaussian at the coolest temperatures (
18°C, including the cells in Fig 3 D) to slightly negatively skewed at warmer temperatures (22, 25, and 29°C). In general, photoreceptors with the largest dark-adapted impulse responses also had the largest light-adapted steady-state potentials. Thus, the relation µ/Vmax increases with warming, from 13% at 16°C (n = 3) to 43% at 27°C (n = 4), confirming that cooling reduces the steady-state potential of light-adapted photoreceptors. By contrast, the size of the contrast-evoked voltage signals, sV(t), of light-adapted photoreceptors is not proportional to their dark-adapted impulse responses, and photoreceptors with Vmax of
70 mV produce an sV(t) similar to that of photoreceptors with Vmax of
40 mV.
The voltage signal (Fig 3 A) increases with temperature, being in two cells less than the noise at temperatures below 16°C (Fig 3D and Fig F), but much greater under warmer conditions. Strikingly however, the average noise variance is virtually insensitive to the temperature (Fig 3B and Fig F) and its probability distribution (Fig 3 C, dotted line) is Gaussian. Since the warming-induced changes in the signal overwhelm those of the noise, an increasing temperature improves the photoreceptor SNRV often >10-fold over the studied temperature range (Fig 3 G). At least three (not necessary mutually exclusive) interpretations can be suggested to explain why both sV(t) and µ (steady-state potential) increase with warming, while nV(t)i does not. First, the quantum efficiency of photoreceptors (i.e., the probability of producing an elementary voltage response, quantum bump, from an absorbed photon) increases with warming. Thus, the observed larger contrast responses and the steady-state potential at warm temperatures would simply result from the summation of a larger number of bumps. Second, the intracellular pupil mechanism (
The Signal and Noise Dynamics in Frequency Domain
Fig 4 shows the signal and noise power spectra of light-adapted Drosophila photoreceptors, and related functions at different temperatures. Because the photoreceptor signal power spectrum (Fig 4 A) is calculated from the contrast-evoked voltage signals, it contains information about the mean bump waveform and its latency, whereas the noise power spectrum (Fig 4 B), portraying the mean of the coding errors, is largely light-induced voltage noise (i.e., bump voltage noise; SV(f )
|2(Fig 4 A), and extends its bandwidth, whereas the power and shape of the corresponding voltage noise, |
NV(f )
|2 (Fig 4 B), changes relatively little. Assuming that the instrumental noise and light-induced voltage noise are independent but additive, we can estimate the bump voltage noise power, |
BV(f )
|2 (Fig 4 F), at different temperatures by subtracting the photoreceptor voltage noise power spectrum measured in the dark, from the photoreceptor voltage noise power spectra, |
NV(f )
|2, measured at the adapting background of BG0 at different temperatures. Then, by fitting a single Lorentzian to the obtained bump voltage noise power spectra, |
BV(f )
|2:
![]() |
(2) |
we obtain two parameters, n and (
![]() |
(3) |
and the effective duration, T (Fig 4 H), of the bump,
![]() |
(4) |
|
The mean bump amplitude, (used for scaling the bump waveforms in Fig 4 G), is estimated from Campbell's theorem (
![]() |
(5) |
where 2 is the noise variance and µ is the mean membrane potential. The bump rate,
(Fig 4 I), is given by (
![]() |
(6) |
The derived light-induced voltage noise power, |BV(f )
|2 (Fig 4 F), appears to be virtually independent of the temperature. Accordingly, the effective bump duration (Fig 4 G) shows, at most, a marginal decrease with warming. Although the bump amplitude (Fig 4 H) appears to decrease slightly upon warming, this cannot account for the increased steady-state potential, or for the much higher SNRV(f ) (Fig 4 C) and information content (Fig 4 D) of the photoreceptor voltage responses. The Q10 for bump duration (T) and amplitude (
) is 1.2 ± 0.2 and 1.8 ± 0.1, respectively (n = 2). On the other hand, the average bump rate,
(Fig 4 I), increases with warming (Q10 = 4.0 ± 0.2, n = 2). The quantum efficiency of light-adapted Drosophila photoreceptors, hence, increases with temperature, and this may be at least partially responsible for the observed increase in the light-induced steady-state potential at temperatures above 18°C.
We found that, on average, a 10°C warming leads to 6.5 ± 2.8-fold increase in the photoreceptor information capacity (n = 3; Fig 4D and Fig E). Since the average bump rate at different recording temperatures can vary >10-fold (Fig 4 I), so that some photoreceptors with rates <105 bumps/s are still able to have information capacities >300 bits/s, it is very unlikely that the huge increase in the photoreceptor information capacity is solely due to the summation of a larger number of bumps. Presumably, the accelerated bump timing dynamics, as seen in the expanding signal bandwidth (Fig 4 A), is also contributing.
Frequency Response Analysis
The temperature dependence of the photoreceptor signal power spectrum suggests that photoreceptors can follow higher contrast stimulus frequencies at higher temperatures, but this provides no details about the underlying mechanisms. To characterize how warming influences the signaling dynamics, we calculated the photoreceptor frequency response at different temperatures.
The acceleration of signaling dynamics is apparent in the photoreceptor contrast gain, GV(f ) (Fig 5 A). The 3-dB cut-off frequency shifts towards higher frequencies (Q10 = 2.3 ± 0.3, n = 3; Fig 5 B), and the corresponding phase, PV(f ) (Fig 5 C), lags the stimulus less at higher temperatures. Superficially these heat-induced changes in the signal dynamics resemble light adaptation from very dim to very bright mean light, including a significant increase in the absolute contrast gain (
|
The photoreceptor coherence function, exp2(f) (Fig 5 E), is close to unity at all the tested temperatures, reconfirming the earlier findings that the responses of insect photoreceptors to dynamic contrast stimuli are linear (
SNR2(f), which was estimated from the photoreceptor signal-to-noise ratio (see
The effect of warming on the photoreceptor's signaling speed is also clearly seen in the first order Wiener kernels, kV(t) (Fig 5 G). These impulse responses calculated via inverse FFT (see
Bump Latency Distribution Changes with Temperature
The photoreceptor voltage responses to contrast stimulation at a particular mean light intensity level are generated by a summation of bumps. If the average waveform of the bumps is very short and small, the speed and time resolution of the voltage response depends critically on the synchronization of the bumps, i.e., their timing (see -distributionfitted bump waveforms,
V(t) (Fig 4 G), and the calculated latency distributions, respectively, vary with temperature. Fig 6 D shows the normalized bump latency distribution. The bumps appear earlier and in greater synchrony at higher temperature levels. The same is confirmed by calculating the bump latency, l(t), from the photoreceptor frequency responses, TV(f ), and the corresponding voltage noise spectra, |
NV(f )
| (Fig 6 E; see also
![]() |
(7) |
|
The bump latency distribution was also calculated by deconvolving (denoted by in
Equation 8) the
V(t) bump waveforms from the real impulse response data, kV(t) (Fig 6 F):
![]() |
(8) |
All the methods revealed that warming shortens the bump latency distribution and diminishes its width. The corresponding average Q10 for the latency distribution, which was calculated from the peak time and half-width values, are 3.4 ± 0.2 and 3.5 ± 0.5 (n = 3), respectively, coinciding with the Q10 of the dead-time and similar to previously reported Q10 values for the bump latency distribution in Limulus photoreceptors (
Cell Membrane during Natural-like Stimulation
In our companion paper (see
|
Warming Accelerates Both Light Responses and Photoreceptor Membrane
Fig 7 A shows samples of 1 s of the photoreceptor voltage signal and noise evoked by 10-s-long current modulation at different temperatures. Increasing the temperature reduces the amplitude modulation of the voltage signal. In the particular photoreceptor of Fig 7, warming from 22 to 29°C reduces the signal variance by 26%. Since the current stimulus is unchanged, the diminishing average responses at higher temperatures result from reduced membrane impedance. The variance of the voltage noise is small, compared with the signal, and unaffected by the temperature in the studied range. These findings are compared with those of contrast stimulation at the same test temperatures (Fig 7 B). In contrast to the current stimulation and in line with the previous experiments (Fig 3D and Fig F), the photoreceptor signals to light contrast stimulation increase with the temperature. Again, the variance of the photoreceptor voltage noise has no obvious temperature dependence.
Fig 7 C shows typical probability distributions of voltage signals to dynamic contrast stimulation and current injection, |<NVC(f)>|2 and |<NVI(f)>|2, respectively at the test temperatures. Warming broadens the signal distribution and increases its skewness to Gaussian light contrast, but symmetrically reduces the depolarizing and hyperpolarizing voltage signals to Gaussian current injection. This confirms our previous findings (see
Between 3 and 200 Hz, the photoreceptor voltage noise power spectrum appears not to be affected by temperature and current-induced voltage modulation (Fig 7 D), indicating that the processes responsible for the bump shape are fully determined by the adapting light background. Consequently, although different in size, the voltage responses to dynamic light contrast and current stimulation at BG0 are equally reproducible, as seen in their highly similar noise power spectra, |<NVC(f)>|2 and |<NVI(f)>|2, respectively. However, the noise power in the low frequency range below 3 Hz is the highest at 29°C (Fig 4 B). During some experiments at higher temperatures, we observed that the center of the photoreceptor's receptive field shifted sporadically, causing slow fluctuations in the steady-state potential and, thus, affecting the power of the low frequency voltage noise. These movements may be due to an increased rate of intracapsular muscle activity at higher temperatures.
The effects of increased temperature on the photoreceptor membrane are very similar to those of increasing light adaptation shown in our companion paper (see 1.7 and
2.3, respectively, in the photoreceptor of Fig 8 (F and G).
|
Temperature-sensitive Signal and Noise Properties of Light Current
Because light-adapted photoreceptors respond to both the dynamic contrast and current stimulation with linear voltage responses, we can derive the output of the phototransduction cascade (light current), rI(t)i, by deconvolving the contrast-induced voltages, rV(t)i, from the membrane impedance impulse response, z(t), measured in the same cell at the same mean light and temperature (see
![]() |
(9) |
The light current frequency response, TI(f ), is calculated from the contrast stimulus, c(t), and the deconvolved current response, rI(t)i (as shown in
|
The phototransduction noise spectrum, |I(f)|, is estimated by deconvolving the normalized bump noise spectrum, |
V(f)|, with the corresponding membrane impedance, Z(f ):
![]() |
(10) |
Given that the Fourier transform of I(t) is its minimum phase representation in the frequency domain (
I(f)| at different temperatures to the corresponding normalized membrane impedance function, Z(f ) (Fig 9, EG). In general, warming shifts the bandwidth of |
I(f)| in tune with Z(f ) so that they overlap at all the test temperatures (Fig 8, EG;
As the timing of the bumps becomes faster and more precise (as seen in the bump latency distribution, Fig 6) and the changes in the bump waveform are matched by the temperature-sensitive filtering by the photoreceptor membrane (Fig 9), the bandwidth of reliable signaling and the photoreceptor information capacity improves with warming (Fig 10 A). The information capacity increases from values of below 50 bits/s at dim illumination (Fig 10 A) or cool temperature conditions (Fig 4 E) to >400 bits/s during 0.32 dynamic contrast stimulation at BG0 at 29°C. Since the quantum efficiency of the light-adapted photoreceptors drops at cool temperatures, possibly because of some saturation related processes (see DISCUSSION), we also calculated the Q10 for the average information capacity estimates at different mean light intensity levels at 25 and 29°C (where the estimated photoreceptor bump rates (r) for the same adapting backgrounds are very similar). We found that the Q10 for information capacity appears to be roughly independent of the adapting background (Fig 10 B), and, hence, its high value does not result from some light-dependent saturation phenomenon, but is largely due to the increased speed of the phototransduction reactions.
|
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The rate of photon absorption and the dynamics of the phototransduction machinery and the photoreceptor membrane together set the limits for the information capacity of photoreceptor voltage responses, and ultimately for the temporal resolution of neural images affecting visual behavior. Comparative studies of insect photoreceptors suggest that their phototransduction and membrane dynamics are tuned to accommodate the statistical properties of rapidly moving images encountered in the natural habitat (
In the next paragraphs, we will first summarize the general effects of temperature on the photoreceptor responses, compare these to the relevant literature, suggest possible mechanisms behind them, and correlate them to more general neural coding schemes.
Response Dynamics at Cold and Warm Temperatures
In cold environments (below 20°C), photoreceptor signaling is badly impaired. The light-induced steady-state potential is lower (Fig 3 E), although the bump amplitude (Fig 4 G) and duration (Fig 4 H) increase slightly with cooling. The bandwidth of the signal-to-noise ratio and its absolute values (Fig 4 C), even at low frequencies, are greatly reduced (sometimes >10-fold). Since the photon density is high (BG0) and the linear photoreceptor membrane filters the signal and noise of the light current equally (Fig 9), cooling must increase the variability in the bump dynamics in some fundamental way. Indeed, we find that the two most crucial elements of the neural code, the rate of events, and their timing precision, are jeopardized. Thus, cooling not only reduces the quantum efficiency (Fig 4 I), but it also smears out the latency distribution of the bumps in time (Fig 6 D), so that the light contrasts produce smaller and less synchronized responses (Fig 5 G).
In warm environments (above 25°C), photoreceptors produce large responses with little noise. Warming slightly reduces the average shape and size of the bumps (Fig 4 G), yet, more importantly, it increases the effective rate of bump production (Fig 4 I), shortens the time delays in phototransduction (i.e., the bump latency distribution; Fig 6 D), and accelerates the photoreceptor membrane dynamics (Fig 8 F). As photoreceptor signaling is faster and has a higher quantum efficiency, the phototransduction cascade can generate faster and larger receptor currents, which are accommodated by the accelerated membrane characteristics so that the resulting voltage responses are more reproducible.
Sensitivity to Temperature
The temperature sensitivity of biochemical reactions is expressed by Q10, which is the fractional increase in their speed per 10°C. In vertebrate photoreceptors, Q10 values of light response kinetics are 2 (
Our study is unique in the sense that we could isolate the effects of temperature on the phototransduction signal and noise and the filtering properties of the photoreceptor membrane by applying combined shot noise and signal analysis. This investigation reveals that the phototransduction processes related to the signal timing and the quantum efficiency (QE) are highly temperature-sensitive. The Q10 values for the dead-time, bump latency distribution, and the bump rate are 3.1, 3.5, and 4.0, respectively. On the other hand, the stochastic processes responsible for the voltage noise of light-adapted photoreceptors and the filtering properties of the membrane are less temperature-sensitive. Here, in contrast to findings of
Early Enzymatic and Late Diffusion Reactions
In our companion article on signaling dynamics in Drosophila photoreceptors at 25°C (see
Reduction of the Quantum Efficiency
An unexpected finding of this study is the high temperature sensitivity of bump production rate in bright light conditions. What kind of processes could reduce the effective QE of light-adapted photoreceptors? Saturation of the available transduction units, possibly individual microvilli, has been shown to occur under very bright daylight conditions in Calliphora (1030 times the estimated rate of the photons absorbed at the same temperature (30,000100,000 photons/s), it is very unlikely that the phototransduction machinery is operating right at its saturation level. Another evidence for this conclusion comes from the information capacity recordings at different mean light intensity levels (Fig 10 A). We find a similarly steep temperature dependence of information capacity at the adapting backgrounds of BG-3 and BG-2, where the number of photons per second absorbed is less than the number of transduction units.
Further experiments will be required to determine the cause of the unexpected loss of QE at lower temperatures. It does not appear to occur at the level of the visual pigment, since the dark-adapted QE appears to be unaffected by cooling to 15°C (Hardie, R.C., unpublished observations); but, it might represent saturation/exhaustion of some limiting step in the phototransduction pathway such as the PLC substrate (PIP2), which must be continually recycled via a multi-enzyme resynthesis process.
Temperature-dependent Limitations on the Speed of the Voltage Responses
Because of the high cut-off frequency of the photoreceptor membrane, the speed of the photoreceptor voltage responses is not significantly limited by the membrane over the tested temperature range, but is set by the delays in the phototransduction cascade. However, since the Q10 for the membrane corner frequency is 1.7 and the Q10 of latency processes is over 3, in high temperatures the filtering effect by the membrane on the light current becomes gradually more important, but not limiting. On the other hand, at 35°C, the extrapolated average bump duration would be 7.5 ms, which is 60% larger than the estimated half-width of the latency distribution of 4.3 ms. Hence, at such high temperatures, the speed of the light current would depend at least as much on the average bump duration as it does on the bump timing.
Benefits of Accelerated Responses
Previous studies in toads on the effect of temperature on visual performance have emphasized how cooling can improve performance by reducing the rate of thermal isomerizations of rhodopsin, thereby lowering the absolute detection threshold (
Conclusion
In summary, we have provided a comprehensive description of the temporal resolving capability in Drosophila photoreceptors under natural conditions and, to our knowledge, the first analysis of the effects of temperature on information capacity in the nervous system. Although it has often been reported that temperature accelerates the kinetics of light responses (
![]() |
Acknowledgements |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We thank Andrew French, Hugh Robinson, and Matti Weckström for their comments in the initial stages of this work, Doekele Stavenga for critical reading of the final draft, and Simon Laughlin for discussions and drawing our attention to the relevant literature on visual ecology. Special thanks to Mick Swann and Chris Askham for taking part in designing and building the new set-up.
This work was supported by grants from The Royal Society, Academy of Finland, Wellcome Trust and Oskar Öfflund Foundation (to M. Juusola), and Biotechnology and Biological Sciences Research Council (to R.C. Hardie).
Submitted: 10 August 2000
Revised: 14 August 2000
Accepted: 16 August 2000
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
French, A.S. 1980. Phototransduction in the fly compound eye exhibits temporal resonances and a pure time delay. Nature. 283:200-202[Medline].
French, A.S., and Järvilehto, M. 1978. The dynamic behaviour of photoreceptor cells in the fly in response to random (white noise) stimulation at a range of temperatures. J. Physiol. 274:311-322[Abstract].
Hardie, R.C. 1991. Voltage-sensitive potassium channels in Drosophila photoreceptors. J. Neurosci. 10:3079-3095[Abstract].
Heinrich, B. 1993. The hod-blooded insects. Berlin, Springer-Verlag, pp. 600 pp.
Henderson, S.R., Reuss, H., and Hardie, R.C. 2000. Single photon responses in Drosophila photoreceptors and their regulation by Ca2+. J. Physiol. 524:179-194
Hevers, W., and Hardie, R.C. 1995. Serotonin modulates the voltage dependence of delayed rectifier and Shaker potassium channels in Drosophila photoreceptors. Neuron. 14:845-856[Medline].
Hochstrate, P., and Hamdorf, K. 1990. Microvillar components of light adaptation in blowflies. J. Gen. Physiol. 95:891-910[Abstract].
Howard, J., Blakeslee, B., and Laughlin, S.B. 1987. The intracellular pupil mechanism and the maintenance of photoreceptor signal to noise ratios in the blowfly Lucilia cuprina. Proc. R. Soc. Lond. B. 23:415-435.
Juusola, M. 1993. Linear and non-linear contrast coding in light adapted blowfly photoreceptors. J. Comp. Physiol. A. 172:511-521.
Juusola, M., and R.C. Hardie. 2000. Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25°C. J. Gen. Physiol. 325.
Juusola, M., Kouvalainen, E., Järvilehto, M., and Weckström, M. 1994. Contrast gain, signal-to-noise ratio and linearity in light adapted blowfly photoreceptors. J. Gen. Physiol. 104:593-621[Abstract].
Lamb, T.D. 1984. Effects of temperature-changes on toad rod photocurrents. J. Physiol. 346:557-578[Abstract].
Laughlin, S.B. 1981. A simple coding procedure enhances a neurone's information capacity. Z. Naturforsch. 36:910-912.
Laughlin, S.B., and Weckström, M. 1993. Fast and slow photoreceptors: a comparative study of the functional diversity of coding and conductances in the Diptera. J. Comp. Physiol. A. 172:593-609.
Leutscher-Hazellhoff, J.T. 1975. Linear and nonlinear performance of transducer and pupil in Calliphora retinular cells. J. Physiol. 246:333-350[Abstract].
Lo, M.-V., and Pak, W.L. 1981. Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. J. Gen. Physiol. 77:155-175[Abstract].
McCann, G.D., and MacGinitie, G.F. 1965. Optomotor response studies of insect vision. Proc. R. Soc. Lond. B. 163:269-401.
Pak, W.L., Ostroy, S.E., Deland, M.C., and Wu, C.-F. 1976. Photoreceptor mutant of Drosophila: is protein involved in intermediate steps of phototransduction? Science 194:956-959[Medline].
Postma, M., Oberwinkler, J., and Stavenga, D.G. 1999. Does Ca2+ reach millimolar concentrations after single photon absorption in Drosophila photoreceptor microvilli? Biophys. J 77:1811-1823
Roebroek, J.G.H., van Tjonger, M., and Stavenga, D.G. 1990. Temperature dependence of receptor potential and noise in fly (Calliphora erythocephala) photoreceptor cells. J. Insect Physiol. 36:499-505.
Scott, K., Becker, A., Sun, Y., Hardy, R., and Zuker, C.S. 1995. G(alpha) protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron 15:919-927[Medline].
Scott, K., and Zuker, C.S. 1998. Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses. Nature. 395:805-808[Medline].
Tatler, B., O'Carroll, D.C., and Laughlin, S.B. 2000. Temperature and the temporal resolving power of fly photoreceptors. J. Comp. Physiol. A. 186:399-407[Medline].
Weckström, M., and Laughlin, S.B. 1995. Visual ecology and voltage-gated ion channels in insect photoreceptors. Trend. Neurosci. 18:17-21[Medline].
Wong, F., and Knight, B.W. 1980. Adapting-bump model for eccentric cells of Limulus. J. Gen. Physiol. 76:539-557[Abstract].
Wong, F., Knight, B.W., and Dodge, F.A. 1980. Dispersion of latencies in photoreceptors of Limulus and the adapting-bump model. J. Gen. Physiol. 76:517-537[Abstract].
|
|