Neuroscience Letters, 111 (1990) 87-91 Elsevier Scientific Publishers Ireland Ltd.
87
NSL 06758
Evidence for light-induced release of Ca 2 + from intracellular stores in bee photoreceptors Andreas Ziegler and Bernd Walz
lnstitut fiir Zoologie, Universitiit Regensburg, Regensburg ( F.R.G.) (Received 10 October 1989; Revised version received 30 November 1989; Accepted 4 December 1989)
Key words: Calcium;Intracellular store; Extracellular space; Compound eye; Photoreceptor; Honeybee In the drone retina light elicits an increase in the extracellular Ca2+ concentration ([Ca]o). After withdrawal of extracellular Ca2÷ and addition of 1 mM EGTA (ethyleneglycol-bis (fl-aminoethyl ether) N,N,N',N'-tetraacetic acid) a short light flash still caused an increase in [Ca]oas measured with Ca2+-sensitive microelectrodes. This increase vanished after a few flashes. When [Ca]owas reduced to 10-5 M Ca2+ (no EGTA) the rise in Cao disappeared after several light flashes. Subsequent stimulation with a dim steady light produced a decrease in [Ca]o and caused a recovery of the increase in [Ca]o elicited by a test flash. The results show that bee photoreceptors have a light-depletable intracellular Ca2÷ store which can be reloaded by dim continuous lights.
In invertebrate photoreceptor cells, a light-induced increase in the intracellular free Ca 2+ concentration ([Ca]i) causes light adaptation and is perhaps also a necessary step in the reaction chain leading to excitation [6, 8]. The increase in Cai in the ventral nerve p h o t o r e c e p t o r o f Limulus results in part f r o m a release o f Ca 2+ from intracellular stores. The release is mediated by inositol 1,4,5-trisphosphate (Ins(1,4,5)P3) [9]. In contrast, the photoreceptors o f Balanus exhibit a light-induced increase in [Ca]i which is apparently entirely caused by an influx o f Ca 2+ from the extracellular space (ECS) [3]. Thus the sources f r o m which light mobilizes Ca 2+ appear to differ according to species. F o r the photoreceptors in the c o m p o u n d eyes o f insects it is u n k n o w n whether light induces Ca 2+ release from intracellular stores. In the photoreceptors o f the h o n e y bee drone (Apis mellifera) the endoplasmic reticulum (ER) has been identified as a morphologically extensive, Ins(1,4,5)Pa-sensitive Ca 2+ store [1, 2]. While intracellular Ca2+-measurements are difficult in these cells, it is possible to record large light-induced changes in the extracellular Ca 2+ concentration ([Ca]o) with Ca2+-sensitive microelectrodes [7, 11]. These changes are due
Correspondence." B. Walz, Institut fiir Zoologic, Universitiit Regensburg, D-8400 Regensburg, Universitfitsstr. 31, F.R.G. 0304-3940/90/$ 03.50 © 1990 Elsevier Scientific Publishers Ireland Ltd.
8~
m,~ o.8
~
-
Cao Eref
'.[
I min .
~
e
+EGTA
mM 0.1
*-_,_.i
-- Ca o I
,, Eref
~ Ca 0 -
-,
E ref
I min Ca o
d
Eref
f
i
t 1 min
I
Ca ° 1 rain
~ Ca-free +EGTA
t /r
/ ~
/ 4F ~ E ref e
Fig. 1. Effect of drastic extracellular Ca 2+ reduction on changes in Cao elicited by strong 20 ms light flashes. All responses are from one continuous recording. Cao, apparent extracellular Ca 2÷ concentration; Eref, extracellularly recorded field potentials, a: light-induced change in [Ca]o in normal physiological saline (PS). The spikes at the beginning of the responses are electrical subtraction artefacts, b: change of resting [Ca],, after superfusion with 0-Ca :+ saline in the dark. c,d: light-induced changes in [Ca]o in 0-Ca 2÷ PS (containing 1 mM EGTA), e: recovery of resting [Ca]o after superfusion with normal PS. The insert shows the electrodes response to a change from normal to 0-Ca 2+ PS, while the tip of the electrode was in the bath.
to C a 24 fluxes b e t w e e n p h o t o r e c e p t o r s a n d E C S [11]. T h e i n c r e a s e in t h e Cao is m e d i a t e d by the N a / C a - e x c h a n g e m e c h a n i s m [7, 11]. S t r o n g , 20 m s light flashes elicit a b i p h a s i c c h a n g e in the Cao. A s h o r t d e c r e a s e in the Cao is f o l l o w e d by a large t r a n s i e n t i n c r e a s e (Fig. l a ) [11]. P a r t o f the i n c r e a s e
89 in the [Ca]o could be due to Ca 2+ that was released from the ER and extruded across the plasma membrane. We approached this open question by analysing light-induced changes in the Cao in slices of drone retina which were superfused with physiological saline solutions (PS) of reduced Ca 2+ content. The extracellular measurements were made with double-barreled Ca2+-sensitive microelectrodes containing the neutral Ca 2+ ligand ETH 1001 (Fluka). The electrodes were fabricated and the recordings made as previously described in detail [11]. For the calibration of the electrodes we used PS of equal ionic strength containing 10, 1, 0.1 and 0.01 mM Ca 2+. The slice preparation was continuously superfused with an oxygenated PS containing 270 mM NaC1, 10 mM KCI, 1.6 mM CaC12, 10 mM MgC12 and l0 mM Tris(hydroxymethyl)aminomethane(pH: 7.4). When the slice was superfused in darkness with a PS containing 1 mM EGTA (ethylenglycol-bis(fl-aminoethyl ether) N,N,N',N'-tetraacetic acid) and no calcium added (0-Ca 2+ PS), the [Ca]o decreased very slowly to a value too small for detection ([Ca]o < 10 - 6 M ) (Fig. lb). After 10-60 min in 0-Ca 2+ PS in the dark light flashes still caused a change in Cao, apparently biphasic (Fig. lc). The transient rise in Cao vanished completely after a few flashes (Fig. Ice). This was observed in 8 out of 13 experiments. In 5 experiments light failed to induce an increase in the [Ca]o after 15-20 min in 0-Ca 2+ PS in the dark. Fig. le shows the recovery of the [Ca]o after returning to normal PS. The insert presents the measurement of bath Ca 2+ concentration in normal and 0-Ca 2+ PS after the electrode was withdrawn from the tissue. These measurements using 0-Ca 2+, EGTA-containing PS allowed only a qualitative interpretation. For quantitative measurements we designed experiments in which neither Ca 2+ nor EGTA were added to the superfusate (low-Ca PS, [Ca 2+] ~ 10 -5 M as determined with a Ca2+-sensitive macroelectrode). Fig. 2a shows the change in the [Ca]o after a 20 ms light flash in normal PS. The initial decrease in [Ca]o is undetectably small in this particular recording (probably because of the high resting [Ca]o). After superfusion with low-Ca PS for 55 min in darkness the resting [Ca]o was reduced to 80/tM. Then, the preparation was stimulated with a 20 ms light flash about once every 3.5 min. The first flash induced a transient rise in [Ca]o of 140/~M. After the 4th flash the light-induced rise in [Ca]o was reduced to 50/zM and vanished after the 1l th flash (Fig. 2b). The transient increase in [Ca]o induced by a 20 ms test flash recovered after exposure to a dim, continuous (1 min) light of an intensity 10 4 times lower than that of the 20 ms flashes. These dim lights produced a decrease in [Ca]o from 36 to 15/~M (not shown). After the dim illumination the [Ca]o recovered slowly to a value of 22/~M. A strong 20 ms test flash given after 2 such conditioning lights produced an increase of [Ca]o by 13/tM (Fig. 2c). Ca2+-sensitive electrodes are somewhat Na+-sensitive when they are used in 0-Ca 2+ PS (containing 1 mM EGTA). The initial transient decrease in [Ca]o observed in 0-Ca 2+ PS (Fig. lc--e) is due to the light-induced decrease in the extracellular Na + concentration ([Na]o). Such a decrease had been observed in drone retina before [4]. The transient increase observed in the recordings shown in Fig. lc,d is due to the rise in [Ca]o above the detection limit of the Ca2+-sensitive microelectrode (which is about 10 -5 M using PS containing 270 mM Na+). This increase in Cao must result
90
El
E re f lOm
C.,.,m.iOl/
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~.c°ntr°l
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Eref
/
low-Cao (-O-'M)
/
80 100
@-94'
~'-~'~~
/
Cao'b,M) C
35[ 22
l
f~_~_ ~--~ /, /
'i,i/
~ ~-~
106' after 2xlmin cont, light I
, ,,
20 S
I
Fig. 2. Effect of a physiological saline (PS) at a reduced Ca 2 ~ concentration (Ca 2+ ~ 10 -5 M) on changes in [Ca]o produced by 20 ms light flashes. All recordings are from the same experiment. Cao, extracellular Ca 2÷ concentration; Eref, extracellularly recorded field potential, a: light-induced change in [Ca]o in normal physiological saline (PS). b: light-induced changes in Cao in low-Ca 2+ PS produced by some representative light flashes from a series. The preparation was stimulated with one flash every 3.5 min after 55 min of superfusion in darkness. The responses of the 1st, 4th and 1 lth flash in the series are presented (labeled 1, 2 and 3, respectively), c: recovery of the light-induced increase in [Ca]o in low-Ca 2÷ PS after stimulation with dim continuous light.
from Ca 2+ released from a light-sensitive intracellular Ca 2+ store, which is most probably the ER in the photoreceptor cells [1]. Since the light-induced change vanishes after a few flashes, the Ca 2+ store is light-depletable. A contribution of the pigmented glial cells to the transient rise in Cao is very unlikely because the recordings were made close to the basal membrane. Here the pigmented glial cells are very narrow and contain little ER and no pigment granules [2]. The observation that in some cases
91
light did not elicit an increase in [Ca]o after the prolonged superfusion with 0-Ca 2+ PS indicates that the intracellular Ca 2+ stores are also depleted by the prolonged withdrawal of extracellular Ca 2+, even in darkness. In the experiment with low-Ca 2+ PS the initial transient decreases of [Ca]o (Fig. 2b,c) are due to decreases in the extracellular Ca 2+ concentration. The experiment confirms the qualitative result of that with 0-Ca 2+ PS containing EGTA: the light-induced transient increase in Cao is due tot Ca 2+ released from a light-depletable intracellular Ca2+ store. In addition, this experiment shows that these stores can be reloaded with Ca 2+ by continuous dim lights. These stimuli produced a decrease in [Ca]0 that also occurs in normal PS [11]. The decrease is probably brought about by an influx of Ca 2+ into the photoreceptor cells. It has been shown that the ER in the photoreceptors of the drone [2] and other invertebrates [5, 10] accumulates Ca 2+ actively. Therefore, the Ca2+-influx from the" ECS caused by dim continuous lights has probably reloaded the light-depleted intracellular Ca 2+ stores. The recovery of the light-induced increase following a strong test flash is in accordance with this interpretation. This work was supported by a grant from the Deutsche Forschungsgemeinschaft (SFB 4, I 1). We wish to thank Ms. E. v. Ciriacy-Wantrup for excellent technical assistence. We are grateful to Dr. R. Loftus for attentive linguistic corrections. 1 Baumann, O. and Walz, B., Calcium and inositol polyphosphate-sensitivity of the calcium sequestering
2
3 4 5 6
7 8
9
10 I1
endoplasmic reticulum in the photoreceptor cells of the honey bee drone, J. Comp. Physiol. A, 165 (1989) 627436. Baumann, O. and Walz, B., Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honey bee drone, Cell Tissue Res., 255 (1989b) 511-522. Brown, J.E. and Blinks, J.R., Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin, J. Gen. Physiol., 64 (1974) 643~65. Coles, J.A. and Orkand R.K., Changes in sodium activity during light stimulation in photoreceptors, glia and extracellular space in drone retina, J. Physiol. (Lond.), 362 (1985) 415-435. Frixone, E. and Ruiz, L. Calcium uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish, J. Comp. Physiol., 162 (1988) 91-100. Lisman, J.E. and Brown, J.E., The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus vental photoreceptors, J. Gen. Physiol., 59 (1972) 701-719. Minke, B. and Tsacopoulos, M., Light induced sodium dependent accumulation of calcium and potasium in the extracellular space of bee retina, Vision Res., 26 (1986) 679490. Payne, R., Corson, D.W., Fein, A. and Berridge, M.J., Excitation and adaptation of Limulus ventral photoreceptor by inositol (1,4,5,)trisphosphate results from a rise in intracellular calcium, J. Gen. Physiol., 88 (1986) 127-142. Payne, R., Walz, B., Levy, S. and Eein, A., The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its contol by negative feedback, Phil. Trans. R. Soc. Lond. Ser. B, 320 (1988) 359-379. Walz, B., Ca2*-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor II. Its properties as revealed by microphotometric measurement, J. Cell Biol., 93 (1982) 849-859. Ziegler, A. and Walz, B., Analysis of extracellular calcium and volume changes in the compound eye of the honey bee drone, Apis mellifera, J. Comp. Physiol. A, 165 (1989) 697-709.
87
NSL 06758
Evidence for light-induced release of Ca 2 + from intracellular stores in bee photoreceptors Andreas Ziegler and Bernd Walz
lnstitut fiir Zoologie, Universitiit Regensburg, Regensburg ( F.R.G.) (Received 10 October 1989; Revised version received 30 November 1989; Accepted 4 December 1989)
Key words: Calcium;Intracellular store; Extracellular space; Compound eye; Photoreceptor; Honeybee In the drone retina light elicits an increase in the extracellular Ca2+ concentration ([Ca]o). After withdrawal of extracellular Ca2÷ and addition of 1 mM EGTA (ethyleneglycol-bis (fl-aminoethyl ether) N,N,N',N'-tetraacetic acid) a short light flash still caused an increase in [Ca]oas measured with Ca2+-sensitive microelectrodes. This increase vanished after a few flashes. When [Ca]owas reduced to 10-5 M Ca2+ (no EGTA) the rise in Cao disappeared after several light flashes. Subsequent stimulation with a dim steady light produced a decrease in [Ca]o and caused a recovery of the increase in [Ca]o elicited by a test flash. The results show that bee photoreceptors have a light-depletable intracellular Ca2÷ store which can be reloaded by dim continuous lights.
In invertebrate photoreceptor cells, a light-induced increase in the intracellular free Ca 2+ concentration ([Ca]i) causes light adaptation and is perhaps also a necessary step in the reaction chain leading to excitation [6, 8]. The increase in Cai in the ventral nerve p h o t o r e c e p t o r o f Limulus results in part f r o m a release o f Ca 2+ from intracellular stores. The release is mediated by inositol 1,4,5-trisphosphate (Ins(1,4,5)P3) [9]. In contrast, the photoreceptors o f Balanus exhibit a light-induced increase in [Ca]i which is apparently entirely caused by an influx o f Ca 2+ from the extracellular space (ECS) [3]. Thus the sources f r o m which light mobilizes Ca 2+ appear to differ according to species. F o r the photoreceptors in the c o m p o u n d eyes o f insects it is u n k n o w n whether light induces Ca 2+ release from intracellular stores. In the photoreceptors o f the h o n e y bee drone (Apis mellifera) the endoplasmic reticulum (ER) has been identified as a morphologically extensive, Ins(1,4,5)Pa-sensitive Ca 2+ store [1, 2]. While intracellular Ca2+-measurements are difficult in these cells, it is possible to record large light-induced changes in the extracellular Ca 2+ concentration ([Ca]o) with Ca2+-sensitive microelectrodes [7, 11]. These changes are due
Correspondence." B. Walz, Institut fiir Zoologic, Universitiit Regensburg, D-8400 Regensburg, Universitfitsstr. 31, F.R.G. 0304-3940/90/$ 03.50 © 1990 Elsevier Scientific Publishers Ireland Ltd.
8~
m,~ o.8
~
-
Cao Eref
'.[
I min .
~
e
+EGTA
mM 0.1
*-_,_.i
-- Ca o I
,, Eref
~ Ca 0 -
-,
E ref
I min Ca o
d
Eref
f
i
t 1 min
I
Ca ° 1 rain
~ Ca-free +EGTA
t /r
/ ~
/ 4F ~ E ref e
Fig. 1. Effect of drastic extracellular Ca 2+ reduction on changes in Cao elicited by strong 20 ms light flashes. All responses are from one continuous recording. Cao, apparent extracellular Ca 2÷ concentration; Eref, extracellularly recorded field potentials, a: light-induced change in [Ca]o in normal physiological saline (PS). The spikes at the beginning of the responses are electrical subtraction artefacts, b: change of resting [Ca],, after superfusion with 0-Ca :+ saline in the dark. c,d: light-induced changes in [Ca]o in 0-Ca 2÷ PS (containing 1 mM EGTA), e: recovery of resting [Ca]o after superfusion with normal PS. The insert shows the electrodes response to a change from normal to 0-Ca 2+ PS, while the tip of the electrode was in the bath.
to C a 24 fluxes b e t w e e n p h o t o r e c e p t o r s a n d E C S [11]. T h e i n c r e a s e in t h e Cao is m e d i a t e d by the N a / C a - e x c h a n g e m e c h a n i s m [7, 11]. S t r o n g , 20 m s light flashes elicit a b i p h a s i c c h a n g e in the Cao. A s h o r t d e c r e a s e in the Cao is f o l l o w e d by a large t r a n s i e n t i n c r e a s e (Fig. l a ) [11]. P a r t o f the i n c r e a s e
89 in the [Ca]o could be due to Ca 2+ that was released from the ER and extruded across the plasma membrane. We approached this open question by analysing light-induced changes in the Cao in slices of drone retina which were superfused with physiological saline solutions (PS) of reduced Ca 2+ content. The extracellular measurements were made with double-barreled Ca2+-sensitive microelectrodes containing the neutral Ca 2+ ligand ETH 1001 (Fluka). The electrodes were fabricated and the recordings made as previously described in detail [11]. For the calibration of the electrodes we used PS of equal ionic strength containing 10, 1, 0.1 and 0.01 mM Ca 2+. The slice preparation was continuously superfused with an oxygenated PS containing 270 mM NaC1, 10 mM KCI, 1.6 mM CaC12, 10 mM MgC12 and l0 mM Tris(hydroxymethyl)aminomethane(pH: 7.4). When the slice was superfused in darkness with a PS containing 1 mM EGTA (ethylenglycol-bis(fl-aminoethyl ether) N,N,N',N'-tetraacetic acid) and no calcium added (0-Ca 2+ PS), the [Ca]o decreased very slowly to a value too small for detection ([Ca]o < 10 - 6 M ) (Fig. lb). After 10-60 min in 0-Ca 2+ PS in the dark light flashes still caused a change in Cao, apparently biphasic (Fig. lc). The transient rise in Cao vanished completely after a few flashes (Fig. Ice). This was observed in 8 out of 13 experiments. In 5 experiments light failed to induce an increase in the [Ca]o after 15-20 min in 0-Ca 2+ PS in the dark. Fig. le shows the recovery of the [Ca]o after returning to normal PS. The insert presents the measurement of bath Ca 2+ concentration in normal and 0-Ca 2+ PS after the electrode was withdrawn from the tissue. These measurements using 0-Ca 2+, EGTA-containing PS allowed only a qualitative interpretation. For quantitative measurements we designed experiments in which neither Ca 2+ nor EGTA were added to the superfusate (low-Ca PS, [Ca 2+] ~ 10 -5 M as determined with a Ca2+-sensitive macroelectrode). Fig. 2a shows the change in the [Ca]o after a 20 ms light flash in normal PS. The initial decrease in [Ca]o is undetectably small in this particular recording (probably because of the high resting [Ca]o). After superfusion with low-Ca PS for 55 min in darkness the resting [Ca]o was reduced to 80/tM. Then, the preparation was stimulated with a 20 ms light flash about once every 3.5 min. The first flash induced a transient rise in [Ca]o of 140/~M. After the 4th flash the light-induced rise in [Ca]o was reduced to 50/zM and vanished after the 1l th flash (Fig. 2b). The transient increase in [Ca]o induced by a 20 ms test flash recovered after exposure to a dim, continuous (1 min) light of an intensity 10 4 times lower than that of the 20 ms flashes. These dim lights produced a decrease in [Ca]o from 36 to 15/~M (not shown). After the dim illumination the [Ca]o recovered slowly to a value of 22/~M. A strong 20 ms test flash given after 2 such conditioning lights produced an increase of [Ca]o by 13/tM (Fig. 2c). Ca2+-sensitive electrodes are somewhat Na+-sensitive when they are used in 0-Ca 2+ PS (containing 1 mM EGTA). The initial transient decrease in [Ca]o observed in 0-Ca 2+ PS (Fig. lc--e) is due to the light-induced decrease in the extracellular Na + concentration ([Na]o). Such a decrease had been observed in drone retina before [4]. The transient increase observed in the recordings shown in Fig. lc,d is due to the rise in [Ca]o above the detection limit of the Ca2+-sensitive microelectrode (which is about 10 -5 M using PS containing 270 mM Na+). This increase in Cao must result
90
El
E re f lOm
C.,.,m.iOl/
""" ~ - ~
~.c°ntr°l
1.9t
b
Eref
/
low-Cao (-O-'M)
/
80 100
@-94'
~'-~'~~
/
Cao'b,M) C
35[ 22
l
f~_~_ ~--~ /, /
'i,i/
~ ~-~
106' after 2xlmin cont, light I
, ,,
20 S
I
Fig. 2. Effect of a physiological saline (PS) at a reduced Ca 2 ~ concentration (Ca 2+ ~ 10 -5 M) on changes in [Ca]o produced by 20 ms light flashes. All recordings are from the same experiment. Cao, extracellular Ca 2÷ concentration; Eref, extracellularly recorded field potential, a: light-induced change in [Ca]o in normal physiological saline (PS). b: light-induced changes in Cao in low-Ca 2+ PS produced by some representative light flashes from a series. The preparation was stimulated with one flash every 3.5 min after 55 min of superfusion in darkness. The responses of the 1st, 4th and 1 lth flash in the series are presented (labeled 1, 2 and 3, respectively), c: recovery of the light-induced increase in [Ca]o in low-Ca 2÷ PS after stimulation with dim continuous light.
from Ca 2+ released from a light-sensitive intracellular Ca 2+ store, which is most probably the ER in the photoreceptor cells [1]. Since the light-induced change vanishes after a few flashes, the Ca 2+ store is light-depletable. A contribution of the pigmented glial cells to the transient rise in Cao is very unlikely because the recordings were made close to the basal membrane. Here the pigmented glial cells are very narrow and contain little ER and no pigment granules [2]. The observation that in some cases
91
light did not elicit an increase in [Ca]o after the prolonged superfusion with 0-Ca 2+ PS indicates that the intracellular Ca 2+ stores are also depleted by the prolonged withdrawal of extracellular Ca 2+, even in darkness. In the experiment with low-Ca 2+ PS the initial transient decreases of [Ca]o (Fig. 2b,c) are due to decreases in the extracellular Ca 2+ concentration. The experiment confirms the qualitative result of that with 0-Ca 2+ PS containing EGTA: the light-induced transient increase in Cao is due tot Ca 2+ released from a light-depletable intracellular Ca2+ store. In addition, this experiment shows that these stores can be reloaded with Ca 2+ by continuous dim lights. These stimuli produced a decrease in [Ca]0 that also occurs in normal PS [11]. The decrease is probably brought about by an influx of Ca 2+ into the photoreceptor cells. It has been shown that the ER in the photoreceptors of the drone [2] and other invertebrates [5, 10] accumulates Ca 2+ actively. Therefore, the Ca2+-influx from the" ECS caused by dim continuous lights has probably reloaded the light-depleted intracellular Ca 2+ stores. The recovery of the light-induced increase following a strong test flash is in accordance with this interpretation. This work was supported by a grant from the Deutsche Forschungsgemeinschaft (SFB 4, I 1). We wish to thank Ms. E. v. Ciriacy-Wantrup for excellent technical assistence. We are grateful to Dr. R. Loftus for attentive linguistic corrections. 1 Baumann, O. and Walz, B., Calcium and inositol polyphosphate-sensitivity of the calcium sequestering
2
3 4 5 6
7 8
9
10 I1
endoplasmic reticulum in the photoreceptor cells of the honey bee drone, J. Comp. Physiol. A, 165 (1989) 627436. Baumann, O. and Walz, B., Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honey bee drone, Cell Tissue Res., 255 (1989b) 511-522. Brown, J.E. and Blinks, J.R., Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin, J. Gen. Physiol., 64 (1974) 643~65. Coles, J.A. and Orkand R.K., Changes in sodium activity during light stimulation in photoreceptors, glia and extracellular space in drone retina, J. Physiol. (Lond.), 362 (1985) 415-435. Frixone, E. and Ruiz, L. Calcium uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish, J. Comp. Physiol., 162 (1988) 91-100. Lisman, J.E. and Brown, J.E., The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus vental photoreceptors, J. Gen. Physiol., 59 (1972) 701-719. Minke, B. and Tsacopoulos, M., Light induced sodium dependent accumulation of calcium and potasium in the extracellular space of bee retina, Vision Res., 26 (1986) 679490. Payne, R., Corson, D.W., Fein, A. and Berridge, M.J., Excitation and adaptation of Limulus ventral photoreceptor by inositol (1,4,5,)trisphosphate results from a rise in intracellular calcium, J. Gen. Physiol., 88 (1986) 127-142. Payne, R., Walz, B., Levy, S. and Eein, A., The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its contol by negative feedback, Phil. Trans. R. Soc. Lond. Ser. B, 320 (1988) 359-379. Walz, B., Ca2*-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor II. Its properties as revealed by microphotometric measurement, J. Cell Biol., 93 (1982) 849-859. Ziegler, A. and Walz, B., Analysis of extracellular calcium and volume changes in the compound eye of the honey bee drone, Apis mellifera, J. Comp. Physiol. A, 165 (1989) 697-709.
