Electrical Properties of Developing Oocytes of the Migratory Locust, Locusta migratoria ZVI WOLLBERG, EPHRAIM COHEN A N D MOSHE KALINA Department of Zoology, The George S . W i s e Center f o r Life Sciences, a n d Department of Cell Biology a n d Histology, Sackler School of Medicine, Tel-Auiv University, Tel-Auiv, Israel

ABSTRACT The electrical properties of developing nonfertilized oocytes of Locusta mzgratorza were studied, using intracellular microelectrodes. The inseries potential of the combined oomembrane and of the follicular cells was about 20 mV in the youngest oocytes. It increased as the oocytes developed and it reached a plateau of about 50 mV before f u U maturation, generally four to seven oocytes away from the fully-developed terminal oocyte. Current-voltage relations were always linear for hyperpolarizing currents. Most oocytes exhibited, however, rectification to outward current. Input resistance values varied with oocyte size from about 5 X 106 ohm for young oocytes to about 0.2 X 1 0 6 ohm for the more developed ones. Some oocytes displayed a transient depolarization on turning off a hyperpolarizing step of current. This depolarization was not correlated with the size of the oocyte or with any observed morphological feature. Any two adjacent oocytes were electrotonically coupled. A single ovariole thus represented a longitudinal chain of developing oocytes which were connected electrically. This was supported by electron microscope observations which revealed junctions partially impermeable to lanthanum and gap junctions between the follicular cells themselves and between follicular cells a n d oocytes. The coupling coefficient was dependent on the direction of current flow. The attenuation of voltage along a n ovariole was always greater at the distal than a t the proximal side.

The female reproductive system of insects includes a pair of ovaries. Each ovary consists of a series of oocyte tubes or ovarioles. Locusts have the primitive panoistic type of ovarioles, where the developing oocytes are not associated with special nurse cells (Imms, '64). Each oocyte is surrounded by follicular cells and a single ovariole forms a chain of "oocyte-chambers" held together by an ovariole sheath. The follicular cells which face this sheath are arranged in a monolayer. However, any two adjacent oocytes are separated by several layers of follicular cells. The oocytes become progressively larger towards the oviduct, yet yolk deposition takes place at the terminal oocyte only. The surface membrane of the terminal oocyte is engaged in absorption of vitellogenins from the haemolymph. This process involves the action of a juvenile hormone (JH) which is present when females are at their reproductive period (Highnam, '64; Minks, '67). J. CELL.


... 8 8 :


It should be mentioned that penultimate oocy tes are also capable of selectively absorbing vitellogenins, but apparently require higher levels of JH than those existing in the normal reproductive female (E. Wajc, personal communication). The latter may point to a gradual change in the capacity of oocytes along the ovariole to respond to the gonadotropic hormone. The difference in the membrane sensitivity to the hormone presumably reflects some maturation process of the oocyte membrane. Therefore, one may also expect changes in the electrical properties of the oocyte membrane along the ovariole. Electrical properties of egg cells, particularly of mature oocytes, have been studied in different animal groups. They were analyzed before, during and after fertilization or activation, and at the first stages of cleavage (Tyler et al.,'56; Hori, '58; Hiramoto, '59; Maeno, '59; Ito '62; Kanno and Loewenstein, '63; Morrill and Received Aug. 11, '75. Accepted Nov. 10, '75.




Fig. 1 A single desheathed ovariole. At the bottom, a n isolated terminal oocyte (No. 1 ) is separated from t h e rest of the ovariole. The boundaries i n some of the small oocytes are retouched.

Watson, '66; Woodword, '68; Morrill et al., '71; Steinhardt et al., '71; Miyazaki et al., '74; Powers and Tupper, '74). Activation and fertilization were typically accompanied by transient or sustained alterations in some electrical features of the membranes. Kano and Loewenstein ('63) have demonstrated that membrane potential and specific membrane resistance of amphibian oocytes increase with size. If we assume that size is related to the developmental stage it can be concluded that the changes in the electrical properties of the oomembrane were correlated with maturation. The locust's ovariole consists of a longitudinal chain of oocytes at various developmental stages. This characteristic renders it as a good model for investigating several aspects regarding development and specialization of the electrical properties and the relevant ultrastructural aspects of developing oocytes of Locusta migratoria.

males and transferred to a physiological solution devised by Mordue ('69). The ovarioles were carefully separated from the oviduct and the ovariole sheath was easily removed. The "naked" chain of oocyte chambers was used for the electrophysiological measurements (fig. 1). The oocytes were numbered according to their location, starting with the terminal oocyte in which vitellogenesis takes place.

Electrophysiolog y For electrophysiological measurements, an isolated ovariole was stretched between a pair of miniature stainless steel needles in a sylgard bottomed (Dow Corning Co.) lucite petri dish. The terminal oocyte (No. 1) and the terminal filament were used as stretching points. Stretching was essential for successful penetration into oocytes. Glass microelectrodes were filled with 3 M KC1 and had, i n the physiological solution, resistance values from 5 to 20 x 106 ohm. Two to four microelectrodes were MATERIALS AND METHODS used in each experiment. One or two served lnsect material for intracellular current injection and anBreeding stocks of Locusta migratoria other one or two, were used for the recordmigratorioides were kept under crowded ing of membrane potentials. The recording conditions at 28"-3OoC in a constant light electrodes were connected via chlorided regimen. The locusts were supplied daily silver wires to electrometers (Bioelectric with fresh grass and flaked oats. Jars con- &.-model NFI) with negative capacitance taining humid sand were periodically in- feedback. The system was grounded by a troduced into the cages just before the re- chlorided silver electrode immersed in a 3 productive period, to serve as oviposition M KCI pool, which was connected to the sites. experimental bath via a Ringer-agar bridge. A Bioelectric Co. CA5 calibrator was conOuariole preparation nected in series with the recording circuit. Pulses of current, produced by a comOvaries were dissected from mature fe-



bination of Tektronix 161 pulse generator, a 162 waveform generator and a Bioelectric ISA 100 isolation unit passed through a fixed resistor of 10* ohm which was connected in series with the current electrode. The current was measured by monitoring the voltage drop across the 1 0 6 ohm input impedance of an oscilloscope. Signals were monitored on a double beam Tektronix 549 storage oscilloscope and photographed with apolaroid camera. When more than two channels were required, an additional Tektronix 5 0 2 A oscilloscope was used. Penetrations were performed under a Nippon-Kogaku dissecting microscope with a maximum magnification of X 100. The dimensions of individual oocytes were measured with a calibrated ocular micrometer. All experiments were conducted at room temperature.

Electron microscopy Ovarioles were fixed for two hours in Karnovsky’s fixative (Karnovsky, ’65) containing 1% formaldehyde, 3 % distilled glutaraldehyde and 0.45 mM CaClz buffered to pH 7.4 with 0.1 M Sodium cacodylate. In experiments with lanthanum nitrate as a tracer, the technique of Revel and Karnovsky (‘67) was employed. Following fixation, the tissue was postfixed for one hour in 1% osmium tetraoxide stained in block with 0.5% uranyl acetate, dehydrated and embedded in Epon 812. Ultrathin sections were cut with a Reichert ultramicrotome, stained with uranyl acetate and lead citrate and viewed under a JEM lOOB electron microscope. RESULTS

Membrane potential Two abrupt potential changes could be recorded when oocytes were penetrated by a microelectrode. The first change signalled the penetration through the follicular layer and showed a range of 3-12 mV. The second change appeared when the oocyte wall itself was impaled. In the latter case, potential values ranged from 15 to 40 mV. In both cases the inside was negative with respect to the external grounded medium. Sometimes, particularly in the smaller oocytes, stabilization of the potential was reached only several minutes after pene-

lot 1















N o . of Cell Fig. 2 Membrane potential of oocytes as a function of their relative location along the ovariole. The oocytes are numbered according to their location, starting with the terminal oocyte which is the most developed one. Each curve is based on values recorded from a single ovariole. Each ovariole was taken from a different female.

tration. This phenomenon may be attributed to the temporary damage caused by the penetration of the microelectrode. The recording electrode could remain within an oocyte for several hours, with no significant change in the potential. No morphological damage to the cells could be observed. Figure 2 illustrates potential measurements in four ovarioles from four different females. It can be seen that there was an increase in the total potential difference (oocyte membrane follicular layer) 1 as the recording electrode was moved along the ovariole from the distal towards the proximal region, where more mature oocytes are found. Figure 3 is a plot of membrane potential vs. size of oocytes from different ovarioles. These pooled data demonstrate


1 For convenience, this potential will be, hereafter, referred to as “membrane potential.”







t 0

.. .. . . ... ..... . .=










Length of Oocyte (rnrn.) Fig. 3 Membrane potential of oocytes as a function of their size. The points represent com bined data from different ovarioles and from different females.

fore, the obtained values represent the combined values for both. The existence of electrical coupling between oocytes (see next section) introduced another limitation to our measurements. Yet, following the standard terminology for electrically coupled neurons (c.f. Bennett, ’SS), we used the term input resistance (Rin) for the ratio of steady state potential change to the applied current. Current-voltage (I-V) relations of different oocytes were obtained by measuring the potential change at steady state as a response to square pulses of current of different strengths. The current and recording electrodes were inserted into the oocyte 15-20 pm apart. Within the range of currents used, the I-V relations for all oocytes analyzed were linear for inward current. Resistance For outward current, however, most oocytes The membrane of an oocyte and the revealed some rectification (fig. 4). The follicular cells are tightly connected. We potential change following the “make” and could not separate them for the determin- the “break” of the current step were usualation of current-voltage relations. There- ly symmetrical. However, in several cases,

a correlation between the size or maturation of oocytes and the membrane potential. The latter reached a maximum value before completion of oocyte maturation. The scatter can be attributed to variability of the experimental material. The following findings argue against a possibility that low membrane potentials recorded in smaller cells were due to irreversible damage which might have occurred during penetration into the young oocytes: (1) membrane potential was maintained for a long period after stabilization, even in the very small oocytes; (2) the kind of correlation between input resistance and size of oocytes (see next section); and ( 3 ) the intermediate values of membrane potentials observed in intermediate size oocytes.




P .

2olf l 10



30 I (nA

-1 0

-2 0


Fig. 4 Current-voltage relations in four different oocytes. Abscissae: Total membrane current. Ordinate: Steady state potential changes i n response to hyperpolarizing (downwards) and depolarizing current steps. Note the rectification to outward current in three of the oocytes.

the fall of the transmembrane potential change on turning off an hyperpolarizing step of current was steeper than the rise of that potential change, and was followed by a transient overshoot of depolarization (fig. 5). The amplitude of that overshoot was correlated with the degree of hyperpolarization. We have not studied this overshoot in detail, and we could not find any obvious correlation between it and other electrical or morphological properties. However, from our preliminary observations it seems that it tends to occur more frequently in oocytes located i n the proximal side of the ovariole, namely, in the more mature oocytes. As expected, input resistance was correlated with size of the oocyte (fig. 6A). We could not estimate the specific electrical constants using the conventional equations, because of the electrical coupling and the geometry of the ovariole. We tried two

models in order to find whether there was any correlation between specific membrane resistance (R,) and the stage of development of oocytes. Figure 6 B is a plot of R i n versus l/s ( s , surface area of the oocyte) based on the assumption that the preparation behaves as a n equipotential sphere. The slope of the graph would be a measure of Rm. The points fall along two straight lines, suggesting an increase in Rm as oocytes mature. Figure 6C is a plot of R i n versus I / p (p = radius of oocyte) assuming that the preparation behaves as a n infinite cable. The slope here is a measure of R m X Ri (Ri = specific resistance across one cm cube of cytoplasm). The points fall as in the previous case along two straight lines. This suggests that as oocytes develop, an increase in Rm or i n Ri or in both occurs.

Electrotonic coupling Application of square pulses of constant



current to one oocyte, caused electrotonic changes of membrane potential in its adjacent neighbors. The coupling coefficients, namely the ratio of the steady state potential changes produced in the nondirectly




r r



Fig. 5 Steady state potential changes i n two oocytes (both No. 6), taken from two different females, to hyperpolarizing current steps. A comparison between a n oocyte which reveals a transient depolarization overshoot on turning off the current step (A), and a n oocyte which does not reveal that phenomenon (B). Calibration pulse: 10 mV and 20 nA for A; 20 mV and 15 n A for B. Time scale (below calibration pulse in A): 100 msec.

polarized oocyte (V,) to that found in the directly polarized oocyte (V,), were dependent of the current direction (fig. 7). V2IV1 values for distal-proximal direction ranged from 0.70 to 0.92, while in the opposite direction the range was 0.85 to nearly 1.0. The asymmetry in the coupling coefficients may result from higher input resistance of oocytes located more distally. However, i t may reflect also some rectifying properties of the junctional membranes. Figure 8 illustrates current-voltage relations for two coupled oocytes. In this example, current was injected into cell No. 3 and the voltage changes were recorded simultaneously in oocytes 3 and 2. The input resistance for cell No. 3 was, in this case, 0.6 X 1 0 6 ohm, and the transfer resistance was 0.44 X 106 ohm. Curves of similar shapes, though different in input and transfer resistances, were typical €or all the couples analyzed. Rectification to outward current, whenever it occurred in the polarized oocyte, was also reflected in the coupled one. It became evident that all the oocytes which are arranged along a single ovariole are electrically coupled. A voltage change produced in one oocyte induced potential changes in all other oocytes. Attenuation of voltage as a function of distance was, therefore, expected. In order to determine this


l B





0.8 1.2 Length tmm)






1 0


Fig. 6 Input resistance (Rin) of oocytes as function of size. The points represent combined data from different ovarioles and different females. A. Rin versus length of oocytes. B. Rin versus 1/S. S, surface area of oocyte (for the calculation of S , oocytes are considered as 1 p 3 p , radius of cylinders). Based on the model for a n equipotential sphere. C. Rin vs. oocyte. Based on the model for a n infinite cable.




Fig. 7 A simultaneous recording of steady state potential changes in oocyte No. 5 (upwards deflection) and oocyte No. 4 (downwards deflection) to a n hyperpolarizing step of current (40 nA). A. Current is applied to oocyte No. 5. B. Current applied to oocyte No. 4. Coupling coefficient for A is 0.77 and for B, 0.93. Calibration pulse 20 mV.


V h v ) ,cl


attenuation, square pulses of constant current were applied at a fixed position in one oocyte, and the potential changes in other oocytes were recorded with a roving electrode at different distances from the injected oocyte. At the same time, potential changes were recorded with a second electrode close to the current electrode. Attenuation of voltage as a function of distance (x) where Vo was the was defined as potential change at the site of current injection, and Vx the potential change at a distance X from the current electrode. Complete ovarioles could not be analyzed since cells were often damaged by unsuccessful penetrations. To minimize damage and to analyze the longest possible fractions of ovarioles, oocytes were penetrated only at one site, usually close to the nucleus. Ten such fractions from six females were analyzed. The results of three such experiments are illustrated in figure 9. Data of one experiment (ovariole C) are shown in detail. cell # 3



Fig. 8 Input &..J transfer resistances for electrotonic coupling of two adjacent oocytes. Hyperpolarizing and depolarizing steps of current are applied to oocyte No. 3, and potential changes are recorded simultaneously in oocytes Nos. 3 and 2. Abscissae: current applied. Ordinate: potential changes. Outward current and depolarization are positive.




vx ___ vo









I 3.6


X (rnrn) A

u 15 10 I3








Fig. 9 Attenuation of membrane potential changes along a chain of oocytes. Hyperpolarizing current steps are applied to the most distal oocyte i n the chain (0 o n the abscissae) and the electrotonic potential changes are recorded with a roving electrode at different distances (abscissae) from the current source (Vx), and close to the current electrode (Vo). Attenuation 3 vo is represented on a logarithmic ordinate. A, B and C: attenuation along three different fractions of three different ovarioles, which are represented schematically at the bottom of the graph. The two extreme oocytes in each fraction of ovariole are labeled by numbers based on their relative location along the ovariole. Right inset: samples of potential changes along ovariole C. The most upper oocyte is No. 7. The lowest one is No. 2 . Figures under the potential record indicate the number of polarized oocyte (first figure) and the number of oocyte where the potential was recorded (second figure). Calibration pulse: 20 mV. Time scale: 100 msec. Total current step: 20nA.

It is evident that attenuation of voltage as a function of distance cannot be expressed by a single exponential function. Such a function would be expected if the ovariole behaves as a cable conductor with a continuous ooplasmic core, bounded by a homogeneous insulating sheath, and having a uniform diameter. Instead, the slope versus X is steeper i n the plot of In towards the distal side of the analyzed fraction. A similar result was obtained when comparison was made between different fractions: The more distal the fraction was, the steeper were its slopes (figs. 9 A , B,C). Electron microscopy A typical contact between two adjacent

oocytes (Nos. 10-11) is shown in figure 10. A single layer of follicular cells was found to cover the oocytes, whereas several layers of follicular cells were found in the contact region itself. This type of contact between adjacent oocytes was found along the entire ovariole. Figure 10a is a low magnification electron micrograph of the contact region between two oocytes indicating the complexity of membranes in this region. Two types of cell junctions were observed by using lanthanum as a tracer. One which was at least partially impermeable to the tracer, was found between the follicular cells facing the basement membrane (figs. 11a,b). The second was permeable to lanthanum and possessed a periodic substructure with a gap of about 30 A



Fig. 10 a. An Epon section (1 fi thick) of the contact region between two oocytes (No. 10-11) stained with toluidine blue. Note the single layer of follicular cells which cover each oocyte (small arrow) and the several layers of cells in the contact region (large arrow). 0, oocyte. X 500. b. A n electron micrograph of the contact region between two adjacent oocytes (0). Note the number of follicular cells (F) and the n u m b e r of membrane folds between the two oocytes. X 4800.

between the two opposing membranes (fig. l l c ) . Such junctions, which could easily be identified as gap junctions, were found between the follicular cells as well as between the follicular cells and oocytes.


It was demonstrated that the membrane potentials in the developing oocytes of h c u s t a migratoria increase as the oocytes mature. Similar observations were described



Figure 1 1


for oocytes of various amphibians (Maeno, '59; Kanno and Loewenstein, '63). The change in membrane potential as oocytes mature may be caused by one or more of several factors: (1) a redistribution of ions; (2) a change in perm-selectivity; (3) the action of an electrogenic pump. The membrane potential reached its maximum value before the oocytes reached their full size and before yolk deposition took place. Maeno ('59) and Kanno and Loewenstein ('63) have also demonstrated that the specific membrane resistance in amphibian oocytes increases with development. Because of the electrical coupling between the oocytes and the geometry of the ovariole, we could not determine the specific membrane resistance in our material. However, by applying the conventional equations for a n equipotential sphere and for an infinite cable, an increase in Rm as oocytes mature was suggested. It should be mentioned in this regard, that the change was quite abrupt and occurred in oocytes 4 to 7, where the membrane potential reached a plateau and where the elasticity of the membrane was the highest. Oocytes at this stage appeared less transparent and contained whitish globules. The nucleus in such oocytes was at the proximal end of the cell. It seems likely, therefore, that at this region of the ovarioles some maturation processes still proceed, while some electrical properties of the membrane have already been established. Current-voltage relations showed a rectification to outward currents, yet they were linear for inward currents. Egg cells of different animal species, mainly from aquatic environments have linear current-voltage


relations (Tyler et al., '56; Maeno, '59; Hiramoto, '59; Kanno and Loewenstein, '63; It0 and Hori, '66). Miyazaki et al. ('74), who used routinely a single microelectrode for current injection and for potential recordings, have shown that in the Tunicate eggs these relations show rectifications both for inward and outward currents. They suggest two possible alternative explanations for the discrepancy between their results and those of others: (1) a difference between species; or (2) differences in measuring techniques. From their experience the common use of two intracellular electrodes, one for current and the other for voltage, tend to make the current-voltage relations more linear than a single electrode. Our data support the first alternative, since in our measurements we used routinely two intracellular electrodes, and yet observed obvious rectification. Transient changes in membrane potentials, manifesting some excitable properties, were reported for different egg cells upon activation and fertilization (e.g. Ito, '62; Steinhardt et al., '71; Morrill et al., '71). Recently, it was shown that the membrane of unfertilized egg cells of several aquatic invertebrates may also be excitable (Miyazaki et al., '74, '75). The membrane of the locust oocyte was not clearly excited at any current applied. Yet the fast decay of the transmembrane potential change and the transient overshoot which occurred in several cases, upon turning off an hyperpolarizing step of current, indicate that it may possess some excitable properties. The question whether the mechanism responsible for this phenomenon is characteristic to the oocyte only, or whether it is somehow related to the excitable properties of differentiated excitable tissues remains Fig. 11 Preparations (a, b, c) were treated with unsolved. lanthanum nitrate as a tracer. a. A contact region The corpora allata hormone (Juvenile between three follicular cells (F) of the single layer which cover each oocyte. Electron density of the hormone-JH) was implicated in the process tracer can be observed between the follicular cells. of vitellogenesis of many insects, includThe intercellular space between the follicular cells ing the locust (Highnam, '64; Wigglesworth, beyond the arrows and toward the basement mem'64; Telfer, '65; Minks, '67; Engelmann, brane is partially impermeable to lanthanum. X 42,500. h. A high magnification of the lanthanum '70). Transplantation of several active corimpermeable junction seen in a. Note the disappora allata glands in a mature Locusta pearance of the tracer beyond the junction marked migratoria female resulted in significant by arrow. B, basement membrane. X 225,000. c. A yolk deposition in the penultimate oocytes lanthanum nitrate permeable junction between two follicular cells in the region of contact between ad- (E. Wajc, personal communication). The jacent oocytes. The normal intercellular space is oocytes have probably acquired the potenreduced to a gap about 3 0 4 0 A wide, which possess tial to selectively absorb vitellogenins, but a periodic substructure indicating a gap junction being less sensitive than the terminal (between the two arrows). X 250,000.



oocytes, required higher levels of the hormone. One may speculate that oocytes in the process of development along the ovariole, become gradually capable of absorbing hemolymph proteins. This process might be related to changes in membrane potential, in specific membrane resistance or in membranal consistency. In our experiments we used females in their reproductive period, where the target organs have already been exposed to JH. It would be interesting to determine whether maturation of oocytes in terms of electrical properties of the membrane are affected or modulated by JH. Studies on allatectomized females and on very young females in which the endogenous hormone has not yet been released, are in progress in this laboratory. Baumann ('68) provided some evidence suggesting that J H affects the electrical properties of insect cells. He demonstrated that exposure of Galleria mellonella salivary gland cells to this hormone raised the conductivity of the membrane, and strongly depolarized it. Our electron-microscopy studies indicate the existence of junctions, that are partially impermeable to lanthanum, between the follicular cells facing the basement membrane. Gap junctions were found between the follicular cells which separate adjacent oocytes, and between these follicular cells and the oocytes. These lanthanum-impermeable junctions are probably septate junctions known to coexist in invertebrates, together with gap junctions (Hudspeth and Revel, '71). Gap junctions, and possibly septate junctions, are generally considered to participate in intercellular interactions such as electrotonic coupling (Hudspeth and Revel, '71; Azarnia, '74; Gilula, '74). It seems likely, therefore, that the electrotonic coupling found between adjacent oocytes is mediated by these junctions. At present, no clear function for such interaction can be proposed. It may be related to the movement of inorganic ions, of nutrients, metabolites or other low weight molecules (Furshpan and Potter, '68; Loewenstein, '72). Such substances may play an important role in regulating the growth of the oocytes in the ovaries. Woodruff and Telfer ('73) revealed an electrophoretic movement of macromole-

cules along the voltage gradient between nurse cells and oocytes in egg chambers of the Cecropia moth. We have shown the existence of a voltage gradient along the panoistic ovariole of the locust. However, so far, we have no data which might support a similar mechanism. LITERATURE CITED Azarnia, R., W. J . Larsen and W. R. Loewenstein 1974 The membrane junctions i n communicating and noncommunicating cells. Their hybrids and segregants. Proc. Nat. Acad. Sci., 71: 880884. Baumann, G. 1968 Zur wirkung des Juvenilhormons: Elektrophysiologische Messungen a n der Zellmembran der Speichel Druse von Galleria mellonella. J . Insect. Physiol., 14: 14591476. Bennett, M. V. L. 1966 Physiology of electrotonic junctions. Ann. N.Y. Acad. Sci., 137: 509539. Engelmann, F. 1970 The Physiology of Insect Reproduction. Pergamon Press, Oxford. Furshpan, E. J., and D. Potter 1968 Low-resistance junctions between cells in embroys and tissue culture. I n : Current Topics in Developmental Biology. Vol. 3 A. A. Moscona and A. Monroy, eds. Academic Press, New York, pp. 95-127. Gilula, N. B. 1974 Junctions between cells. In: Cell Communications. R. P. Cox ed. J. Wiley & Sons, New York, pp. 1-29. Highnam, K. C. 1964 Endocrine relationships in insect reproduction. Symp. R. Ent. SOC. London, 2: 2 6 4 2 . Hiramoto, Y. 1959 Electrical properties of Echinoderm eggs. Embryologia, 4: 219-235. Hori, R. 1958 On the membrane potential of the unfertilized egg of the medaka, Oryzias Zatipes, and changes accompanying activation. Embryologia, 4: 79-91. Hudspeth, A . J., and J. P. Revel 1971 Coexistence of gap and septate junctions i n a n invertebrate epithelium. J . Cell Biol., 5 0 : 92-101. Imms, A. D. 1964 A General Textbook of Entomology. Methuen and Co. Ltd., London. Ito, S. 1962 Resting potential and activation potential of Oryzias eggs. 11. Changes of membrane potential and resistance during fertilization. Embryologia, 7:47-55. Ito, S., and N. Hori 1966 Electrical characteristics of Triturus egg cells during cleavage. J. Gen. Physiol., 49: 1019-1027. Kanno, Y., and W. R. Loewenstein 1963 A study of the nucleus and cell membranes of oocytes with intracellular electrode. Ekptl. Cell Res., 31 : 149-166. Karnovsky, M . J. 1965 A formaldehyde-glutaraldehyde fixative of high osmolarity for use i n electron microscopy. J. Cell Biol., 27: 137 A (abstract). Loewenstein, W. R. 1972 Transport through membrane junctions. In: Molecular Basis of Biological Transport. J. F. Woessner and F. Huijing, eds., Academic Press, New York, pp. 85-98. Maeno, T. 1959 Electrical characteristics and

ELECTRICAL PROPERTIES OF DEVELOPING OOCYTES activation potential of Bufo eggs. J. Gen. Physiol., 43: 139-157. Minks, A. K. 1967 Biochemical aspects of juvenile hormone action in the adult Locusta migratoria. Arch. Neerl. Zool., 17: 175-258. Miyazaki, S. I., H. Ohmori and S. Sasaki 1975 Action potential and non-linear current-voltage relation in starfish oocytes. J. Physiol., 241 : 3754. Miyazaki, S. I., K. Takahashi and K. Tsuda 1974 Electrical excitability i n the egg cell membrane of the Tunicate. J. Physiol., 238: 37-54. Mordue, W. 1969 Hormonal control of malpighian tube and rectal function in the desert locust Schistocerca gregai-ia. J. Insect Physiol., 15 :273-285. Morrill, G. A., A. B. Kostellow and J. B. Murphy 1971 Sequential forms of ATPase activity correlated with changes i n cation binding and membrane potential from meiosis to first cleavage in R a n a pipiens. Exptl. Cell Res., 66: 281-298. Morrill, G. A,, and D. E. Watson 1966 Transmembrane electropotential changesin Amphibian eggs at ovulation, activation and first cleavage. J. Cell Physiol., 67: 85-92. Powers, R. O., and J. T. Tupper 1974 Some


electrophysiological and permeability properties of the mouse egg. Dev. Biol., 38: 320-331. Revel, J. P., and M. J. Karnovsky 1967 Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol., 33: c.7. Steinhardt, R. A., L. Lundin and D. Mazia 1971 Bioelectric responses of the echinoderm egg to fertilization. Proc. Nat. Acad. Sci., 68(10): 24262430. Telfer, W. H. 1965 The mechanism and control of yolk deposition. Ann. Rev. Entomol., 10: 161-184. Tyler, A., A. Monroy, C. Y. Kao and H. Grundfest 1956 Membrane potentials and resistance of the starfish egg before and after fertilization. Biol. Bull., 1 1 1 : 153-177. Wigglesworth, V. B. 1964 Hormones i n growth and reproduction. Adv. Insect Physiol., 1 : 247336. Woodruff, R. I., and W. H. Telfer 1973 Polarized intracellular bridges i n ovarian follicles of the Cecropia moth. J. Cell Biol., 58: 172-188. Woodword, D. J. 1968 Electrical signs of new membrane production during cleavage of Rana p i p i e n s eggs. J. Gen. Physiol., 52: 509-520.

Electrical properties of developing oocytes of the migratory locust, Locusta migratoria.

The electrical properties of developing nonfertilized oocytes of Locusta migratoria were studied, using intracellular microelectrodes. The inseries po...
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