2 Electric organs (1)

Prévia do material em texto

The Origin of Electric Organs of 
Electrophorus electricus ' 
THOMAS SZABO 
Brain Research Institute, Depmtment of Anatomy and Department of 
Zoology, University o f California at Los Angeles 
ABSTRACT The electric organs (main, Sachs' and Hunter's) of a 23 cm and a 
38 cm long Electrophorus electricus were studied by histological methods. The results 
were compared with 12 cm (Keynes, '61) and 140 cm (Couceiro and Ackermann, '48) 
specimens. Al l three electric organs originate from striated muscle fiber as indicated 
by the presence of a striated structure in the undeveloped electroplates. The three 
organs do not develop simultaneously but in succession: first Sachs' organ, then the 
main organ and finally Hunter's organ, with considerable overlap in time. In all three 
cases, the anterior extremity of the organ develops last. The classical notion that the 
main organ originates from the lateralis i m u s muscle is not supported by the present 
findings. 
Several histological studies have shown 
that electroplates, the elementary units of 
electric organs in fish, originate from mus- 
cle tissue. In Torpedo (Ogneff, 1897) and 
in Astroscopus (White, '18) the electro- 
plates develop from myoblasts, whereas 
in Raja (Engelmann, 1894), in Gym- 
narchus (Dahlgren, '14) and in mormyrids 
(Szabo, '60) they develop from already 
well formed striated muscle fibers. Little 
is known about electric organ develop- 
ment of Malapterurus (Johnels, '56) and 
of gymnotids (Keynes, '61) because of the 
difficulty in procuring embryonic material 
due to our ignorance of the breeding habits 
of these species. 
During an expedition to the Amazon 
river in 1964 we had the good fortune to 
obtain two small specimens of Electro- 
phorus electricus of 23 and 38 cm in 
length. Although the specimens were of 
relatively large size, their electric organs 
had not yet fully developed. Observations 
concerning these organs will be presented 
in the paper. 
MATERIAL AND METHODS 
Two young Electrophorus electricus 
originating from the Amazon delta region 
(Marajo, State Para) have been used. Both 
showed normal electric activity - spon- 
taneous low voltage activity and high volt- 
age discharges evoked by touch (Hagi- 
wara, Szabo and Enger, ' 6 5 ) . 
The 23 cm long fish was fixed in Helly's 
solution, the 38 cm long one in 10% for- 
ANAT. REC., 155: 103-110. 
malin. From the former we took four 
slices and from the latter two slices, each 
5 mm thick obtained from different levels 
of the longitudinal axis of the fish (fig. 1). 
The slices were embedded in paraffin, 
cut in serial sections, partly in transverse, 
partly in sagittal plane. Mallory's triple 
stain and Bodian's protargol silver impreg- 
nation were used. 
Only critical levels will be described, 
since the structure of complete transverse 
sections does not vary significantly centi- 
meter by centimeter along the longitudinal 
axis. In order to compare equivalent levels 
in fish of different length, the ratio of a 
given level to the total length of the fish 
was used as an index of position. 
Couceiro and Ackermann's ('48) find- 
ings on a 140 cm full grown specimen and 
Keynes ('63 ) observations on a 12 cm elec- 
tric eel were compared with our results. 
RESULTS 
General. Ekctrophorus has three pairs 
of electric organs (Hunter, 1775; Sachs', 
1877): the main organ ( M ) extends cau- 
dally from the abdominal cavity along two- 
thirds of the fish (it surrounds partially 
the caudal end of the liver); the organ of 
Sachs' ( S ) extends caudally from the main 
organ, beyond the latter to the tip of the 
1 Supported in part by grants to Drs. S. Hagiwara. 
L. Kruger and T. H. Bullock from the U. S. Air Force, 
National Institute of Health Office of Naval Research 
and National Science Founhation. 
2 On leave from the Centre $Etudes de Physiologie 
Nerveuse, C.N.R.S., 4, av. Gordon Bennett, Paris, 16e, 
France. 
103 
104 THOMAS SZABO 
MAIN ORGAN 
I SACHS ORGAN 
A '6 
HUNTER'S ORGAN 
Length 
I I I I I I I I I I I I , , I I I I I ',' oFlish 5 10 15 
2 7r (6) I " 4 I 1 2 c m ............... ~~~~~ .... ~ ~~ ~~ ~~~ 
3 
7/3 . ~ ~ . ~ ............................. .... .... ~. ~ ~ 
----..---.----.-. .....~~.....~ --.. . . . ... ~. .... ~ 3ec.1 
5,2 
-... ~~ ................... ~~ .... ~ ~~ .~~ ~ ..... -...@ ~. ... ~~ ...... .......................... ~ ~ . . . ~ ~ . ~ ~ 
(& (3 s i 
Figure 1 
Above: Schematic drawing shows the position of the three electric organs of Electrophorus. 
Below: Number of electroplates at different levels of the 12, 23, 38 and 140 cm long fish. Com- 
parison was made between real levels of the 23 cm and relative levels of the 12, 38 and 140 cm 
long fish. Actual levels are indicated in parenthesis. 
tail. There is some overlap between the 
two organs as shown in figure 1. Hunter's 
organ ( H ) extends for the total length of 
these two organs, lying on the ventral sur- 
face. The three organs consist of a num- 
ber of columns of electric plates oriented 
in the dorso-ventral axis. 
In the 23 cm long fish it 
is obvious that the electric organs con- 
stitute the principal component of the 
transverse sections at the 6 ( A ) , 10 (B) 
and 15 cm (C) levels (fig. 2). However, 
the ratio of electric organjmuscle varies, 
so that electric organ tissue decreases cau- 
dalwards: at level 10 cm this ratio is 2 : l , 
whereas, at 15 cm it is 1.1 : 1, and at the 
level of Sachs organ (level 19 cm), the 
muscle volume is larger than the electric 
organ volume. Exactly the same ratios 
were found in the full grown (140 cm) 
specimen, which suggests parallel growth 
of muscle and electric tissue. 
However, the comparison of ratios of 
horizontal/vertical diameter in transverse 
sections of animals show that the electric 
eel grows more in the horizontal axis than 
in the vertical one. In the 23 cm long ani- 
mal, the horizontal/vertical diameter ra- 
tios are 1 : 1.5 at the anterior level and 1 : 2 
at the posterior level, whereas, for identi- 
cal levels they are 1 : 1 and 1 : 1.5 in the 
full grown animal. 
Main organ. 
If one compares the transverse sections 
of different levels under low magnification, 
an essential difference can be observed in 
the 140 and the 23 cm fish concerning the 
thickness (vertical diameter) of the elec- 
tric plates. In the former, the plates are 
equally thick in the dorsal as well as in 
the ventral region. In the latter, the ven- 
tral plates are much thinner and tightly 
packed than the dorsal ones. These differ- 
ences are particularly well seen in sagittal 
sections of paramedian regions (fig. 3B 
and C) . A comparison of different levels 
in the 23 cm long fish shows the anterior 
ones to have thinner plates than the pos- 
terior ones (compare in fig. 2 the 6 cm 
and 15 cm levels). In the 38 cm long fish 
the ventro-dorsal differences of plate thick- 
ness are already almost insignificant for 
the posterior region (fig. 4B), whereas, 
they are still pronounced in the anterior 
region (fig. 4 A ) . 
The number of electric plates contained 
in one column at different levels in 12, 
23, 38, and 140 cm long specimens is 
shown in figure 1. The plates of one col- 
umn, seem to be more numerous in the 23 
cm than in the 38 cm long fish, which is 
contrary to what might be expected. What- 
ever the reason for this apparent decrease 
may be (comparison of different speci- 
mens for example), it is probable that our 
ELECTRIC ORGAN DEVELOPMENT 105 
Fig. 2 Transverse sections of a 23 cm long Electrophorus electricus at four levels A, B, C and D 
(see fig. 1) of the length axis of the fish. M , main organ; H , Hunter’s organ; S, Sachs’ organ. Bar = 1 mm. 
youngest animal possesses the full num- 
ber of electric plates. 
Histologically the electroplates,i.e., the 
elementary units of electric organ, do not 
show their definitive form and structure 
everywhere. The fully developed electro- 
plate is constituted of thin electroplasm, 
filling only about one-tenth of its connec- 
tive tissue compartment. That is the case 
for the posterior electric organ region of 
our youngest fish (fig. 3C) . The plate has 
finger-like processes on both anterior and 
posterior surfaces. At any given level the 
ventrally located plates are more volumi- 
nous, their dorso-ventral axes smaller, and 
their surfaces have fewer processes. How- 
ever, in neither ventral nor dorsal plates 
does the structure of the electroplasm dif- 
fer significantly in the posterior region of 
the main organ. 
As one advances further anteriorly, the 
histological picture changes progressively 
in the ventral region of individual plates. 
The processes of the plates disappear com- 
pletely and the electroplasm becomes in- 
creasingly structured. Finally at the 10 cm 
level, a clearly defined striation appears 
(fig. 5B), similar to that found in the 
neighboring striated muscle. Tangential 
sections show an enormous accumulation 
of nuclei of electro-(sarco) lemma. 
At the same antero-posterior level the 
striation becomes progressively less pro- 
nounced as one proceeds from the ventro- 
medial to the dorsal region. The electro- 
plasm displays only a partial striation until 
it disappears completely. Figure 5B1 shows 
plates containing only some debris and a 
nearly total loss of striation. Their verti- 
cal axis increases as regions of fully de- 
veloped plates are reached. 
It can be concluded that the striated 
structure in the ventral region of the main 
organ, represents the primitive form of 
electric tissue, which suggests that this 
part of the main organ is the germinative 
region of its electric tissue. 
In the 23 cm speci- 
men the number of plates in a given col- 
umn is complete everywhere in Hunter’s 
organ. As shown in figure 1, the number 
of plates at any antero-posterior level is the 
same as in a full grown fish. However, 
comparison of the 23 cm (fig. 2 ) and 38 
Hunter’s or,gan. 
106 THOMAS SZABO 
Figure 3 
A: Transverse section of the spinal cord at A level. The electro-motor 
cells are situated dorsal to the central canal ( c ) . Notice undeveloped electro- 
motor cells close to the central canal. ‘u.T., ventral root. Bar = 100 p. 
Sagittal section close to the midline showing small electroplates in 
the ventral region of the main eIectric organ M. H , Hunter‘s organ; n, nerve 
trunk, A t P antero-posterior direction. Bar = 1 mm. 
B: 
C : 
D: 
Same as B with higher magnification. Bar = 100 p. 
Sagittal section of Sachs’ organ at level D. Bar = 500 p. 
cm (fig. 4) animals shows that Hunter’s 
organ in the former is at an early stage 
of development. Hunter’s organ is better 
developed in the posterior region (fig. 2D), 
where it lies ventral to Sachs’ organ and 
inserted between the two pinnalis analis 
externalis muscles. In the more anterior 
region, Hunter’s organ represents only a 
small (fig. 2C) or even tiny (fig. 2B) vol- 
ume of electric tissue and in the most an- 
terior region (fig. 2A), the four plates of 
Hunter’s organ can only be seen under 
high magnification. 
At levels B and C, an intermuscular 
space can be observed between t he pin- 
nalis analis externalis and internalis mus- 
cles, into which Hunter’s organ will sup- 
posedly grow. This would provide some 
explanation why no muscular atrophy 
is apparent during organ growth. Hunter’s 
organ enlarges its volume 100 times at 
level C, and 300 times at level B. 
ELECTRIC ORGAN DEVELOPMENT 107 
The foregoing observations suggest that 
the most anterior part of Hunter’s organ 
i s the less developed at this stage. The his- 
tological picture of electroplates supports 
this suggestion. Only ia the anterior part 
of Hunter’s organ (level A and B ) do the 
plates show a striated structure (fig. 5C) 
similar to that found in the ventral region 
of the main organ. These plates are rela- 
tively thick, and the electrolemma displays 
no finger-like processes. At level C, stria- 
tion of the electroplasm has already dis- 
appeared. ‘The electrolemma begins to fold, 
but the electroplasm still remains thick. 
In sagittal sections at C level (fig. 3B) , 
the ventral region shows slightly smaller 
plates than in the dorsal region, indicating 
some evidence for a ventro-dorsal develop- 
ment of Hunter’s organ, similar to that of 
the main organ. 
Sachs’ organ. In the 23 cm fish, sec- 
tions cut transversally at any level of the 
tail region reveal a well developed struc- 
ture characteristic of the full grown ani- 
mal. However, the ventral plates of the 
Sachs’ organ are somewhat thinner (dorso- 
ventral axis), the electroplasm more 
voluminous (antero-posterior axis) and 
the finger-like processes of the plates 
shorter than the dorsal ones. No striation 
can be seen in any of these plates. 
We found, however, in the very anterior 
part of Sachs’ organ, at its ventral border, 
some undeveloped electric tissue. It has 
the appearance of very large muscle fi- 
bers, some part of which is striated (fig. 
SD), and its cell membrane crowded by 
nuclei. This structure, very much like un- 
developed electroplates, is enclosed in the 
general connective tissue envelope of 
Sachs’ organ. These are the only indica- 
tions of the muscular origin of Sachs’ 
organ. 
Fig. 4 Transverse sections of the 38 cm long fish at the middle (A) and posterior (B) 
region of the main organ (M). H , Hunter’s organ. Bar = 1 mm. 
Figure 5 
A: 
€3 and BI: 
C: 
D: 
Transverse section of the 23 cm long fish at A level showing the germinative region 
of the main organ. Bar = 100 p . 
Higher magnification of the regions B and B I indicated in A. 
Undeveloped electroplate of Hunter’s organ at level B indicated in figure 1. 
Undeveloped electroplate of Sachs’ organ (arrow). Ears for E, B1, C and D = 10 P. 
ELECTRIC ORGAN DEVELOPMENT 109 
DISCUSSION 
According to Max Ellis (’13), Fritsch in 
1881 concluded that the main electric or- 
gan of Electrqhorus originated through 
the metamorphosis of the lateralis i m u s 
muscle, because of the “position occupied 
by the large electric organ” (Fritsch com- 
pared gymnotids and Electrophorus). From 
this statement originates the classical no- 
tion that the electric tissue of the electric 
eel is of muscular origin. 
We compared different muscle tissue 
volume ratios in fish of different sizes and 
found that the lateralis imus muscle as 
well as other muscles grow proportionally. 
It is, therefore, unlikely that electric tis- 
sue grows “at the expense of” muscle tis- 
sue. Also, if we compare carefully the 
relative size of the lateralis imus muscle in 
Ekctrophorus and other gymnotids, there 
is no reason to conclude that this muscle 
is only a remnant in Ekctrophorus. How- 
ever, our results do not exclude the possi- 
bility that the electric tissue of the main 
organ originates from that part of meso- 
derm from which the lateralis imus arises. 
We can only say, on the basis of Keynes’ 
(’61) and our results, that the germinative 
region of the electric organ is separated 
from the lateralis imus muscle by the thick 
collagenous envelope of this muscle. 
We have confirmed Keynes’ findings 
(’61), that the germinative region of the 
main organ is the ventral part of this or- 
gan, close to the midline. In contrast, the 
striated structure of undeveloped electro- 
plates of the main, Hunter’s and Sachs’ 
organ indicates that all three electric or- 
gans of Electrophorus originate from 
striated muscle fibers, the structure and 
form of which will fundamentally change 
during development. Consequently the 
electroplatesdo not develop directly from 
myoblasts (cf. Keynes, ’61) but from well 
formed striated muscle fibers, similar to 
Gymnarchus (Dahlgren, ’14), Raja (Engel- 
mann, 1894) and normyrids (Szabo, ’60). 
Wachtel’s (’64) electron microscopical ob- 
servations support this statement. This 
author finds some remnant of muscle tis- 
sue of myofibrillar origin in adult electro- 
plates. 
The course of development of the three 
organs is not simultaneous. It seems prob- 
able that Sachs’ organ develops first, then 
the main organ and finally Hunter’s organ. 
The fact that Keynes (’61) did not find 
Hunter’s organ in the tail region of a 12 cm 
fish, also confirms a successive develop- 
ment of the organs, although a wide over- 
lap in time is certain. Considering the or- 
gans individually, they have a ventro- 
dorsal development, and at an appropriate 
level (A or B level) the successive steps of 
transformation of a striated muscle fiber 
into an electroplate can be followed. The 
posterior part of each organ, containing 
undeveloped electroplates, develops more 
rapidly than the anterior part. This antero- 
posterior temporal difference has also been 
described in Gymnarchus (Dahlgren, ’14) 
where the anterior region of the electric 
organ develops last. However, it is possible 
that the organ differentiation starts in an- 
other region since the rate of differentia- 
tion may not necessarily be the same in all 
parts of the organ (cf. Dahlgren, ’14). 
Our findings also indicate that electric or- 
gan development in Electrophorus is 
largely a post-embryonic one. 
We could not follow the course of inner- 
vation of the organs, because silver im- 
pregnation were not successfuly accom- 
plished in our youngest fish. The fact, 
however, that this fish was producing low 
voltage as well as high voltage impulses 
(Hagiwara, Szabo and Enger, ’ 6 5 ) , indi- 
cates that the innervation was complete at 
least for the fully developed plates. How- 
ever, the presence of undeveloped electro- 
motor cells (fig. 3A) in the spinal cord 
suggests that the germinative region still 
had not received its nerve endings. 
The central command nucleus of the 
electric discharge, situated in the medulla, 
was fully developed, as might be expected 
from results obtained in other electric fish 
(Szabo, ’61 ). 
ACKNOWLEDGMENTS 
The author is indebted to Drs. T. H. 
Bullock and L. Kruger for their helpful 
criticism of the manuscript and to Dr. G. 
Krauthamer €or correcting the English. 
LITERATURE CITED 
Couceiro, A., and M. Ackermann 1948 Sur 
quelques aspects du tissu Blectrique de 1’Elec- 
trophonrs electficus (Linnaeus). Ac. bras. 
Cienc., 20: 383-395. 
110 THOMAS SZABO 
Dahlgren, U. 1914 Origin of the electric tis- 
sue of Gymnamhus nibticus. Dept. Marine 
Biology, Carnegie Institution, Washington. 
Papers from the Tortugas Laboratory, 6 (Publi- 
cations No. 183): 161-194. Ellis, M. 1913 The gymnotid eels of tropical 
America. Memoirs of the Carnegie Museum, 
Engehnann, T. W. 1894 Die Blatterschicht des 
elektrischen Organs von Raja in ihren geneti- 
schen Beziehungen zur quergestreiften Muskel- 
substanz. Pfluger's Arch., 57: 149-180. 
Hagiwara, S., T. Szabo and P. Enger 1965 
Physiological properties of electroreceptors in 
the electzic eel, Electrophorus electricus. J. 
Neurophysiol., 28: 775-783. 
Hunter, J. 1775 An account of the Gymnotus 
electricus. Phil. Trans., 65: 395. 
Johnels, A. G. 1956 On the origin of the elec- 
tric organ in Malapterurus electricus. Quart. J. 
Micr. Sc., 97: 45-64. 
Keynes, R. D. 1961 The development of the 
electric organ in Electrophorus electricus (L). 
NO. 111, 109-195. 
In: Bioelectrogenesis, C. Chagas and A. Paes 
de Carvalho, eds., Elsevier Publ. Co., Amster- 
dam, pp. 14-19. 
Ogneff, J. 1897 Uber die Entwicklung des elek- 
trischen organs bei Torpedo. Arch. f. Anat. 
und Physiol., Physiol. Abt., 270-304. 
Sachs, C. 1877 Beobachtungen und Versuche 
an siidamerikanischen Zitteraale. Arch. f. 
Physiol., 66-95. 
Szabo, T. 1960 Development of the electric or- 
gan of Mormyridae. Nature, 188: 760-762. 1961 Rapports ontog6nCtiques entre 
l'organe blectrique, son innervation et sa com- 
mande endphalique (Mormyrus rume). Zeit- 
schrft. Zellf., 55: 200-203. 
Wachtel, A. W. 1964 The ultrastructural re- 
lationships of electric organs and muscle. I. 
Filamentous systems. J. Morph., 114: 325-360. 
White, E. G. 1918 The origin of the electric 
organs in Astroscopus guttatus. Dept. Marine 
Biology, Carnegie Institution, Washington. 
Papers from the Dept. of Marine Biology, 12 
(Publications No. 252): 139-172.