First published online February 12, 2007
Journal of Experimental Biology 210, 800-814 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000638
Post-natal development of the electromotor system in a pulse gymnotid electric fish
Ana Carolina Pereira1,
Alejo Rodríguez-Cattaneo1,
María E. Castelló1,2 and
Angel A. Caputi1,*
1 Departmento de Neurociencias Integrativas y Computacionales, Instituto de
Investigaciones Biológicas Clemente Estable, Unidad Asociada de la
Facultad de Ciencias, Montevideo, Uruguay
2 Departmento de Histología y Embriología, Facultad de
Medicina, Universidad de la República, Montevideo, Uruguay
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Fig. 1. The electric organ of larval fish. Photomicrographs of coronal sections of
12 mm-long fish impregnated with silver at the abdominal region (A) and the
middle region (B) of the fish body. As shown in A, in the abdominal region,
the electric organ consists of pairs of tubes on each side of the body
midline. A nerve is also evident, cut in cross section, lying at the dorsal
edge between the lateral and medial electrocytes on each side (arrows). Thin
branches innervating the caudal faces of the electrocytes emerge from these
nerves (not shown here), indicating that they correspond to the anterior
electromotor nerves observed in the adult. After the emergence of the anal
fin, the electric organ consists of two sets of four tubes on each side of the
midline (B). Note the dorsal–ventral decrease in the electrocytes'
cross-sectional area. (C) Microphotograph of a semi-thin section of a 12
mm-long fish showing parts of two electrocytes. The striated appearance of the
cytoplasm of one of them indicates its myogenic origin (black and white arrows
point to the clear and dense phases of the stria, respectively). The
periodicity of this striation is similar to that of skeletal muscle (inset),
although it is much fainter.
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Fig. 2. Development of the electric organ (EO) from larval to adult stages. (A)
Area of the fish body occupied by the EO (expressed as a percentage of the
cross-sectional area) as a function of the distance from the jaw (expressed as
a percentage of the fish length). The area of the fish body occupied by the EO
in the rostral half of the fish body is greater in larvae (30 mm) than in
juveniles (65 mm), and the contrary holds for the caudal half of the fish
body. (B) For all studied fish (28, 68 and 185 mm), the density of
electrocytes (expressed as the number of electrocytes per 1% of fish body
length) increases from the rostral to the tail regions.
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Fig. 3. Characteristics of the pacemaker frequency as a function of fish length.
(A) Raster of the first-order intervals emitted by a resting fish of 37 mm
length. Note the regularity of electric organ discharge (EOD) interval,
interrupted by accelerations, followed by slower relaxations up to the basal
EOD interval (arrows). (B) Histogram of the inter-EOD intervals represented in
A. Note the skew of the histogram that results from the accelerations
indicated by the arrows in A. (C) Box plot comparing the individual means of
the EOD intervals exhibited by fish of different lengths. The first category,
fish shorter than 30 mm, discharged their EO at a rate significantly lower
than the others. (D) Box plot comparing the variance of the EOD intervals
exhibited by fish of different lengths. The EOD was significantly more regular
for the two categories above 60 mm. (E) First-order frequency polygon of the
inter-EOD interval normalized to the mean interval obtained from 45 fish
ranging from 12 to 226 mm, showing the constancy of the distribution.
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Fig. 4. Electric organ discharge (EOD) rate as a function of water temperature
comparing larvae and juveniles of different length, gathered in the same day.
Note that in all specimens there is a linear relationship with similar slope
and that the smaller fish have a lower rate.
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Fig. 5. Novelty responses elicited by electrosensory stimuli. (A,B) Mean ±
s.d. (N=10) of the inter-EOD (electric organ discharge) interval
normalized to basal EOD interval (upper dashed line=100%), plotted as a
function of time. The arrows indicate the moment when two wires are short
circuited in front of the fovea. (A) Biphasic larvae exhibit larger and
longer-lasting accelerations than (B) juveniles and adults in response to
changes in reafferent signals. (C) The amplitude of the novelty response
(defined as the maximum shortening of the inter-EOD interval as a percentage
of the basal interval) decreases with fish length. (D) The half relaxation
time (defined as the time in which the interval returns to values equal to
basal minus 50% of the amplitude of the response) also decreases with fish
length.
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Fig. 6. The electric field generated by the electric organ discharge (EOD). (A)
Typical EOD waveforms corresponding to biphasic larval, triphasic larval and
juvenile stages, showing the progressive incorporation of EOD components. (B)
The root mean square value of the EOD associated field (rmsEOD) is a linear
function of the square of the fish length. This relationship holds for larvae,
juveniles and adults, in spite of the differences in EOD waveform. (C) During
the larval and juvenile stages, the frequency at which the power spectrum of
the EOD peaks, increases with fish length.
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Fig. 8. The spatio-temporal pattern of the equivalent electromotive force along
development was studied using the multiple air gap technique [a procedure that
allowed the identification of the generation site of the different waveform
components of the electric organ discharge (EOD)
(Caputi et al., 1993 )]. (A)
The 30 mm fish exhibited a three-phase EOD with a slow early negative
component generated at the abdominal region, a positive component generated
all along the body, and a late negative component generated at the tail
region. (B) The last component to appear (V2) was clearly
identified in the fish of 47 mm length (second trace, arrowhead) and was
completely developed in (C) the juvenile of 68 mm length. Note the progressive
reduction of the EOD duration and the relative increase of the late negative
component (V4).
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Fig. 9. Regional contribution of the fish body to the electromotive force during
development. The contribution of regions corresponding to 1% of the fish
length was estimated by plotting the regional electromotive force normalized
by the length of the fish region in which it is generated (electromotive force
per 1% of fish length) as a function of the position of the center of the
region along the fish body (distance from the jaw expressed as percentage of
fish length). The early negativity shows two components of different spatial
origin and maturation times. In larvae (A,B), the generated electromotive
force is largest at the rostral portions of the generating electric organs and
shows a slow decay as a function of the distance from the jaw. Note that the
peak of the curve moves rostrally as the fish grows (arrows in B). This
coincides with the smooth wave observed in time-based recordings and therefore
should be classified as V1 (light gray box). (C) A second component
appears in juveniles of about 47–52 mm length and (D) is clearly defined
beyond 55 mm of fish length. This component corresponds to the fast component
generated at the center of the fish body, V2 (dark gray box).
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Fig. 10. Further evidence of the different mechanisms of generation of V1
and V2 can be obtained by fish curarization, which blocks
transmission at the neuro-electrocyte junction. The dose was adjusted to be
just enough to stop breathing but not enough to completely block the
discharge. (A) The head-to-tail equivalent electromotive force of a fish in
control (black) and curarized (red) conditions. (B) The spatial profile of the
first negative deflection in control (black) and curarized (red) conditions.
Note the differential effect on V1 and V2; V1
is the less affected component because it is generated by the subthreshold
activation of the rostral membranes of doubly innervated electrocytes.
V4 is absent because the amount of current generated by
V3 is subthreshold for generating an action potential at the
rostral faces of single innervated electrocytes.
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Fig. 11. Development of (A) V3 and (B) V4. To compare the data
from fish of different length (i–iv), we calculated an electrogenic
index: the electromotive force divided by the length (expressed as a
percentage of the fish length) of the generating region. In all fish, there is
a head-to-tail progressive increment of the electrogenic index with percentage
of fish length. Note that both the maximum amplitude and the slope of the
curves of both waveform components increase as fish grow. The increase of the
growth coefficient for V4 is larger than for V3.
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Fig. 12. (A) Schematics of the electrogenic system in the adult fish [modified from
Caputi (Caputi, 1999)]. The
activation of the electric organs (EO) in the biphasic larvae (B), in the
triphasic larvae (C) and in juveniles and adults (D) is indicated in a
schematic based on the adult electrogenic system. Arrows of different colors
indicate the different waveform components that are progressively added in the
course of postnatal development.
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© The Company of Biologists Ltd 2007
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