First published online February 29, 2008
Journal of Experimental Biology 211, 921-934 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014175
Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation
Roland Pusch1,
Gerhard von der Emde1,
Michael Hollmann1,
Joao Bacelo2,
Sabine Nöbel1,
Kirsty Grant2 and
Jacob Engelmann1,*
1 University of Bonn, Institute of Zoology, Department Neuroethology/Sensory
Ecology, Endenicher Allee 11-13, 43115 Bonn, Germany
2 UNIC, CNRS, 1 Avenue de la Terrasse, 91190 Gif-sur-Yvette, France
View larger version (19K):
[in this window]
[in a new window]
|
Fig. 1. Explanation of the recording procedure for the vectorial components of the
local electric organ discharges (LEOD). (A) An example of the three local
electric organ discharges recorded at a position of 50% of the body length.
For each orthogonal axis the single LEOD is shown. (B) Each LEOD was recorded
using a specialised probe (c.f. text) in the medial plane of the fish
(depicted by the black arrow). (C) The time difference of the LEOD in the
dorsoventral and rostrocaudal direction (indicated by the black bar in A)
results in a vector loop when both LEODs are plotted against each other (data
are given in V cm–1).
|
|
View larger version (39K):
[in this window]
[in a new window]
|
Fig. 2. Example of the LEOD measurements obtained from a single fish. All data
shown are averages of 15 consecutive measurements. The position relative to
the length of the fish is given in the topmost row; the LEOD components (z and
y) are shown in the second row. The field vector trajectory of the z
and y LEOD is depicted in blue in the third row. At the 50% position,
the direction of rotation of the vector loop is shown as an example. Note that
the LEODs at the nasal region and the Schnauzenorgan (SO) are highly in phase,
which can also be seen in the individual field components of the z
and y data shown in black and orange in the second row. The fourth
row shows the field module of all three LEODs. In the bottom row, the field
vector calculated at the peak of the field module is shown, i.e. the vectors
represent the effective stimulus strength and direction. Here, black arrows
indicate the vectors as determined relative to the x, y and
z plane. Orange arrows are identical to the black vectors, except
that their angle is given with respect to the sensory surface of the fish. The
drawing of the fish is aligned to match the relative body positions where
measurements were taken. Note that the electric organ is situated in the
caudal peduncle before the tail fin. Each dot in the drawing indicates the
location of an individual mormyromast, showing that the density is highest at
the Schnauzenorgan.
|
|
View larger version (24K):
[in this window]
[in a new window]
|
Fig. 3. (A) The peak-to-peak values for all measured positions of the rostrocaudal
(orange trace) and dorsoventral (black trace) EOD components. At the trunk of
the fish, the dorsoventral component is prominent but at the Schnauzenorgan
the rostrocaudal component dominates. In the head region only, both components
are similar in their contribution to the LEOD. Note that the fish's constantly
open mouth leads to an increase in the amplitude of both components at the
head region (black arrow). (B) Plot of the peak-to-peak values in the
different body regions. The z component is plotted versus
the y component of the LEOD. Note that at the head region (red dots)
the influence of both components is similar.
|
|
View larger version (24K):
[in this window]
[in a new window]
|
Fig. 4. Colour-coded peak-to-peak distribution of the LEOD amplitude at the head as
measured with a single electrode referenced against the internal tissue. Note
that the EOD amplitude is fairly constant over the nasal region and only
changes further caudally.
|
|
View larger version (11K):
[in this window]
[in a new window]
|
Fig. 5. Effect of movement of the Schnauzenorgan (SO) on the amplitude of
LEODy (light grey bars) and LEODz (dark grey bars). Dots
represent the electrode positions. In position I, mean amplitudes
(N=7) normalised to the peak-to-peak amplitude of the
LEODz are shown, measured at the tip of the Schnauzenorgan in a
normal position. At II, the Schnauzenorgan was bent to the left by
62±13.5° whereas the LEODs were recorded at the same site as in I.
The initial amplitudes could be recovered by readjusting the recording
position to the new tip-position (III), while a subsequent return of the
Schnauzenorgan to its normal position without moving the recording electrodes
decreased the amplitudes again (IV).
|
|
View larger version (23K):
[in this window]
[in a new window]
|
Fig. 6. The `tip-effect' on the amplitude of LEODy (light grey bars) and
LEODz (dark grey bars) as a function of distance. The distance
between the Schnauzenorgan and the recording electrode was varied from less
than 1 mm to 5 mm. (A) The Schnauzenorgan is in its normal position and the
probe (black dot) is in front of the tip. (B) The Schnauzenorgan is in its
normal position and the probe is positioned left of the tip. (C,D) The same
probe conditions as in the top row but with the Schnauzenorgan bent to the
side (depicted in red) (cf. Fig.
5).
|
|
View larger version (38K):
[in this window]
[in a new window]
|
Fig. 7. (A) The voltage distribution (peak-to-peak amplitude of the LEOD) on the
skin, measured in the presence (red squares) and absence (blue squares) of a
metal cube. Each symbol represents the average of ten LEODs. The abscissa
shows the plane where the voltages were measured along the fish at the left
and right side of the mouth, with 0 indicating the position of the mouth. Note
the relatively stable voltage distribution in the range from –15 to +15
mm (the arrows indicate the distortions caused by the nostrils). (B) The
resulting voltage difference caused by the presence of the metal cube. (C) The
modulation of the voltage due to the presence of the object. (D) Normalised
modulation (maximum set to 1), which was used to calculate the slope of the
electric images. In B and C, values are means ± s.d.
(N=10).
|
|
View larger version (81K):
[in this window]
[in a new window]
|
Fig. 8. Three-dimensional comparison of the electric images of different objects,
with the modulation caused by the object colour coded. (A) The electric image
of a metal cube. (B) The electric image of a plastic cube. (C) The electric
image of a metal sphere. (D) The electric image of a plastic sphere. Note that
high modulation values are shown in red and low modulation values are shown in
blue. Therefore, the baseline for conductive objects (metal) is shown in blue
and the baseline for non-conductive objects (plastic) in red.
|
|
View larger version (27K):
[in this window]
[in a new window]
|
Fig. 9. Comparison of the electric images of different objects. (A) Modulation of
metal cubes (red squares) and metal spheres (blue circles) in the horizontal
plane. Each point represents the mean of three measurements. (B) The same
comparison in the medial plane. (C) Comparison of the modulation resulting
from a plastic cube (red squares) and a plastic sphere (blue circles). (D) The
same comparison in the medial plane.
|
|
View larger version (21K):
[in this window]
[in a new window]
|
Fig. 10. (A) LEOD amplitudes (LEODy) measured along the midline of the
fish in the presence (orange line) or absence (black line) of a metal cube
placed in front of the animals mouth at the same distance as in the other
experiments (distance to skin, 0.25 cm). (B) Colour-coded voltage modulations
plotted along the midline of a fish, from the tip of the Schnauzenorgan to the
head. Modulations <1 (a decrease in voltage caused by the object) are drawn
in dark blue and were found only at the Schnauzenorgan. The modulation caused
by the object changes at the snout of the animal. At the nasal region,
voltages are increased, which cause modulation values >1 (depicted in
red).
|
|
View larger version (6K):
[in this window]
[in a new window]
|
Fig. 11. (A) Mean count of mormyromasts (N=20) in successive bins each
representing 10% of the total length of the Schnauzenorgan (SO), showing s.d.
only in the positive direction. (B) Mean density of mormyromasts
(N=3) for different body regions. Note that the nasal region (NR)
contains the second highest density of mormyromasts. Differences in densities
were tested with the Student–Newman–Keuls post-hoc test:
**P<0.001.
|
|
View larger version (10K):
[in this window]
[in a new window]
|
Fig. 13. Schematic illustrations of the ambiguity of the slope of electric images at
different body regions. (A) A cube opposite a flat sensory surface. The
distance between the object and the sensory surface is constant. The resulting
electric image is bell-shaped and the slope is steep (depicted by the red line
intersecting the horizontal line to indicate the angles). (B) A spherical
object opposite a flat sensory surface. The edges of the object are farther
away than the middle of the object. Therefore the slope of the electric image
is less steep. (C) A cube opposite a curved sensory surface. The edges of the
object are farther away than the middle of the object. Compared to the trunk
the slope is less. (D) A spherical object facing a curved sensory surface. As
the distance between the edges of the object and the sensory surface is
greater than for the flat surface (B) the slope is steeper.
|
|
© The Company of Biologists Ltd 2008
of the novelty response. A dipole object of variable resistance was suddenly
switched from a high to a low resistance or vice versa. The EOD
frequency was monitored in response to the switch (see arrow). Several trials
with identical switches and identical positioning of the dipole objects were
normalised (normalised 
) by subtracting the mean frequency and dividing
by the variation of the 20 EODs prior to a switch. Note that negative values
in the normalised data correspond to an acceleration of EOD frequency and that
this measure is transformed to positive values in B. (B) Mean response
magnitude (determined in four fish, based on 64 switches at each position) for
a switch occurring at the indicated positions along the fish at a distance of
3 mm from the skin. Note that the response was maximal for a dipole positioned
at the tip of the Schnauzenorgan. NS, not significant.