First published online June 7, 2004
Journal of Experimental Biology 207, 2443-2453 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01053
Pre-receptor profile of sensory images and primary afferent neuronal representation in the mormyrid electrosensory system
Leonel Gómez1,
Ruben Budelli1,
Kirsty Grant2 and
Angel A. Caputi3,*
1 Departamento de Biología Celular y Molecular, Facultad de Ciencias,
Universidad de la Republica, Montevideo, Uruguay
2 Unité de Neurosciences Intégratives et Computationnelles,
CNRS-UPR 2191, Gif sur Yvette, France
3 División de Neurofisiología Comparada (Unidad Asociada a la
Facultad de Ciencias, Universidad de la Republica) IIBCE, Montevideo,
Uruguay
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Fig. 1. (A) Schema of experimental paradigm, showing the object (a metal plate),
the receptive field on the skin surface (gray circle) and the position of the
electrode pair used to record the local electric organ discharge (LEOD). (B)
Photomicrograph of the electrosensory lobe (ELL) in cross section, showing the
position of the microelectrode recording field potentials in the granular
layer. (C) Comparison of LEODs recorded at the receptive surface and field
potentials recorded in the ELL for the control situation without any external
object and in the presence of a variety of objects of different conductivity
but similar in volume and form, aligned with the center of the receptive
field. Left column: LEOD recorded at the receptive field center (green).
Middle column: field potentials recorded in the ELL in the presence of a
reafferent sensory input (red) and in the absence of reafferent sensory input
(black). To obtain the latter traces, the output of the electric organ was
shunted with a metal plate close to the tail: in this case reafferent sensory
input is absent and the field potential corresponds to the effect of the
corollary discharge alone. Right column: the field potential equivalent to the
sensory response (FPSR; blue) calculated as the difference between the
recordings with and without reafferent input (red minus black traces in middle
column). Field potentials are averages of 10 traces.
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Fig. 2. Electrosensory coding by field potentials and primary afferent unit
activity. (A) Change in area of the negative peak of the field potential
equivalent to the sensory response (FPSR) plotted as a function of the
peak-to-peak amplitude of the local electric organ discharge (LEOD), when a
metal plate (black circles) or plastic plate (red diamonds) were placed
parallel to the fish in the region of the electric organ, at increasing
distances lateral to the fish's body. Zero represents the control value, in
the absence of any object. (B) Area of the negative peak of the FPSR as a
function of its latency at half-amplitude. (C) Raster plot of the activity of
a single afferent fiber while a metal object was moved along the side of the
fish. The vertical lines indicate the mean latencies of spike timing in the
absence of any object (two spikes only). (D) Interval between the first and
the second spikes as a function of the latency of the first spike after the
motor command. Points of different colors correspond to data from different
primary afferent units recorded in the same fish.
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Fig. 6. Response patterns to a metal object located at different distances lateral
to the fish's body. Top: primary afferent unit response as a function of the
rostro-caudal position and lateral distance of the object. Two groups of 10
raster diagrams represent the latency of the spikes of a primary afferent unit
when an object was moved in 5 mm steps rostro-caudally along the fish body, at
distances of 2 mm (left) and 7 mm (right) from the skin. The vertical red
lines indicate the mean latencies of the basal spike discharges in the absence
of an object. Bottom: color maps represent the field potential equivalent to
the sensory response (FPSR) as a function of time and object position as in
Fig. 5, for objects moved
rostro-cadally along the fish's body axis, at lateral distances of 1 mm
(left), 7 mm (middle) and 17 mm (right) from the skin. Object position is
shown relative to the fish picture on the left; the red dot indicates the
receptive field center.
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Fig. 3. This theoretical schema explains qualitatively how the local electric organ
discharge (LEOD) at the receptive field center (RF) changes with the position
of a conductive object. (A) The colored bars indicate different positions of a
cylindrical object. (B) Colored curves indicate the corresponding image
profile, i.e. the change in LEOD peak-to-peak amplitude compared with the
basal LEOD (broken line), projected on the fish's receptive surface when the
object is placed at the different positions indicated by corresponding colors
in A. Image amplitudes at points indicated by colored dots are plotted below
in C. (C) The changing image as the object moves past the receptive field
center. The graph was constructed by plotting the change in LEOD peak-to-peak
amplitude seen at the center of the receptive field as a function of the
rostro-caudal position of the object. Colored points represent the image
amplitude compared with the basal LEOD, seen at the receptive field center
when the object is in the corresponding color-coded position. Note that this
graph reflects the Mexican hat shape present in the LEOD profiles but shows
inverse asymmetry: thus, when the object is caudal to the center of the
receptive field, the surround effect at the receptive field center is larger
than when the object is rostral.
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Fig. 4. Area of the field potential equivalent to the sensory response (FPSR)
negative peak as a cylindrical object (metal or plastic, oriented
perpendicular to the skin) was moved from rostral to caudal along the body,
passing through the center of the receptive field (gray bar, 0 mm). The
horizontal dotted line indicates the area of the FPSR negative peak in the
absence of any object, as a control value.
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Fig. 5. Primary afferent and field potential response patterns to objects of
different conductivity. Top: primary afferent unitary response as a function
of the longitudinal position and conductivity of the object. Two groups of 10
raster diagrams show the latency of a primary afferent unit firing when a
plastic object (left) or a metal object (right) was moved in 5 mm steps along
the fish's body. Position zero indicates the center of the receptive field.
Bottom: the color maps represent the field potential equivalent to the sensory
response (FPSR) as a function of time after the electromotor command
(horizontal axis) and as a function of object position along the fish's body,
relative to the receptive field center (red dot; vertical axis indicated by
the fish body at the left). Results obtained with a plastic cylinder are shown
on the left and with a metal cylinder on the right. The horizontal color bar
shows the basal FPSR in the absence of an object. The vertical color bar
indicates the color code for instantaneous voltage of FPSR record. (Note that
the time scales used in the raster plots and the color maps are
different.)
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Fig. 7. Effect of the surround on the field potential equivalent to the sensory
response (FPSR). (A) An artificial stimulus was given via a dipole
electrode simultaneously with the electric organ discharge (EOD) at the
receptive field center (RFC; red dot; 0 on the horizontal axis of the graph)
and at different points along the rostro-caudal axis (dotted line),
illustrated relative to the fish's head. Potentiation of the field potential
reafferent sensory response (relative to the basal response, =0) was maximal
when the simultaneous artificial stimulation was applied close to the
receptive field center but was also observed when the artificial stimulation
was rostral to the receptive field center or up to 20 mm caudal to this point.
Surround inhibition was not seen when the artificial and natural stimuli
occurred simultaneously. (B) Comparison of the basal FPSR with that obtained
when an artificial excitatory stimulus was applied synchronously with the EOD,
in the center of the receptive field. The effect of this stimulus is
represented by difference between the two FPSRs, shown by the blue and red
areas. (C) The basal FPSR (blue trace; control) and FPSRs obtained at the same
recording point when a metal cylinder (green trace) or a plastic cylinder (red
trace) were placed facing the non-electroreceptive area of the flank labeled
`object' in A. Electrical stimulation at the same point had no visible effect
on the reafferent sensory response.
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© The Company of Biologists Ltd 2004
