Contextual effects of small environments on the electric images of objects and their brain evoked responses in weakly electric fish
Department of Integrative and Computational Neurosciences, Instituto de Investigaciones Biológicas Clemente Estable, Av. Italia 3318. Montevideo Uruguay
* Author for correspondence (e-mail: angel{at}iibce.edu.uy)
Accepted 6 January 2005
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Summary |
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Key words: active electrolocation, prereceptor mechanism, refuge behaviour, sensory adaptation, electric fish
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Introduction |
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There are theoretical and experimental reasons to believe that contextual
effects are also present in electroreception, a sensory modality evolved by
aquatic animals (Lissmann,
1958; Bullock and
Heiligenberg, 1986
; Moller,
1995
). Electric fish are electroreceptive animals that explore
their environment with the discharge of specialized electric organs (electric
organs, EOs; electric organ discharges, EODs). The EO generates an electric
field that is sensed by cutaneous electroreceptors
(Lissmann and Machin, 1958
;
Bullock et al., 1961
). Objects
in the near environment cause changes in the electric field and in the
patterns of transepidermal current density and voltage stimulating the
electroreceptive surface. The `electric image' of an object has been defined
as the change in the pattern of the transepidermal field caused by that object
(Bastian, 1986
;
Caputi et al., 2002
;
Budelli et al., 2002
).
Two lines of arguments converge to suggest that electric images of given objects are conditioned by the presence of other objects in the electric scene.
First, previous work done by our group has shown that the body of the fish
is itself an object that decisively shapes the electric field generated by the
EOD (Castelló et al.,
2000; Aguilera et al.,
2001
; Caputi,
2004
). The fish body implements a pre-receptor mechanism enhancing
the reafferent signals at the perioral region, which may be described as an
electroreceptive fovea (Castelló et
al., 2000
; Caputi et al.,
2002
). The presence of large objects near the fish may alter the
above-mentioned funnelling effect, causing consequent changes in the electric
image of other objects (Budelli et al.,
2002
; Rother et al.,
2003
).
Second, the presence of such large objects is not an exceptional event, but the rule in fish life. In fact, rather than swimming in the middle of the stream, electric fish are frequently found among the roots of floating plants or inside caves on the banks of the rivers. Moreover, most electric fish in captivity choose to stay long periods resting in tubes, or at the angle between the floor and the side of a large object when they are in captivity. These objects may be likened to the structures used as refuges in the nature environment.
This article shows contextual effects on electric images of objects caused by the characteristic electric fish behavior of hovering in tubes. The article also reports the experimental analysis of (i) the physical basis of the changes imposed by small environments on electric images; (ii) the field potential responses at the electrosensory lobe of chronically implanted animals when entering and leaving tubes; and (iii) the effect of context on object discrimination and its implications for electrosensory processing.
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Materials and methods |
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Recorded variables
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Voltage signals were differences amplified and filtered (band pass 1010 kHz) using a high input impedance differential amplifier. A digital oscilloscope was used for online observation and averaging of EOD triggered traces (864 sweeps). Signals were also recorded for offline measurement and data processing using a Labmaster card and Axotape software.
Effects of tubes on the physical image of objects
sLEODs were measured in fish restrained within a band of tissue paper and
inside copper or plastic tubes (22 mm inner diameter, 10 cm length) in the
presence and in the absence of the stimulus object. Different longitudinal
resistances for the object were tested using the procedure described above
(Fig. 1B).
Effects of tubes on the sensory carrier
The carrier of sensory signals is the basal energy that the object presence
modulate for generating images. In the case of active electroreception the
carrier is the electric field `illuminating' the object. This field can be
considered as generated by an equivalent source completely described by two
parameters: its electromotive force and its internal resistance (Thevenin
theorem'; Edminister, 1965).
In order to estimate these parameters we measured in the same experiments the
voltage drop between the two carbon electrodes of the stimulus-object and
calculated the current through the object by dividing the measured voltage
across the load resistor. The electromotive force and internal resistance
correspond to the ordinate intersection point and the slope of the line fitted
to the voltagecurrent plot, respectively.
Mechanisms of the effects caused by small environments
We hypothesize that the tubes modify the summation of currents generated by
different regions of the EO at the foveal region. In order to test this
hypothesis, we studied sLEOD components generated by the caudal or rostral
portions of the EO when the fish was inside or outside a tube. To dissociate
the abdominal and the trunktail components of the sLEOD we applied the
following procedure. Under cold anesthesia the spinal cord was exposed by a
laminectomy and severed between the rostral and middle third of the fish.
Spinal section was used to abolish the trunk- and tail-generated EOD (three
fish) leaving intact V1 and a small remnant of V3
generated by the abdominal region
(Trujillo-Cenóz et al.,
1984; Caputi and
Trujillo-Cenóz, 1994
). Stimulation of the sectioned cord at
the caudal stump was used to evoke the sequence
V2V3V4 generated by the caudal
two thirds of the fish body. Electrical stimuli (0.1 ms, 20 Hz, amplitude
supra-maximal for the EOD) were applied through a pair of nichrome wires (200
µm thick, 50 k
) implanted within the canal to stimulate the
bulbospinal electromotor tract. In order to assess the completeness of
the section and the effectiveness of the spinal cord stimulation we checked
the amplitude and waveform of the resultant EOD equivalent electromotive
forces using the air-gap technique (see
Caputi, 1999
).
Effects of the tubes on electrosensory discrimination
Increases in stimulus-object conductance and thus image contrast elicited
changes in the EOD rate characterized by transient reductions of the inter-EOD
interval (novelty responses; Bullock,
1969). We used novelty responses to evaluate the fish's
electrosensory discrimination ability, as in previous studies
(Aguilera and Caputi, 2003
;
Caputi et al., 2003
). Novelty
responses evoked by the same changes in object resistance were studied in
three experimental conditions: (a) in open field, (b) inside a plastic tube
and (c) inside a metal tube (both tubes were 10 cm in length). In these
experiments, each trial consisted in the change of image amplitude from a
basal (the stimulus-object without resistive load) to a comparison level (set
by shunting the carbons for 5 s every 30 s with a known resistor). The sLEOD
was simultaneously measured and the change in its amplitude provoked by the
variations in object resistance was calculated as the increment of the r.m.s.
value (
r.m.s.). To detect novelty responses, we plotted the inter-EOD
interval sequence. For each response the intervals were numbered starting at
the first interval after the resistance change (I1,
I2....In). The baseline inter-EOD
interval (I0) was defined as the mean of the five
intervals preceding the change in stimulus-object resistance. We defined the
amplitude of the novelty response as the normalized maximum shortening of the
inter-EOD interval (novelty response amplitude = 1 minimum of
Ii/I0, I = 1 to n).
Effects of the small environments on brain field potential responses
We recorded field potentials in the electrosensory lobe in four fish. To
study the dynamic effects of small environments on these field potentials the
fish were restrained wrapping them in tissue paper within a long pen made by
stretching a plastic netting over a frame consisting of three longitudinal
plastic rods (1 cm x 1 cm x 50 cm) held at either end by plastic
frames (squared contour of 5 cm x 5 cm). One of the beams was against
the bottom of the tank and the others were one at each side. The fish
naturally stayed at the bottom of the V-shaped duct and its
longitudinal movements were restrained by a couple of cotton balls. Recording
procedures for sLEOD and field potentials were as explained above (1 and 2).
The relative positions of the electrodes and the fish were visually controlled
and remained unchanged during the experiments. Trials in which fish moved were
cleared from the records. A U-shaped plastic structure (6 cm between
the U arms, 8 cm tall, 10 cm long) was manually moved back and forth
with the aid of a system of pulleys (Fig.
1D). One of the pulley wheels was attached to a variable resistor
that conducted a constant current square pulse (5 ms, 1 mA) triggered by each
EOD. In this way, the recorded voltage drop across the variable resistor coded
the structure position at the time of each EOD. We explored the effects of
different kinds of longitudinal movement of the plastic structure, including
step-like and sine wave-like oscillatory movements of different span,
velocities and/or frequencies.
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Results |
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The relative positions of the fish and the tube also change the reafferent stimulus. While the maxima of the r.m.s. value occurred when the snout was just protruding from the limit of the U-shaped plastic structure (in the most commonly observed position adopted by the fish) their minima occurred when the jaw was at the middle of the structure. Important changes in the waveform were also observed as a function of the tube position. Fig. 3 shows sV3 (Fig. 3A) and the ratio sV4/sV3 (Fig. 3B) as a function of the distance between of the rostral border of a U-shaped plastic structure and the fish jaw (see Materials and methods, field potentials).
To assess the effects of the tubes on electric images we changed the
longitudinal resistance of the cylindrical stimulus-object and recorded the
sLEOD at the facing skin (see Aguilera and
Caputi, 2003). The sLEOD amplitude decreased as a function of
object resistance in all conditions. The sLEOD corresponding to each
resistance value of the object changed in proportion to the carrier amplitude,
i.e. the amplitude of the sLEOD in the absence of any object (sLEOD increased
markedly in the plastic and decreased slightly in the metal tube,
Fig. 4AC).
Physical mechanisms underlying tube effects
In this section we report a series of experiments to investigate how tubes
modify imaging mechanisms. The carrier of sensory signals is the basal energy
that the object presence modulates for generating images. In the case of
active electroreception the carrier is the electric field `illuminating' the
object. According to the Thevenin theorem
(Edminister, 1965), if in a
given condition the source `illuminating' the object were linear it could be
represented by an electromotive force (EMF) in series with a resistance
(Rs). This source is the equivalent source of the system
containing all other elements (the fish, the water and, potentially, the tube)
in the scene except the object. In this context the LEOD is proportional to
the EMF and to the inverse of the sum of the series plus the object
resistances (Rs+Ro):
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In Fig. 4, we compared the electric image in three conditions: inside the plastic tube, inside the metal tube or outside the tube (the control condition). While changing the condition caused changes in amplitude and waveform of the sLEOD, the changes in object resistance only affected sLEOD total energy (r.m.s. value) and did not affect the sLEOD waveform in a significant way. This feature and the proportionality between the r.m.s. values of the sLEODs evoked by the same object impedance at the three different conditions explored (Fig. 4C and insets), suggested that the physical mechanism explaining the change in object image is the change in the electromotive force of the electric source `illuminating' the object.
The changes in the LEOD r.m.s. value associated with a given object
(Ro) when changing the condition from `outside the tube'
to `inside tube' could be due to at least one of the following reasons: (i)
tubes cause a change the r.m.s. value of the electromotive force (EMF) or (ii)
tubes cause a change in the series resistance (Rs) of the
equivalent source `illuminating' the object. Our experiments show that the
LEOD inside a tube was proportional to the LEOD outside tubes. This implies
that:
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We confirmed this theoretical conclusion in a series of experiments showing that plastic tubes increase the electromotive force of the equivalent electric source `seen' from the object in an amount similar to the increase of the carrier and electric image. In Fig. 5 voltage measured between the object tips is plotted as a function of the current through the object. This allowed us to calculate the electromotive force (ordinate intersection point) and the series resistance (slope) of an equivalent source `seen' by the object. This indicates that plastic tubes increase object's electric `illumination' which, in turn, increase the imprimence (see Discussion) that they cause and also increase the constrast of the electric image that they project. The plot of Fig. 5A shows the r.m.s. value of the voltage between the poles of the stimulus object as a function of the current through the object. While the slope of the line, corresponding to the internal resistance of the electric source `illuminating' the object was constant, the ordinate intersection, (i.e. the electromotive force) increased by 2.5 times (the same amount as the increase in LEOD).
The change in waveform of the sLEOD also reflected the change in waveform of the electromotive force of the `illuminating' source. Wave components generated more caudally showed a more pronounced increase. While sV3 generated all along the fish exhibits the smaller increase (about 2 times), sV4 generated mainly at the tail exhibits the maximum increase (about 3.5 times); sV2, generated at the centre of the fish body increases in an intermediate manner (about 2.5 times). This is shown in Fig. 5BD by the gradation of the increase in ordinate intersection. Taking into account these results and that the sLEOD is the `weighted sum' of multiple regional EOD components, we hypothesized that caudally generated currents reach the foveal region in larger proportion when the fish is inside a plastic tube.
This hypothesis was tested by altering the electrogenic properties of
different regions of the EO in animals by spinal sections. In three fish the
sLEOD was recorded inside and outside the tube before and after spinal section
silencing the caudal region of the EO. When the spinal cord was severed at
about one third of the distance from head to tail, the remaining EOD consisted
mainly of sV1 (Fig.
6A, orange trace). In addition, when stimulating the distal stump
of the severed spinal cord we recruited the electromotoneuron pools and
reproduced the normal activation of the caudal region of the EO generating
sV2, sV3 and sV4
(Aguilera, 1997;
Caputi, 1999
;
Fig. 6B, orange trace). When
the fish was inside the tube, sV1 decreased to about one half of
the control value (Fig. 6A,
green trace) and the caudally evoked sV3 increased about 3 times
the control value (Fig. 6B,
green trace). We concluded that the carrier changes are explained by the
simple physical model described in Fig.
6C,D.
Effects of the context on object discrimination
A first strategy to assess how the changes in the electrosensory carrier
and images are relevant for sensory processing was to explore discrimination
of small resistive objects facing the fovea. In six fish, we applied the
technique described by Aguilera and Caputi
(2003).
Fig. 7AC show the
novelty responses when changes in object conductance from open circuit to 4.5
µS, 15 µS and 2000 µS were applied respectively. When fish were
inside plastic tubes the amplitude of the novelty response was significantly
larger than seen in the control (Fischer exact test, P<0.01; 6
fish and 6 different changes in object conductance). No significant
differences were found between the metal tube and control experiments. This
implies that there is a larger sensitivity of the electrosensory system to the
same change in object conductance when the fish is in the plastic tube.
Moreover, changes in stimulus-object conductance that were close to threshold
for eliciting the novelty response in the metal tube or in control conditions,
always generated a novelty response when the fish was inside the plastic tube.
The amplitude of the novelty response was an increasing function of the change
in object conductance and the presence of the tube shifted the curve upward
and the abscissa intersection point (threshold) to the left
(Fig. 7D), indicating an
increase in sensitivity for the same change in object conductance. However,
when the amplitude of the novelty response was plotted as a function of the
change in sLEOD amplitude (
sLEOD), a single logarithmic function fit
the data obtained in both conditions (Fig.
7E), which suggests that the ability to discriminate changes in
object image amplitude was not altered by the presence of the plastic
tube.
Electrosensory lobe field potential responses to the sLEOD
A second strategy to assess how the changes in the electrosensory carrier
and images are relevant for sensory processing was to record field potentials
in animals chronically implanted with electrodes in the rostral regions of the
ELL where the electrosensory fovea is represented.
Field potentials showed a characteristic pattern of response following the
EOD (Fig. 8A). These responses
show three clear components that can be assigned to the fast and slow
electrosensory pathways defined by Szabo et al. (1973): (i) A brief spike
occurs at short latency (13 ms) after the EOD. This corresponds to the
fast electrosensory pathway and will be referred to as FEP response
(Castelló et al.,
1998). (ii) An early slow wave starting at about 24 ms
after the EOD and lasting about 5 ms. In some recordings this response showed
small spikes, probably corresponding to the synchronized activity of primary
afferents and/or granule cells from the deeper layers of the ELL (referred to
as SEP early response). (iii) A series of slow waves starting about 710
ms and lasting for the rest of the interval between EODs (SEP late response).
This response showed larger variability than the early SEP and probably
corresponds to the activity of the more dorsal layers of the ELL
(Maler, 1979
).
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To confirm that these three are evoked electrosensory responses we studied their variability when the sLEOD amplitude was altered by plastic U-shaped structure movements. We calculated the peri-EOD standard deviation across an ensemble of 300 subsequent epochs of 30 msduration, each epoch starting 5 ms prior to the EOD. We plotted the standard deviation of the voltages recorded at a given time after the EOD as a function of such time (Fig. 8B) We compared six sets of responses each obtained using a different experimental protocol altering the sLEOD (top plot, black traces). As a reference the post-EOD averaged response when the fish was in an open field condition is displayed in the bottom plot. This analysis shows three clear peaks in the standard deviation of the signal that we assigned to the changes in the activities of the fast electrosensory pathway (FEP) and the early and late components of the slow electrosensory pathway (SEP). We tested the alternative hypotheses that these changes in the response were provoked by changes in the inter-EOD interval or by lateral line stimuli. In the same fish we recorded the ELL evoked responses by a nearly constant sLEOD when the fish was stimulated by vibratory stimuli causing large EOD accelerations. We recorded an ensemble of 300 consecutive peri-EOD epochs obtained with the fish resting in open field while gentle taps on the aquarium wall were applied. The post-EOD standard deviation did not produce the characteristic trimodal profile observed when the sLEOD was modified. Instead it showed a flat profile (Fig. 8B, red trace), confirming that the three peaks coincident in time with the three described components of the field potentials are caused by changes in electrosensory signals but not by vibratory stimuli or by the change in EOD interval.
Characteristics of the different electrosensory responses to changes in electric images
Discrimination experiments suggested the presence of adaptive mechanisms to
avoid saturation of the electrosensory system. We studied whether the
different responses in the electrosensory lobe showed adaptation when fish
goes in and out small environments.
The FEP response consists of a spike. The amplitude of this spike is linearly correlated with the r.m.s. value of the preceding pulse (Fig. 8C). The slow electrosensory pathway (SEP) response was characterized by two main components characterized by their latency and dynamics. The early SEP response showed little adaptation, whereas the late response showed clear adaptation. Fig. 9A shows the electrosensory lobe field potentials (color coded) in response to a sequence of sLEODs when the tube was moved along the fish axis coming from the caudal region. In this colormap the horizontal dimension corresponds to time after the EOD and the vertical dimension to the course of the experiment. Both early and late potentials changed with tube position. To analyse the change in these responses we subtracted the average response in open field from every evoked response (results shown as a color map in Fig. 9B). We measured the amplitude of the response at selected latencies corresponding to the early and late SEP responses (vertical lines). While the amplitude of the early response remained similar after the step in the sLEOD, the late response showed a progressive attenuation (Fig. 9C,D). In addition, we observed in all fish that sudden increases or decreases of the sLEOD provoked by step-like movements of the tube evoked very large responses at about 710 ms after the EOD. This transient component increased in latency and diminished in amplitude, disappearing in less than 1 s (1015 EODs). Fig. 9E shows three consecutive evoked responses just after a step-like movement of the tube (red traces) caused a change in sLEOD amplitude. These traces are compared with the averaged field potentials obtained outside the tube (green traces) and inside the tube, at the best position (blue traces). In one of the four fish this transient response to a step change in sLEOD appeared clearly separated in time (Fig. 10, single vertical arrow) from the rest of the late response, which exhibited a much less pronounced adaptation (Fig. 10, double vertical arrows).
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Discussion |
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This discussion address three important points about contextual effects of resting in a tube: (a) the physical mechanisms underlying changes in object image caused by small environments, (b) how these contextual effects affect sensory discrimination and (c) how the electrosensory lobe deals with the large changes in waveform and amplitude of object images caused by small environment contextual effects.
Physical mechanisms underlying tube effects
Lissman and Machin (1958) coined the expression `object imprimence' to
describe the `imprint' of an object on the fish's self-generated electric
field. Imprimence may be viewed as a virtual electric field caused by the
presence of the object (Lissman and Machin, 1958). Since the `electric image'
of a given object is defined as the change in the pattern of the
transepidermal field caused by the presence of the object, such an `electric
image' is just the object imprimance at the sensory surface.
All materials other than water cause electric imprimence on the EO
generated field. Because the imprimance of an object is also an electric
field, the imprimance of every object is modified by the presence of other
objects and reciprocally. Therefore, the electric image of a given object is
highly dependent of the presence of other objects
(Rother et al., 2003).
The fish body is the object that most decisively shapes the electric field
generated by the EOD and consequently the electric imprimance of surrounding
objects. This is because the low impedance of the internal tissues and the
silhouette of the fish body facilitates the flow of current from caudal to
rostral regions of the fish
(Castelló et al., 2000;
Aguilera et al., 2001
; A.
Migliaro, A. A. Caputi and R. Budelli, unpublished data). In addition, the
caudal region behaves as a `current generator', forcing current rostrally.
Therefore, the carrier and the local reafferent signals are enhanced in the
perioral region. In addition, the number and variety of receptors as well as
their central projection field are maximal in this region. For these reasons
the sensory mosaic at the perioral region has maximal spatial resolution and
has been likened to an electrosensory fovea
(Castelló et al.,
2000
). Our experiments confirm the hypothesis that a tube
surrounding the fish body modulates such funneling effect and modifies
electric images of nearby objects at the fovea.
We showed that the plastic tube decreased the lateral shunting of current, facilitating funnelling to the perioral region of the faster waves (sV2sV3sV4) generated at the caudal region of the EO. Thus, the most caudally generated sV4 is the component that increases the most. In addition, the slow early component (sV1) as well as the abdominally generated component of the positive wave (sV3) are reduced because abdominally generated current must flow along the tube, facing a larger resistance path. Since the abdominal region of the EO acts as a `voltage' source, the generated current decays because of the voltage drop that occurs along a path of higher resistance (Fig. 7C,D).
The presence of a metal tube causes a different effect. It short-circuits the return of the currents generated at the caudal regions, preventing their funneling to the fovea. Nevertheless, the low internal resistance of the `voltage' equivalent source at the abdominal region of the EO allows it to maintain most of its contribution to the sLEOD. For this reason, the decrease of the sLEOD inside a metal tube is not as dramatic as its increase inside a plastic tube.
Changes in proximal stimuli determine the amplitude of the novelty responses
One of the most important functions of sensory systems is to highlight
perceptual experience of the attributes of objects that are more closely
correlated with the intrinsic properties of the object than with their images.
The objects in the environment are called distal stimulus while the image on
the sensory mosaic is called the proximal stimulus
(Palmer, 1999).
This function of the nervous system allows an evaluation of the attributes
of objects independently of the context or scene in which they are immersed.
For example, the whiteness of a paper remains the same whether looked at
indoors or outdoors under the sunlight (see also Adelson's web page
web.mit.edu/persci/people/adelson/checkershadow_illusion.html).
This is not the case for fish evaluation of electric attributes of objects
that lead to novelty responses. In our previous studies we showed that novelty
responses were graded with both the change in object impedance and the change
in their corresponding images (sLEOD;
Caputi et al., 2003). However,
in those experiments the changes in sLEOD were correlated one-to-one with the
changes in object impedance, and therefore it was impossible to answer the
question about which of those variables determines the amplitude and threshold
of the novelty response. The increase in carrier amplitude and object image
generated by plastic tubes allowed us to compare the effects of the same
change in object impedance when the change in image amplitude was different.
It also allowed us to compare the effects of similar changes in image
amplitude when the change in object impedance was different. The experiments
reported in the present article show that fish respond with larger novelty
responses to the same change in object resistance when the change in image was
larger. In addition, similar changes in the r.m.s. value of the sLEOD
generated similar novelty responses. Thus, novelty response depends only on
changes of the object's image. Thus, the novelty response depends on the
proximal stimulus at the receptor surface, not on the distal stimulus in the
environment. It should be noted, however, that at distal stimulus perception
(i.e. evaluation of the absolute attributes of the object) probably occurs in
parallel by the central nervous system of these fish. The presence or absence
of such function must be evaluated, therefore, by indicators other than the
novelty response.
The discrimination experiments reported here suggest the presence of
central adaptive mechanisms in the sensory evaluation of electric images. Even
though the basal sLEOD in plastic tubes is about 2.5 times the basal stimuli
observed in open field, and its waveform is different, the amplitudes of
novelty responses generated by similar energy changes in the sLEOD were
similar. This indicates that the increase of the basal image caused by the
plastic tubes does not saturate the sensory system, suggesting that adaptation
takes place at central structures. If receptors were adapting to the basal
stimuli they would probably evaluate the change in stimuli differently, which
in fact does not occur. In addition, this confirms that the basal sLEOD
waveform and amplitude are independently subtracted from the present image to
detect novelty (Aguilera and Caputi,
2003; Caputi et al.,
2003
).
Field potential responses in the chronically implanted fish
The fast electrosensory pathway (FEP) was easily identified by the
characteristic early, large peak that was modulated in latency and amplitude,
without adaptation, by changes in the amplitude of the sLEOD
(Castelló et al.,
1998). The simplicity of the fast electrosensory response
corresponds to the simplicity of its circuitry, and the complexity of the slow
electrosensory response (variability, multiple components and long duration)
corresponds to the complexity of its circuitry
(Carr and Maler, 1986
).
Analysis of the standard deviation of the voltage recorded at a given time
after the EOD indicates the presence of an early and a late stage in the SEP
response. The latter could be broken down into subcomponents of different
dynamics in relation to the sequence of images.
Timing and dynamics of the early slow responses suggest that they may
correspond to the deepest layers of the ELL, including primary afferents and
cells of the granule layer (Maler,
1979; Carr and Maler,
1986
; Bastian,
1986
). The late slow electrosensory responses observed in this
study may correspond to more dorsal layers of the electrosensory lobe
including the polymorphic cell layer, and the effects of recurrent inputs
coming from higher centers (Bastian,
1995
; Berman and Maler,
1999
). These late responses show adaptation with two different
rates of decay after step and hold stimuli. Step-like changes in the
electrosensory image caused the appearance of a transient wave at the
beginning of the late response that rapidly decayed and increased in latency.
The step-like increases of the sLEOD also evoked a long-lasting change of the
late response that exhibits a slow decay. Interestingly, the presence of two
subcomponents having different time constants may suggest the presence of
different types of responses in the cells of the ELL. The different dynamics
of these responses is not surprising since the presence of adapting and
non-adapting cells differently involved in the recurrent electrosensory loops
was recently described in wave gymnotids
(Bastian et al., 2004
). These
adaptive responses in the ELL of pulse gymnotids appear similar to those
described in the electrosensory systems of other fish
(Bell et al., 1993
;
Bastian, 1995
;
Bastian et al., 2004
;
Bodznick et al., 1999
). Our
study suggests that the discrimination rules described in G. carapo
by Caputi et al. (2003
) may
partially be implemented at the electrosensory lobe by the storage and
subtraction of a moving average of past electric images from the current
input.
Conclusions
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Acknowledgments |
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References |
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