Probability and amplitude of novelty responses as a function of the change in contrast of the reafferent image in G. carapo
Department of Neurofisiología Comparada, Instituto de Investigaciones Biológicas Clemente Estable, Associated Unit of Facultad de Ciencias, Av. Italia 3318, Montevideo, Uruguay, CP 11600
* Author for correspondence (e-mail: angel{at}iibce.edu.uy)
Accepted 10 December 2002
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Summary |
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Key words: contrast discrimination, contrast adaptation, electric fish, Gymnotus carapo, fovea, short term memory, sensory representation
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Introduction |
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Pulse gymnotids show a typical orienting behavior, the novelty response
(Lissmann, 1958;
Szabo and Fessard, 1965
;
Larimer and McDonald, 1968
;
Bullock, 1969
; cf.
Hopkins, 1983
;
Kramer, 1990
;
Moller, 1995
). This behavior
consists of a transient shortening of the inter-electric organ discharge (EOD)
interval triggered by changes in nearby impedance. It has been frequently used
to test a fish's electrolocation ability and to assess the effects of
reafferent and exafferent input on pacemaker frequency
(Bullock, 1969
;
Heiligenberg, 1980
;
Grau and Bastian, 1986
;
Hall et al., 1995
;
Zellick and von der Emde,
1995
; Post and von der Emde,
1999
).
After studying novelty responses evoked by a short-circuit in the presence
of different amounts of noise, Heiligenberg
(1980) inferred that B.
occidentalis `develop and maintain a `template' or central register of past
electroreceptive afferences against which novel afferent input is
compared'. Taking into account this hypothesis we posed the following
questions: what information is extracted from the input? What information is
stored in the comparison `template'? What are the rules relating changes in
electrosensory image and electromotor output?
Our experiments showed that: (i) the system compares the contrast of every input image with a moving average of the contrast of past images, (ii) when contrast difference between the actual input and the moving average of past images overcomes a threshold, a novelty response is evoked, and (iii) the amplitude of the novelty response is graded with the contrast difference.
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Materials and methods |
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Experimental set up
Fish were held in a net in the middle of a tank (18 cmx25 cmx10
cm) containing 3 liters of water with a conductivity of 100±10 µS
cm-1. To create and change an electric `stimulus-object' we used a
method introduced by von der Emde
(1990). A cylindrical
stimulus-object (2 mm diameter, 1 cm length) was oriented with its long axis
perpendicular to the skin of the electrosensory fovea
(Castelló et al.,
2000
). The two ends of the cylinder were made of graphite carbon
discs (1.5 mm in diameter) inserted into a non-conducting plastic tube. The
carbon ends were connected to an optocoupled switch (Hamlin HE721 Eneka SA,
Montevideo, Uruguay) via insulated copper wires (Cerba SA,
Montevideo, Uruguay), which left the tube at its center. To avoid
non-controlled stimuli due to the reaction of carbon impurities with water,
the probe was maintained immersed in water of 100 µS cm-1
conductivity for a few days prior to beginning the experiments until
completion. In addition, and for the same purpose, we followed the procedure
described by von der Emde
(1990
) of connecting a large
capacitor (2.2 µF) in series with the switch that did not alter the
recorded local EOD (LEOD) waveform.
To quantify the local electric image contrast, the voltage drop between the bare tip of a 100 µm diameter insulated copper wire placed against the skin and the base of the stimulus-object cylinder nearest to the fish was measured (Fig. 1A). These electrodes were 2mm apart and thus the electric field in V cm-1 was five times the voltage drop between the electrodes. Signals were amplified (x100), and filtered (band pass 10-10000 Hz, AM Systems, Inc. Carlsborg WA, USA); a digital oscilloscope (Hewlett-Packard model 54601A, USA) was used for observation of individual LEOD waveforms that were also sampled (20 kHz, 12-bit resolution, Lab Master DMA A/D card, Scientific Solutions Solon, Ohio, USA) for off-line measurement of the inter-EOD interval (home made signal processing program).
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Experimental design
The experimental design was inspired by the methodology introduced by Weber
and formalized by Fechner (cited by
Werner, 1980). Weber's
procedure was based on what is now known as `comparative unidimensional
judgements', where a subject is asked to discriminate between two stimuli. A
particular stimulus of a given type (baseline or standard stimulus) is applied
alternately with one of a number of other stimuli (the comparison stimulus)
that are of the same type but differ in a single physical parameter
(Werner, 1980
).
According to Caputi et al.
(1998), Sicardi et al.
(2000
) and Budelli and Caputi
(2000
), the electrosensory
image of a resistive cylindrical object has a `Mexican-hat'-shaped profile,
controllable by changing the load resistance, and confirmed by our results
obtained in the present study. Thus a single parameter, the amplitude of the
signal at the center of the `Mexican-hat' profile, can be used to estimate the
contrast of the electric image of the stimulus-object.
The experiments were performed at the perioral region, where density,
variety and central representation of the sensory mosaic are maximal, and
therefore this region has been defined as an electrosensory fovea. At this
region, background stimulus in the absence of objects is spatially coherent
(i.e. it shows the same triphasic waveform all over the foveal region;
Aguilera et al., 2001). At the
perioral region, resistive objects modulate the local field, generating a
`Mexican hat' spatial profile of the stimulus amplitude
(Fig. 1). Despite this,
modulation is associated with small waveform changes, which are predictable
from the total energy of the local stimulus
(Aguilera and Caputi, 2003
;
Fig. 1). Therefore, the
amplitude pattern is sufficient to describe the image of resistive objects.
Since the normalized spatial pattern is not modified when the distance of the
object remains constant (Budelli and
Caputi, 2000
), the change in amplitude at the top of the `Mexican
hat profile' (i.e. the skin facing the object) describes the change of the
image. Consequently, the contrast of the image generated by a resistive
stimulus-object can be estimated by a single parameter: the peak-to-peak
amplitude (PP) of the local electric field at the skin facing the object.
It should be noted that PP in the presence of the object may be larger or
smaller than PP recorded in the absence of the object. When the object load
was a resistor of 100 k a flat profile equivalent to that observed in
the absence of the object was recorded, and this image has null contrast.
Resistors lower than 100 k
generated top-external `Mexican hat'
profiles (Fig. 2A, right) and
resistors higher than 100 k
generated top-internal `Mexican hat'
profiles (Fig. 2A, left).
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Four variables were controlled during the experiments: (i) baseline
contrast estimated as PP before a change in the resistance of the object, (ii)
baseline duration, (iii) comparison contrasts estimated as PP after a change
in the resistance of the object, and (iv) comparison stimulus duration. The
difference between baseline contrast and comparison contrast (PP) is
referred to as contrast change. As the electromotor activity is a series of
brief and discrete events, the changes in duration of either the baseline or
the comparison periods lead to changes in the number of images evaluated
during these periods.
In order to control these four parameters, the longitudinal resistance of the stimulus-object was changed by means of the optocoupled switch timed with an S88 stimulator (Grass Instruments, Quincy, MA, USA). In each experiment, an external variable resistor r0 was connected between the carbon discs to set the baseline contrast. A second, variable resistor r1 was connected periodically in parallel to shunt r0, and thus set the comparison contrast (Fig. 2).
Data analysis
Novelty responses are transient reductions of the interval after a change
in image contrast. To detect novelty responses, we plotted the peristimulus
inter-EOD interval (I) 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 5 intervals preceding the change in stimulus-object resistance and
its lower confidence limit as the mean minus 2 standard errors (S.E.M.). Two
criteria were employed to define a novelty response: (1) a successive
shortening of two intervals immediately after the change in impedance and (2)
a second interval (I2) significantly smaller than the
baseline confidence limit (I2<I0-2
S.E.M.). The probability of the novelty response for a given experimental
condition was estimated as the relative frequency of novelty responses in a
set of trials. We defined the amplitude of the novelty response as the
normalized maximum shortening of the inter-EOD interval (novelty response
amplitude = 1 minimum of I/I0). The
second interval was the briefest in most cases (I3 was
exceptionally the briefest).
Experimental paradigms
Stimulus-object resistance (determining PP) was controlled in a
trial-to-trial manner, setting independently the number and amplitude of both
baseline and comparison stimuli. Our experimental paradigms were designed to
answer the following questions.
(1) How many images different from baseline have to occur to be detected?
In order to elucidate whether the number of comparison stimuli determine the
characteristics of the novelty response, we compared the effects of two
stimulation patterns differing only in the duration of the comparison period.
Single odd events (in which the contrast of a single image was increased) were
compared with increase-and-hold patterns (in which the contrast of
approximately 100-120 successive images were increased during a 4 s period).
For every change in contrast (PP), two trials were done. In one case
the sequence was baselineincrease and holdbaselinesingle
odd event, and in the other it was baselinesingle odd
eventbaselineincrease and hold. Baseline contrast was constant
(r0=
open circuit) and baseline duration was 30 s. The results
are shown in Fig. 4.
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(2) How different should the comparison image be for detection? In most
sensory systems, discrimination depends on baseline level (Weber and Fechner's
and Stevens' laws; Werner,
1980). In order to study whether the baseline contrast level
influence the amplitude of the novelty response, we explored the effects of
similar changes in contrast (
PPs) starting at different baselines.
Increase-and-hold patterns (baseline period, 29 s; comparison period, 1 s)
were applied, starting at several different baseline PP values. Up to 30
PP values were explored in each fish for every baseline PP (7 fish; the
results are shown in Fig.
5A).
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(3) Is the amplitude of the response graded with the change in image
contrast? If so, what is the function that describes the relationship? To
explore the effect of the previous electrosensory stimulation on the amplitude
of the novelty response, we performed two sets of experiments. In the first
set, the relative duration of the baseline and comparison periods were
modified from trial to trial, without changing the total trial duration (the
results are shown in Fig. 6).
In five fish, trial duration was 30 s, and in the other two fish trial
duration was 100 s. In all trials, the amplitudes of the baseline and
comparison image contrasts were set by stimulus-object resistances of 470
k and 15
, respectively. In the second set of experiments, the
duration of baseline period and
PP were both varied (three fish; the
results are shown in Fig.
7A,B). Three baseline periods and four
PP were explored for
each fish. In each case the comparison stimulus was set by one of four
different r1 values (100 k
, 47 k
, 22
k
or 15
) connected in parallel with r0 (470
k
), which also set the baseline contrast. Each trial began with a
period in which the stimulus had the same amplitude as the comparison
stimulus, followed by a baseline period of the desired duration (2, 10 or 29
s), and ending by a comparison period lasting 1 s. In all cases the trial
lasted 30 s.
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(4) Does the baseline level have influence on the amplitude or probability
of the response? Similar experimental paradigms were used to explore the
probability of eliciting novelty responses. The probability of novelty
response as a function of PP and baseline PP was studied in five fish.
Discrimination experiments consisted of 10-20 cycles in which object
resistance was alternated between two values, every 30 s. We never found
novelty responses for decreases in the image contrast even though we explored
up to the largest possible
PP (stepping from short to open circuit,
Fig. 3B). Thus, for the purpose
of detailed analysis, the low amplitude period was considered as the baseline
contrast. Probability distribution curves as a function of
PP were
constructed for 4-6 baseline contrasts (results shown in
Fig. 5B).
Threshold50 (T50) was defined as the
PP eliciting
novelty responses in 50% of the cases.
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(5) Finally, does the stimulation history have an influence on the amplitude or probability of the response? In three other fish we applied asymmetric cycles to evaluate the influence of stimulation history on the T50. Cycles consisted of 29, 10, 2 or 0.5 s baseline periods and 1, 20, 28 or 29.5 s comparison periods, respectively, and the results are shown in Fig. 7C,D.
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Results |
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A decrease of object impedance (that produced an increase in electrosensory
stimulus contrast, Fig. 2B,C)
evoked a typical novelty response consisting of an immediate shortening of the
next two inter-EOD intervals (Figs
2C,D and
3, left). The third interval
after the change in image contrast was usually similar or a little longer than
the second. Over the subsequent discharges the inter-EOD intervals slowly
returned to the initial baseline values. In addition, the variability of the
EOD interval after the change in object resistance was larger than during the
baseline period (Fig. 3A). This
typical pattern was constant for novelty responses evoked by changes in
self-generated electric images, allowing us to distinguish these novelty
responses unequivocally from other acceleration-slow return patterns (cf.
Moller, 1995).
Interestingly, we found that only the variability of inter-EOD intervals increased in response to a reduction in image contrast; novelty responses were absent (Fig. 3B). Although the observed change in interval variability could indicate image discrimination, its analysis was not included in this study.
Changes in image contrast induced by a change in object impedance were
presented with a minimum interval of 30 s. This period included 600-1200 EODs,
depending on the baseline pacemaker mean frequency. During successive trials,
the amplitude of the novelty response elicited by the same pattern of stimulus
varied randomly around a mean value, which indicates that under our
experimental conditions the electrosensory-evoked novelty response did not
show habituation. This finding is consistent with the observations of Grau and
Bastian (1986), who showed the
lack of habituation of novelty responses to novel stimuli presented at
intervals larger than 20 s.
A single discrepancy in image contrast is sufficient to provoke the
novelty response
Novelty responses, as other types of orienting responses, result from
comparing a sensory input with some kind of expectation
(Sokolov, 1990). To understand
this kind of comparison we investigated firstly how many images constitute the
sensory input that is compared with the expectation signals. In other gymnotid
fish and under a different stimulation protocol, the amplitude of the novelty
response has been reported to increase with the number of images modified by
the novel stimuli (Heiligenberg,
1980
). On the other hand, Bullock
(1969
) studied the novelty
response in a variety of pulse gymnotids and concluded that `... the
electroreceptor input has a cycle by cycle access to the pacemaker'.
Similar results were obtained in pulse mormyrids by Meyer
(1982
), suggesting that fish
evaluate single images against a stored representation.
Thus, the first set of experiments were designed to test the hypothesis that a sustained increase in contrast of various subsequent reafferent images is more efficient for provoking novelty responses than an increase in the contrast of a single reafferent image.
In three fish a series of 10 novelty responses resulting from a maximum
increase in contrast of a single image (single odd event) were compared with a
series of 10 novelty responses resulting from a maximum increase in contrast
of several consecutive images (increase-and-hold pattern). For the same
experimental conditions, the mean amplitude of the novelty response evoked by
a single odd event was larger in some fish and smaller in others than the mean
amplitude responses evoked by an increase-and-hold pattern. Statistical
analysis performed for each of the fish showed no significant differences
between the means (t-test, P<0.01).
Fig. 4A shows an example from
one fish comparing the effects of both stimulus patterns. The mean amplitude
of the novelty responses to a single odd event was larger but not
statistically significant (t-test, P<0.01, N=10)
than the mean amplitude of the novelty responses to a increase-and-hold
pattern. The similarity in the relaxation time course of both novelty
responses is illustrated by the linear relationship when one response is
plotted against the other (Fig.
4A, right); the slope of the line depends on the occasional
difference between mean amplitudes. From these experiments it can be seen
that, irrespective of the subsequent duration of the comparison period, the
initial increase in contrast of the image (PP) not only triggers the
novelty response but also determines its amplitude. Once the response is
triggered, it follows a time course that is not controlled by the subsequent
electrosensory input.
The amplitude of the novelty response was graded according to the evoked
increment in the image contrast, following the same relationship independently
of the number of comparison stimuli (Fig.
4B). Responses to the increase-and-hold pattern were compared with
those evoked by single odd event following the protocols illustrated in the
inset. Starting from a single baseline level (r0=),
each trial consisted of a pair of stimuli: a single odd event followed 30 s
later by a 4 s held stimulus of identical
PP, or vice versa.
In successive trials
PP was varied randomly. We observed that the
amplitude of the novelty response increased similarly with
PP for both
stimulation patterns. The amplitude of the novelty response was well fitted by
a logarithmic function of
PP:
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Discrimination function and scaling of the response are independent
of the contrast baseline
The general rule is that discrimination threshold increases with the
baseline amplitude (following a function characteristic of the considered
sensory system; Werner, 1980).
This kind of rule would imply a dependence on the absolute value of the
contrasts of the compared images. It has been also speculated that fish
compare images pulse-to-pulse, against a fixed template
(Moller, 1995
), or have the
`ability to remember what the current flow through its skin would look
like in the undisturbed condition and be able to compare at this site the
field in the presence of shadows from objects'
(Hopkins, 1983
).
In a second set of experiments we tested the hypothesis that the described
function parameters are baseline dependent. As shown in
Fig. 5, the relationship
between PP and the amplitude and probability of the novelty response
was independent of the reafferent image baseline contrast. For data obtained
starting from any given contrast baseline, the threshold
(
PP0) and scaling constant (K) were similar to values
calculated from the pooled data of the same fish (ANOVA-test,
P>0.1, Fig. 5A).
For the overall population of the seven fish, means and standard deviations
(S.D.) of these parameters obtained from pooled data for each fish were:
PP0=18±12 mV cm-1 and
K=0.13±0.07.
We also measured the probability of evoking a novelty response as a
function of PP. Changes in object resistance induced
PP of
different amplitudes, ranging from -120 mV to +120 mV. Each amplitude change
was induced from different baseline contrasts (10-20 trials for each
PP
and each baseline contrast). Novelty responses occurred only for
PP
larger than 4-8 mV cm-1. This
PP was comparable to the
`spontaneous' variation of the local signal due to respiration and other small
movements. As illustrated in Fig.
5B, the probability of evoking a novelty response was a sigmoidal
function of
PP. This function was the same for every baseline contrast.
Thus, unlike other sensory systems, the critical factor for evoking a novelty
response was the absolute increase above the baseline contrast rather than a
function of the baseline contrast. The contrast increment that evoked novelty
responses in 50% of the cases (T50) was characteristic for
each fish (ranging between 5 and 25 mV cm-1). It is worth noting
that
PP0 and T50 yielded similar values,
despite being estimated by different methods
(Fig. 5A,B). It is also
important to recall that
PP0 was similar when explored with
a single odd event pattern or with an increase-and-hold pattern in the same
fish (Fig. 4B).
Threshold and scaling constant depend on the preceding temporal
pattern of stimulation
The experiments illustrated in Figs
4 and
5 show that the difference in
contrast between the baseline and the very first image that surpasses an
incremental threshold value determines the amplitude of the orienting
responses according to a logarithmic law. This relationship is baseline
independent. It should be noted that the same change in contrast can be
achieved by flattening a `top-inward' `Mexican-hat' profile or increasing a
`top-outward' `Mexican-hat' profile. These results indicate that G.
carapo is permanently evaluating the change of the stimulus pattern
independently of the baseline contrast. This means that the fish does not
compare incoming images with a fixed template. Moreover, this suggests that
novelty responses result from the comparison of the neural response to the
very first altered electric physical image with a central representation of
the past sensory input. This leads to the question of how many images
contribute to such representation. In the third type of experiments we tested
the hypothesis that fish evaluate PP in a pulse-to-pulse manner, simply
comparing the contrast of each image with that of the immediately preceding
image. We found that this is not the case
(Fig. 6). Novelty response
amplitude is a function of the number of images of the same baseline contrast
that precedes the change in contrast. In these experiments, we changed the
duty cycle regulating the relative timing of baseline and comparison stimulus
periods without altering the total trial duration
(Fig. 6 inset). Object
resistance was alternated between 470 k and 15
to produce large
changes in contrast. This procedure allowed us to control the number of EODs
included in the baseline and comparison periods of the trial. Novelty response
amplitude increased with the number of baseline EODs from 50 to 900, with a
maximum slope at approximately 120 EODs (representing 3-6 s, depending on
pacemaker frequency). Similar results were obtained for different EOD
pacemaker frequencies and for both trial duration studied (100 or 30 s),
suggesting that the number of EODs, and thus the number of electrosensory
images, is the relevant variable.
The increase in novelty response amplitude as a function of the number of
images during the baseline period could result from changes in either the
scaling constant, the threshold, or both. We addressed this issue in a fourth
series of experiments (N=3 fish) in which the duration of the
baseline period (r0=, open circuit) was set at 2,
10 or 29 s, and trial duration was kept constant at 30 s. The results
consistently showed that the scaling constant was an increasing function of
the number of baseline EODs (Fig.
7A,B). The
PP0 values calculated by
curve-fitting were similar for 10 and 29 s in all fish; however, curve-fitting
was not a reliable method for calculating
PP0. Note that all
amplitudes of novelty responses obtained with a baseline period of 2 s were
similarly small, which is consistent with the flat profile shown in
Fig. 6 for less than 80
baseline EODs.
The dependence of novelty response threshold on recent past sensory history
was further studied by comparing the probability distribution functions of
novelty responses for baseline periods of 29, 10, 2 and 0.5 s (including
approximately 900, 300, 60 and 15 EODs). For baseline periods lasting 2, 10
and 29 s, the probability distribution curves were similar (N=3 fish,
Fig. 7C). Although a small
increase in T50 was consistently observed for baseline
periods lasting 2 s, the change in scaling constant was the most important
factor to explain the decay of the amplitude of the novelty response with this
stimulation pattern. Data obtained with a very short baseline period (0.5 s)
were more dispersed and had a larger T50. In these
experiments there were an important number of failures even when the explored
PP was the maximum possible (r0=
, open
circuit, r1=0, short circuit,
Fig. 7D).
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Discussion |
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We used the novelty response as an index of discrimination. This is an
electromotor orienting behavior consisting of the transient reduction of the
inter-EOD interval followed by a gradual return to baseline. The dependence of
the amplitude of the novelty response on the change in stimulus indicates that
occurrence of this orienting behavior is a reliable index that the stimulus
has been sensed and evaluated. For this reason novelty responses have been
extensively used as index of electrolocation
(Bullock, 1969;
Heiligenberg, 1980
;
Grau and Bastian, 1986
;
Hall et al., 1995
;
Zellick and von der Emde,
1995
; Post and von der Emde,
1999
). However, the failure of a sensory stimulus to evoke a
novelty response does not mean that it has not been sensed. In fact, our
experiments show that the interval variability can be modified by a change in
image contrast even though it might not evoke novelty responses. Therefore, it
is important to establish first what kind of information is obtained by
analyzing the amplitude and probability of the novelty response as a function
of the change in electric image contrast.
The function relating probability and change in image contrast is the same
when starting the experiment from different baseline image contrasts. It is
important to note that the compared images consist of spatial modulations of
the self-generated electrosensory carrier, which provides a basal effective
stimulus for electroreceptors. This indicates that the observed behavioural
threshold is not set by the electroreceptor threshold. It also suggests that
the response to the comparison stimulus should be contrasted with the response
to the baseline stimulus by a sensory readout mechanism somewhere in the
central nervous system. The observation that the effect of a single odd event
is the same as the effect of an increase-and-hold temporal pattern indicates
that only the response to the very first event of the comparison stimulus
train (actual input) is contrasted with the response to the baseline input. By
contrast, Heiligenberg (1980)
found that a change of at least two or three images is necessary to elicit
novelty responses in B. occidentalis. Differences between studied
species and experimental designs might account for the discrepancies. While
Heiligenberg's (1980
) strategy
was to add artificial background noise against which a single relatively broad
and blurred image generated on the side of the fish was compared, our results
were obtained by changing the contrast of smaller and sharper images on the
electrosensory fovea.
Our finding of a function relating the amplitude of novelty response to the change in image contrast indicates that the above-mentioned read-out mechanism provides the electromotor system with the relevant input for controlling the amplitude of the novelty response. Thus, the changes in the parameters of the described function were used to study the dynamic effects of stimulus presentation.
As occur with the probability function, the parameters of the amplitude
function are the same for different baseline contrasts held constant for a
long period. This is opposite to the common finding across most sensory
systems where the discrimination threshold generally depends on the baseline
stimulus (Weber and Fechner's and Stevens' laws;
Werner, 1980). For baselines
equal or larger than 2 s the amplitude of the novelty response was scaled with
contrast increase, according to a baseline-duration-dependent rule
(Fig. 7B). For the same change
in contrast, the amplitude of the novelty response gradually decreased as the
fraction of baseline period in the total cycle of stimulation was shortened
(Fig. 6). This suggests that
the amplitude of the novelty response is influenced by a long-lasting
stimulation period including baseline images and also images belonging to the
comparison period of the preceding trial. The most important reduction of the
response was observed when the baseline period included less than 80-100 EODs
(2-4 s), but some influence was detected up to 900 EODs (29 s), indicating
that the relative importance of an electrosensory image on the transference
function parameters fades out as the following images are integrated in a
central expectation signal.
The threshold is significantly affected by past input only when the
baseline period is shorter than 2 s (including up to 60 EODs). This period
might correspond to the `certain minimal period of time to stabilize and
update a central state or `template' of electroreceptive afferences on the
background of which local novelties can be more readily discerned' as
described by Heiligenberg
(1980). However, our results
suggest that threshold for eliciting novelty responses is not the best
parameter for extracting information about sensory processing. Threshold is
independent of previous history, except when the increase in image contrast is
just preceded by a decrease in image contrast. The interaction of two
successive, opposite and different lasting effects (the increase in image
contrast eliciting otherwise a novelty response and the preceding decrease in
image contrast generating a longer lasting effect indicated by the increase in
interval variability) might explain this change in threshold. By contrast, the
scaling constant appears to be a reflection of sensory processing features
such as the generation of a central template. In fact, while the certainty of
provoking a novelty response is only affected by the contrast of the few
preceding images, the amplitude of the novelty response is affected by the
contrast of images occurring up to half a minute before. The scaling constant
is an increasing function of the number of baseline images for all the
explored range of baseline duration, which suggests that the central
expectation signal or `template' is renewed with a much longer constant than
previously calculated based on threshold analysis (60 EODs versus
hundreds of EODs).
Our results support the hypothesis of a `template' generation initially
proposed by Heiligenberg
(1980), but reject the
hypothesis of a fixed template, or a pulse-to-pulse comparison of the incoming
images. In addition, study of the transference function of the
electrosensoryelectromotor transformation indicates that the scaling
constant of this function is the most sensitive parameter for evaluating the
template dynamics. The growth of this parameter with the number of low
contrast baseline images indicates that the relative load of a given image in
creating the `template' fades as consecutive EODs continue to occur.
The most likely structure suited for storage and comparison of sensory
responses is the electrosensory lobe. The principal output cells of this
cerebellum-like structure are driven by the integration of electrosensory
inputs with the parallel fiber input coming from other sensory and motor
structures, as well as serving feed-back from higher level electrosensory
structures (Réthelyi and Szabo,
1973; Maler, 1973
,
1979
;
Bell et al., 1997b
;
Berman and Maler, 1999
). This
type of circuit fulfils the requirements to act as the kind of comparator
between input and internal sensory representations proposed by Sokolov
(1990
). Recordings from single
cells in the electrosensory lateral line lobe of mormyrids
(Bell, 1981
; Bell et al.,
1993
,
1997a
,b
,c
),
wave type gymnotids (Bastian,
1995a
,b
,
1996a
,b
,
1998
,
1999
) and elasmobranch
(Bodznick et al., 1992
,
1999
;
Bodznick, 1993
;
Montgomery and Bodznick, 1995
)
have demonstrated that sensory expectations mirror imaging the moving
average of the past sensory input cancel out expected inputs and boost
novel inputs. It is important to note that this process does not rule out
other synergistic mechanisms such as peripheral receptor adaptation
(Xu et al., 1996
) or further
processing at higher levels of the electrosensory pathway. In fact, Grau and
Bastian (1986
) found that
`most units studied in the torus semicircularis showed very strong,
increased responsiveness' to novel stimuli.
Unlike gymnotid and mormyrid wave fish, exhibiting continuous
sine-wave-like EODs (Bass,
1986), pulse fish electrosensory system must identify a change in
the images generated by the fish's own EOD involving an additional associated
task. Pulse mormyrids compare and update the reafferent information in a
pulse-to-pulse manner by a plastic change of an electromotor command corollary
discharge signal interacting with the reafferent electrosensory input (Bell,
1981
,
1982
, Bell et al.,
1993
,
1997a
). However, in G.
carapo, as well in other pulse gymnotids, there is no evidence of a
pacemaker corollary discharge
(Heiligenberg, 1980
;
Bastian, 1986
;
Castelló et al., 1998
).
The presence of a well-timed expectation signal independent of an electromotor
corollary discharge is reflected in the occurrence of `omitted stimulus
potentials' when stopping repetitive electrosensory stimuli in elasmobranch
(Bullock et al., 1990
). This
phenomenon, signaling the time during which the omitted sensory input should
have occurred, is widespread in nature; it is observed in both vertebrates and
invertebrates, from the very peripheral to the highest levels of sensory
processing (Bullock et al.,
1990
,
1993
; Karamürsel and
Bullock, 1994
,
2000
;
Ramon et al., 2001
), and it
might underline the central expectation mechanism suggested by our data.
However, invasive techniques will be required to elucidate whether and how
pulse-discharging gymnotids simultaneously deal with detection, storage,
comparison and discrimination of reafferent and exafferent signals.
The stereotyped time course of the novelty response is independent of the
stimulus pattern, suggesting that this behaviour is probably not completely
organized within electrosensory structures. Transient accelerations of the
pacemaker frequency are elicited not only by reafferent electrosensory signals
but also by exafferent signals of various sensory modalities, which indicates
that the electromotor control of pacemaker is the final common path of an
alert system triggered by novel sensory stimuli. Theoretical and experimental
studies of pacemaker structures show that the interval between pulses is a
logarithmic function of pacemaker input
(Hansel et al., 1998). Thus,
to fit the present results it should be considered that pacemaker cells, which
set the timing of the EOD, might introduce the logarithmic rule.
In conclusion, we propose the following hypothesis to explain the sensory-motor integration of the novelty response: (1) the central nervous system of the fish computes the difference between the response to each incoming electric reafferent image and a `central expectation signal' or `template' that is repetitively updated with each EOD; (2) the novelty response is triggered by a threshold-based decision process; (3) once threshold is achieved, the amplitude of the novelty response is determined by the difference between the `template' and the response to the reafferent input; (4) the relaxation curve following the initial shortening of the interval is determined by the electromotor side of the system. The creation of the `template' and the comparison process are most probably carried out on the sensory side in electrosensory lateral line lobe. The triggering decision and the logarithmic scaling processes are probably carried out at the pre-pacemaker and pacemaker structures, respectively.
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Acknowledgments |
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