Frontiers in Zoology
BioMed Central
Open Access
Research
The Schnauzenorgan-response of Gnathonemus petersii
Jacob Engelmann*†, Sabine Nöbel†, Timo Röver and Gerhard von der Emde
Address: University of Bonn, Institute for Zoology, Endenicher Allee 11-13, 53115 Bonn, Germany
Email: Jacob Engelmann* - Jacob.Engelmann@uni-bonn.de; Sabine Nöbel - snoebel@uni-bonn.de; Timo Röver - timo.roever@uni-bonn.de;
Gerhard von der Emde - vonderemde@uni-bonn.de
* Corresponding author †Equal contributors
Published: 22 September 2009
Frontiers in Zoology 2009, 6:21
doi:10.1186/1742-9994-6-21
Received: 11 May 2009
Accepted: 22 September 2009
This article is available from: http://www.frontiersinzoology.com/content/6/1/21
© 2009 Engelmann et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background: Electric fish navigate and explore their dark and turbid environment with a
specialised electric sense. This active electrolocation involves the generation and perception of an
electric signal and fish have proven to be useful model systems for the investigation of sensorymotor interactions. A well studied example is the elephantnose fish, Gnathonemus petersii, which
has a characteristic and unique elongated chin covered with hundreds of electroreceptor organs.
This highly moveable so-called Schnauzenorgan constitutes the main fovea of the active
electrosensory system. Here we present first evidence for a sensory-motor loop relating active
electrical sensing to active motor exploration of the environment.
Results: Both anatomical and behavioural evidence have shown that the moveable Schnauzenorgan
is crucial for prey localization. Here we show for the first time that a motor response
(Schnauzenorgan-response, SOR) can be elicited by novel electrosensory stimuli. The SOR could
be triggered with highest reliability by novel electrical stimuli near the Schnauzenorgan and, to a
lesser extend, near the head of the animal. The probability of evoking the response depended on
the magnitude of the amplitude change of the electric input, with bigger changes eliciting SORs
more reliably. Similarly, increasing the distance of the stimulus reduced the response. In this respect
the SOR is comparable to the well described novelty response, a transient acceleration of the
production rate of electric signals, although the latter occurs at a shorter delay and can also be
evoked by non-electrical stimuli.
Conclusion: Our experiments show a novel motor response that is mediated by the active
electric sense of Gnathonemus petersii. This response will allow a detailed analysis of the neural
system underlying direct interaction between sensory and motor processes in future experiments.
Background
In the course of evolution many different sensory systems
and sensory receptors have developed. One of the rather
unique sensory systems is that of active electrolocation
and electro-communication found in Mormyriform and
Gymnotiform weakly electric fishes from Africa and South
America, respectively. During active electrolocation
mormyrids emit and simultaneously perceive electric signals, which enable them to detect and analyse nearby
objects. This is considered as an adaptation enabling electric fish to extend their activity to the hours of darkness,
since the dependence on vision is expected to be reduced.
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The electric field of G. petersii is generated by a synchronous discharge of an electric organ. Each electric organ
discharge (EOD) has a duration of roughly 400 μs, and at
rest EODs are elicited 3 to 8 times per second [1,2]. This
discharge frequency varies between 1 and 100 Hz and
depends on the behavioural context. The electric field that
surrounds the animal during each EOD is optimized for
electrolocation around the head as the field has the highest coherence and impinges at an angle of almost 90°
onto the receptors [3]. Since the amplitude of this field
drastically declines with distance, active electrolocation is
generally confined to the range of one body length of the
animal [4].
Both ampullary and tuberous electroreceptor organs are
devoted to the detection of electrical fields. Ampullary
electroreceptors are extremely sensitive to low frequency
fields of biotic or abiotic origin and are generally used in
the context of passive electrolocation [5]. In contrast,
tuberous electroreceptor organs are involved in active
electrolocation (Mormyromasts, [6,7]) or electro-communication (Knollenorgans, [8]). Central filtering mechanisms enhance sensory information conveyed by the
Mormyromasts in response to the self-generated EOD
only, whereas Knollenorgan input is selectively filtered
centrally such that secondary neurones are very sensitive
to the EODs of conspecifics [9].
In this study we are mainly interested in possible links
between (motor) behaviour and electrolocation. It has
been shown that the Mormyromast system is important
for foraging and orientation [10,11]. Fish can perceive a
wealth of information form their 'electrical' world, including parameters such as size and distance of objects and the
differentiation of various object properties, like capacitive
and resistive electrical properties [for review see: [12]].
The main stimulus parameters utilised by the animals are
phase and amplitude of the EOD. Briefly, the EOD can be
modulated in amplitude as well as in its waveform by a
nearby object. Local EOD amplitude is determined by the
resistance of an object, with low resistance objects causing
an increase in the local EOD amplitude, while non-conductors decrease the stimulus amplitude [13]. Capacitive
objects of a certain range of capacitances change the EODamplitude and additionally distort the EOD waveform
[14,15].
A well known behaviour linked to electro-perception in G.
petersii is a sudden and transient increase in the EOD rate
(shortening of inter-EOD intervals) when a nearby object
is suddenly altered in its properties. This so-called „novelty response [6] is found both in Mormyriform and Gymnotiform weakly electric fishes [16,17]. The novelty
response can be regarded as an active electrical orientation
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mechanism in response to new sensory input [18]. This
response can be evoked by electrical [19-23], acoustical
[24], visual [17] and mechanosensory lateral-line stimuli
[25] as well as multi-model stimuli [26].
Anatomical data indicate a special role of the
Schnauzenorgan (SO) and the head during active electrolocation [3,27]. Based on these data and corroborating
behavioural observations, the SO and the nasal region are
believed to be functionally equivalent to two distinct electrical "foveae". One of the behaviours that support a
foveal function of the SO are oscillating movements during foraging, i.e., the Schnauzenorgan is bent in rapid
movements perpendicular to the animal's longitudinal
axis [28]; Hollmann et al, in preparation). In addition,
sudden movements of the Schnauzenorgan can be
observed when novel objects are detected. A key question
in the current paper is whether SO movements are linked
to electro-perception and if so, which type of stimuli
might evoke this behaviour.
Given the fast rhythmic movements of the SO during foraging, we here investigate the hypothesis that these movements, like the novelty response extend the reach of
electrolocation, especially during the detection and analysis of novel stimuli. We confirm this hypothesis and further characterise this motor-response by determining
which receptors contribute to it, how it is linked to the
novelty response and by determining the sensitivity of the
response for stimuli at various body regions.
Results
Schnauzenorgan response
In the following we describe the movements of the
Schnauzenorgan in response to changes in the impedance
of dipole objects. Following a general description of the
responses to our standard stimulus paradigm, we present
in detail how these responses depend on the distance and
position of the dipole object, and how the SOR is linked
to the novelty response.
In 14 fishes the responses to sudden changes in the
impedance (n = 1206) of a dipole object [14] (Fig. 1) were
tested (Fig. 2). Switches were between a shunted and
open-circuit object (see standard stimulus in the material
and methods section). Motor-responses of the
Schnauzenorgan could be evoked in all fish by both, an
impedance-switch from a low to a high impedance (Fig.
3B, on-stimulus) or when returning from the high impedance state to the low impedance state (off-stimulus).
While the absolute change in resistance is identical for the
on- and off-stimuli, we currently have no data on the effect
of the baseline level, i.e., we do not know if similar contrasts of the stimuli will evoke similar motor-responses
regardless of the baseline from which stimuli come from.
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A
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SO frontal
SO tip
W
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W>
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Set-up 1
Figure
Set-up. A. Schematic illustrating the five paired lateral positions and the frontal position of the dipole-object (see inset). Distances from skin were varied between 1, 3, 5, 7, 10, 12 and 15 mm. B. Example for data extraction for the novelty response.
The top shows EODs in response to four consecutive switches between a low resistance (shunt) and a high resistance as a
raster plot. Following normalisation by the mean and variance (z-score), a significant acceleration of the EOD rate is apparent
in the bottom plot (red dot). Responses were scored as significant if z-scores below -1.96 were achieved within 5 EODs after
the switch (p < 0.05).
SORs had a mean angular velocity of 89.4 ± 34.3 deg/sec
(data based on 15 responses of two fishes using highspeed video-tracking, range: 41 - 151 deg/sec). Depending
on the distance and placement of the dipoles, response
probability reached levels of up to 70% (see Fig. 3B, C).
Responses to both on- and off-stimuli were pooled since
they occurred at equal probability when the standard
stimulus paradigm was applied (χ2 = 0.18, p = 0.67, df =
1). Since either two dipole-objects were placed at both
sides of the animal or a single dipole-object was placed in
front of the Schnauzenorgan, the observed movement
patterns are analysed separately below.
When a single dipole-object was placed frontally to the tip
of the Schnauzenorgan (see Fig 3A), the SORs occurred
either to the sides, or, especially at the shortest lateral distance tested (1 mm), consisted of a downward retraction
of the Schnauzenorgan (Fig 3A).
When the dipole-objects were positioned to the sides of
the animal (see Fig. 2A), the initial movement in response
to the stimulus could be directed either towards (634 of
2412 stimuli) or away (639 of 2412 stimuli) from the
object. Movements in either directions were observed at
equal probability (χ2 = 0.66, p = 0.41, df = 1). On-stimuli
evoked slightly more evasive movements (292 towards,
and 432 away), while off-stimuli resulted in more movements towards the object (330 towards and 309 away) (χ2
= 3,97, p = 0.046, df = 1).
In general, the Schnauzenorgan moved to or away from
the dipole-object, reached a maximal displacement (up to
28 degrees or 5 mm displacement of the tip) and then
moved back to the resting position. Here, it either stopped
(282 responses towards the object, 291 movements away
from the object), continued to move in the opposite direction (n = 94/89), or moved again in the same direction as
in the initial response (n = 93/103). Up to seven consecutive movements of the Schnauzenorgan following a single
stimulus were observed (see Fig. 3C). However, more than
two Schnauzenorgan movements were rarely observed,
and their frequency was equal to that to control stimuli
(see below). Movements were equally likely directed
towards or away from the change in the electric field, i.e.,
the SORs were undirected.
Frequency of the SOR in relation to stimulus location
The probability at which a Schnauzenorgan response can
be evoked depended on the lateral distance and the position of the dipole-object and varied between fishes. In all
cases, the SOR-likelihood was highest when stimuli were
delivered close to the skin and declined with increasing
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Figure 2 of the Schnauzenorgan
Movement
Movement of the Schnauzenorgan. A. Sequence of the SOR filmed at 128 frames/s ordered from left to right and top to
bottom. Every second frame is shown, resulting in a timeline of 15.6 ms from frame to frame. Numbers in each frame give the
time in ms with respect to stimulus onset. The dipole-object's resistance was changed during the 2nd frame of the first row. The
beginning of the SOR is highlighted by the green square (first frame in the second row). The peak displacement of the SO is
indicated by the orange frame. Note that for the sake of clarity, eighteen frames between the stimulus and the initial SOR have
been omitted (see top hand corner in A and blue box in B). B. Tracking data of the Schnauzenorgan's displacement. C. Instantaneous EOD-frequency as measured during the sequence shown in A and B. Note that the SOR peaks about 400 ms after the
novelty response. Time of stimulation, first and maximal SOR are indicated in B and C by the three vertical lines.
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tt ta ttt tat taa tta
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a aa at aaa ata att aat
Responses
Figure 3 of the SOR
Probability
Probability of the SOR. A. Example of the Schnauzenorgan response evoked at the tip of the Schnauzenorgan. The change
in resistivity occurred in the second frame (frame-rate 40 ms/frame, timeline in individual frames is given with respect to stimulus onset). First movement (green) and max SOR (orange) are indicated. B. Bar plot of the probability of the occurrence of a
Schnauzenorgan response with the object placed at different distances from the skin pooled for all dipole-positions. Only
responses that consisted of one (black), two (medium grey) or three full movements (light grey) are shown. White bars show
the absolute probability of a response. The light grey area within the white columns represents the probability of a
Schnauzenorgan response evoked by a control stimulus (no change in object resistance). This measure served as a reference
for the spontaneous level of Schnauzenorgan responses. Data were pooled for on- and off-stimuli. C. Probability of 14 different
types of movement observed during an SOR. Light grey columns correspond to movements starting with a movement towards
the object, while black columns show those responses where the Schnauzenorgan initially was moved away from the object.
The direction of consecutive movements is given by the letters below the bars (a = away, t = towards). Numbers above graphs
in B and C give the absolute number of stimuli the data are based upon.
lateral distance, reaching the level of the controls (16%,
average over all controls) at 15 mm distances (Fig. 3B).
Analysis of the probability of SORs as a function of the
placement of the dipole showed that SORs were evoked
most reliably at the middle of the Schnauzenorgan,
whereas SOR-probability declined towards the operculum
and towards the tip of the Schnauzenorgan (Fig. 4A, C).
Amplitude of the SOR
A considerable variation in the effectiveness of eliciting
SORs was found between fishes, especially with regard to
object distance. SORs in response to changes of the
impedance of dipoles placed at a distance of 1 to12 mm
were of equal amplitude and significantly stronger than
those obtained at a distance of 15 mm (Kruskal-Wallis
test: h = 20.6, F = 3.51, post-hoc Dunn test p < 0.05; Fig
4B). At 15 mm distance, the amplitude of the movement
was indistinguishable from spontaneous movements of
the SO (Fig. 4B, false alarm rate - FAR). Spontaneous SORs
occurred at a low rate (7 SORs in 384 stimuli) and their
amplitude was lower than those caused by dipole-objects
placed within a range of 12 mm from the animal's skin
(see Fig. 4B, C). Thus, within the range where the animals
were responsive, SORs caused by our dipole-objects were
of similar amplitude and this range extended up to a distance of about 12 mm from the skin surface.
Combining SORs at all distances for each position shows
that the SOR amplitude decreased weakly from rostral
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frames/sec; 16 SORs) obtained from one fish. These data
show that the peak of the novelty response occurred at a
mean latency of about 40 ms after changing the electrical
properties of the dipole-object. The latency of "off"
responses was significantly longer than that of "on"
response (paired t-test: p < 0.001)(Figs. 2B, 5A). In contrast to the novelty response, SORs had a much longer
latency (about 500 ms, see also Fig. 2 bottom), and "off"
response latencies were shorter than "on" response latencies (paired t-test: p < 0.001)(Fig. 5B, C).
Figure 4 of SOR
Probability
Probability of SOR. A. Probability of the SOR as a function
of the dipole-object's position along the body of the fish.
Black filling represents a single SOR, medium grey two, and
light grey bars three consecutive responses, respectively. The
total probability of a SOR is given by the white bars. Numbers above the graphs show the absolute number of stimuli
(100%) at each position. B. Box-and-Whisker plot of the
amplitude (peak amplitude) of the SOR as a function of distance. SOR amplitude were almost constant at object distances of 1 to 12 mm, while amplitudes decreased at a
distance of 15 mm C. Box-and-Whisker plot of the peak
amplitude of the SOR as a function of dipole position. SORs
declined in amplitude form rostral to caudal along the fish's
body. In B and C horizontal lines above the plots summarise
the results of the Dunn post-hoc test (p < 0.05). Data
labelled FAR in B and C indicates the false alarm rate amplitudes.
towards more caudal dipole positions (Spearman's rho =
-0.1, p = 0.004, N = 806; Fig 4C). Overall, stimulation at
the Schnauzenorgan and mouth resulted in stronger SORs
than stimulation near the eyes, the operculum or those
caused by control stimuli (Kruskal-Wallis test, h = 57.9, F
= 8.92, post-hoc Dunn test p < 0.05; Fig 4C).
Latency of the SOR and the novelty response
In order to analyse the latency of the SOR and to compare
it with the latency of the simultaneously recorded novelty
response, we used high-speed video sequences (128
Sensory modalities evoking SORs
Several experiments were conducted in order to examine
which modality of the electrosensory system (active/passive) can evoke SORs. In one series of experiments, the
resistance of the dipole-object (3 mm distance, middle of
the Schnauzenorgan) was not altered, while the object's
capacitance was switched from 1 μF to 1 nF. The effect on
the local EOD-amplitude of such purely capacitive
switches is equivalent to the effect of a switch from a big
resistor to a shunt. However, purely capacitive objects
constitute a "filter" for low stimulus frequencies (including DC-potentials) and thus only stimulate tuberous electroreceptors. In contrast, resistive switches can contain
low frequencies and therefore potentially stimulate both
ampullary and tuberous electroreceptor organs [29].
Capacitive switches evoked a SOR in 45% of all stimuli
(70 switches, 32 SORs). In comparison, purely resistive
switches (from a short to an isolator) under otherwise
identical conditions lead to SORs in 55 out of 64 cases
(86%; 64 switches in 4 fish). SORs caused by capacitive
switches were less frequent and also lower in amplitude
compared to those caused by purely resistive switches
(Mann-Whitney U-test, Z = -2.5, p < 0.011; Fig. 6A). In
contrast to these differences, the novelty responses evoked
by the two types of stimuli were indistinguishable in
amplitude (t-test, t = 1.8, p = 0.08) and latency (t-test, t =
1.70, p = 0.11).
The above data suggests that SORs can be elicited by the
active electric sense alone, because purely capacitive
switches were sufficient to evoke SORs.
However, the higher likelihood of evoking an SOR with
purely resistive switches indicates an additional involvement of the ampullary sensory system in mediating SORs.
Recording ampullary receptor activity in response to both
purely resistive and purely capacitive changes showed that
these receptors (n = 3) responded to purely resistive
switches, especially from a shunt to a high resistance (Fig.
6C1). Switching from large to small capacitances, however, did not elicit any changes in receptor activity (Fig.
6C2). Likewise the control, where no change in the resistive load occurred, i.e., switching between two identical
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resistances, did not result in any reproducible modulations of the ongoing discharge rates (Fig. 6C3).
duration) that were either presented in between successive
EODs or within the time period during which one or several EODs were emitted. Switches between EODs are exafferent stimuli and as such only influence the passive
electrosensory system, whereas switches including EODs
are reafferent and thus activate both the active and the passive electrosensory pathways. In accordance with the data
shown above, SORs as well as novelty responses were
most reliably evoked by reafferent stimuli (see Fig 7).
Thus ampullary receptors could potentially contribute to
the SOR. To further test if DC-potentials might cause
SORs, we conducted experiments, in which the dipole was
used to deliver weak DC potentials. If the delivered DC
was of comparable amplitude to that measured in
response to purely resistive switches, SOR and NR probability were low (see Fig. 7). Hence it is unlikely that the
DC-potentials of the resistive switches alone caused
motor responses. Further evidence for this comes from
supplementary experiments where the EOD amplitude
was shunted (decrease of EOD amplitude by 80%). Under
these conditions, SORs were still evoked by resistive
switches. With such a reduced electric field, the mormyromasts are expected to be unresponsive, so the observed
SORs are most likely due to the ampullary system, which
is not affected by the shunting.
In summary, we have shown that the active electrosensory
system is the principal modality leading to Schnauzenorgan responses; however, our data also imply that passive
or multimodal electric stimuli might additionally contribute to some degree.
Comparison to the novelty response
In a separate set of experiments (N = 7) we compared the
probability of SORs and the amplitude of the novelty
response. The stimulus protocol in these experiments
deviated from the standard paradigm: switches from a low
resistance baseline (10Ω) to pre-defined levels of higher
resistance occurred every 6 seconds and lasted only 500
ms. Each step thus resulted in a different amplitude
The above data strongly suggests that the main sensory
channel mediating the Schnauzenorgan response is active
electroreception. To further substantiate this claim, we
compared the responses to short switches (40 or 200 ms
***
C 1.0
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to beginning
to peak
toff
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Schnauzenorgan response
Figure 5 aspects of the SOR
Temporal
Temporal aspects of the SOR. Latency of the novelty response and the Schnauzenorgan response obtained using highspeed video analysis with one fish (128 frames/s). For both responses data are presented with respect to the beginning of a
response and with respect to the peak. A. Latency of the novelty response for on-responses (grey boxes) and off-responses
(black boxes). B. Latency of the SORs with respect to the time of a change in dipole resistance. C. Latency of the SORs relative
to the time of the first EOD following a change in the dipole-objects resistance. In all cases on- and off-responses were significantly different from each other (Mann-Whitney U-test: p < 0.01). A legend to the parameters displayed in A-C is shown at the
right hand side of the figure.
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paradigm as above. Due to the short duration of the stimuli, predominantly on-responses were evoked. As
expected, novelty responses habituated within a session of
16 stimulus presentations (Fig. 9B). SORs habituated with
a comparable time-course, further strengthening the
direct relationship between electrosensory stimuli and the
SOR (Fig. 9A).
p
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Figure 6 and ampullary recordings
Controls
Controls and ampullary recordings. A, B. Box-andWhisker plots showing the latency (A) and the amplitude (B)
of the SOR for a single fish presented with changes in capacitance of the dipole-object (white bars, n = 34 stimuli), and
mean data of four fishes where stimuli consisted of changes
in object resistance (32 stimuli). C. Ongoing discharge rate of
an ampullary receptor in response to changes in resistance
(C1), capacitance (C2) and in response to the control stimuli
(no change, C3). Note that the receptor responds with a
transient increase in spike rate only to a change in object
resistance and that this response is strongest for the return
to the shunted dipole-object. The inset in C1 shows a short
spike sequence.
change of the local EOD amplitude. Both the amplitude
of the novelty response and the probability of SORs
increased with increasing the switch-amplitude (Fig. 8A).
This relation only was found for resistive stimuli. Both,
novelty response amplitude and the probability of a SOR
were low when capacitive stimuli of various strengths
were presented, but future experiments are needed to corroborate this preliminary result.
The above data show that both NR and SOR scale in their
amplitude and probability with the change of the local
EOD-amplitude (reafferent stimulus). To investigate if
both behaviours must be regarded as independent processes, we next analysed the correlation between SORprobability and NR-amplitude (Fig 8B). For this analysis,
data of several experiments were combined, documenting
a weak correlation between both motor responses. This
suggests that the two behaviours might occur sequentially
and may be regarded as indicative of an early object detection system (NR), followed by an object exploration system expressing itself in an orienting behaviour (SOR)
during a period of sustained high sampling of the environment.
Previous studies had shown that the novelty response
habituates [16] when repetitive stimuli are presented. We
therefore tested the effect of repeated stimulation on both
the SOR and the novelty response using the same stimulus
It is well established that some electric fish can respond to
changes in their environment with a change in the rate of
their EODs [16,19,22,26,30,31]. These novelty responses
can be evoked by all sensory modalities. Here we show
that novelty responses caused by changes in the impedance of an object located near the Schnauzenorgan can be
accompanied by a previously un-described motorresponse, the Schnauzenorgan response. Following a novelty response, fish show a quick movement of their
Schnauzenorgan towards or away from the object. Both
SOR and novelty response probabilities scale with the
change in the EOD-amplitude.
Control experiments show that movements of the
Schnauzenorgan also occur spontaneously. However,
spontaneous movements are weaker (degree of deflection
of the Schnauzenorgan) and occur only in about 16% of
the control trials and in 2% of the trials used to estimate
the false-alarm rate. The comparatively high probability of
evoking SORs with the control stimuli probably reflect the
presence of the weak DC fields associated with the
switches. Responses to real changes of the impedances of
the dipole-objects occurred much more reliably. Thus,
SORs can clearly be distinguished from spontaneous
movements and represent a true sensory-motor response.
SORs and stimulus location
SORs depended on the rostro-caudal position of the stimulus object as well as on its lateral distance to the skin. The
range of about 12 mm within which SORs were evoked
above chance level indicates a strong dependency of the
SORs on the EOD-amplitude, which declines exponentially with increasing distance. A shunt of the dipole
placed 1 mm from the skin increase the local EOD-amplitude by 172%, whereas at 15 mm this increase declined to
7% and to 1% at 25 mm. Based on this data, a threshold
of a few percent modulation of the EOD amplitude can be
estimated for the SOR. The present analysis suggests that
SORs occur as all-or-nothing like events, but a more thorough analysis on the relationship between stimulus location and strength of the SOR based on high-speed videos
is needed to confirm this in future experiments.
While our systematic mapping of the response was
restricted to the head region of the fish, experiments with
the objects placed at the trunk of the fish never evoked
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A
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B
reafferent
observation). We can not rule out, however, that these
modalities might evoke SORs under different conditions
(e.g., higher intensities). Hydrodynamic or tactile stimuli
were not investigated. Given the abundance of electroreceptor organs in the head region, we think it very likely
that SORs are only evoked by local electrical stimuli.
exafferent
Frequency (Hz)
Frequency (Hz)
1s
30
20
10
0
-3
-2
-1
0
1
2
3
30
20
10
0
-3
-2
Time (sec)
C
-1
0
1
2
3
Time (sec)
D
SOR
n=134
n = 82
n=35
Probability (%)
Frequency (Hz)
80
30
20
60
40
20
10
0
-3
To which extend do the sub-modalities of the electric sense
contribute to the SOR?
Both amplitude and waveform modulations were effective in evoking SORs, although amplitude modulations
seem to drive the response more efficiently. Mormyromasts have two types of electroreceptor cells, the A- and
the B-cells [32]. Theoretically, the response to both resistive and capacitive changes of object properties could be
conveyed by B-cell input alone. If input from the A-cell
system is also involved in the SOR remains to be clarified.
-2
-1
0
Time (sec)
1
2
3
0
reafferent
exafferent
DC
Figure
Exand 7
reafferent stimuli and the SOR
Ex- and reafferent stimuli and the SOR. A, B, C. Comparison of the EOD pulse behaviour for short switches from
10 Ohm to an open circuit. The response to this stimulus is
presented according to whether the switch occurred during
the occurrence of EODs (A, reafferent) or in between two
consecutive EODs (exafferent, B). In C data are presented
for all switches that caused a SOR, irrespective whether the
stimulus was ex- or reafferent. The upper trace indicates the
recording of the local EOD and the stimulus applied. The
raster below the stimulus represents all EODs associated
with a given stimulus paradigm, and the histogram at the bottom shows the mean inter-EOD frequency. Stimuli not associated with a novelty response are highlighted in grey in B
and C. D Bar-plot showing the probability at which stimuli
evoked no response (dark grey), a novelty response (light
grey), a SOR but no novelty response (green), or both
responses (red). Data are based on three fishes. Note that
reafferent stimuli were most efficient in evoking SORs and
novelty responses, whereas exafferent stimuli and weak DC
pulse had an overall low probability for eliciting either form
of behavioural responses.
It is conceivable that weak DC-potential were present
when the dipole-objects were shunted or disconnected,
which could explain the documented responses of the
ampullary system. Switching between two capacitances (1
μF and 1 nF) effectively prevents DC-potentials and hence
recordings from ampullary receptor organs were not
responsive. However, SORs were still evoked under these
conditions, albeit at lower probability. Our experiments
on comparing the effectiveness of ex- and reafferent stimuli
in evoking SORs and novelty responses suggest that the
predominant stimulus leading to both responses was reafferent and thus based on the mormyromast system. Exafferent DC-potentials only caused SORs or NR at
amplitudes exceeding those due to DC-potentials in our
setup. We therefore conclude that the mormyromast system is involved in triggering SORs and that the ampullary
system also contributes to it, probably in a multimodal
manner. Further experiments addressing the contribution
of either modality more directly are needed to resolve this
question unequivocally.
SORs. In these experiments, the trunk was only partially
covered. We therefore conclude that particularly the
Schnauzenorgan is the focal region for evoking SORs, but
can not exclude that SORs might also be evoked form
other regions in freely behaving animals.
SORs and the Novelty response
The amplitude of the novelty response and the SOR-probability scaled with the change in the local EOD. Thus, SOR
probability is correlated with the amplitude of the novelty
response. This establishes a perceptual link between both
behaviours, where stronger changes in the electric signal
will evoke stronger behaviours. Again, our data indicates
that EOD-amplitude modulations in the order of a few
percent will induce a SOR.
Which sensory modalities contribute to the SOR?
Novelty responses can be evoked by several sensory
modalities and by multimodal stimuli. This contrasts with
the SOR, which was only evoked by electrical stimuli. Neither acoustic nor visual stimulation were effective in evoking SORs (but did evoke novelty responses, unpublished
Novelty responses always occurred at shorter latencies
than the SOR, usually after the first EOD following a
change. The latency of SORs varied between 50 and 280
ms, thus SORs occurred later than the novelty responses.
SORs surely are the result of sensory-motor integration on
a relatively short timescale, yet take much longer than C-
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starts or the amazingly short and precise orienting
response of Archerfish to their prey [33,34]. This and the
fact that SORs were non-directed, indicate that the SOR is
not a reflex, which always is unipolar, i.e. an orientation
is always to be observed towards the stimuli or an escape
from the stimuli.
SOR occurrence also was more localised, with a focus on
the Schnauzenorgan region, further emphasising the role
of the SO as an electrosensory fovea. SORs were rarely
seen when stimulation occurred caudal to the mouth and
control stimuli presented at the trunk never elicited SORs,
whereas novelties were evoked at all position tested
(unpublished observation).
While we have no data concerning the sensory-motor
loop involved in the SOR, it is interesting to note that the
trigeminal nerve is hypertrophied in Mormyrids [35],
including Gnathonemus, where a large branch innervates
the Schnauzenorgan [36-38]. The presence of a motor
response in conjunction with electrosensory input
strongly suggests reciprocal innervations between the
motor nuclei and sensory areas, which will be worthwhile
to investigate further. We speculate that such connections
should be present between medullary centres processing
direct sensory input from both the electroreceptors and
the trigeminal nuclei.
The correlation between the SOR-probability and the NRamplitude might indicate that both motor behaviours are
part of a sequential process that is triggered by the detection of a change in the environment. This initial detection
then leads to a novelty response, followed by a SOR provided that the stimulus was strong enough. Thus, one
could attribute the NR to an early detection phase during
object inspection and the SOR together with an increased
EOD-frequency to an exploration phase.
At present it is impossible to decide whether the two
behaviours are triggered independently by a stimulus
change in the environment or whether they are triggered
sequentially, i.e., a novelty response triggers the SOR.
A further parameter that has been investigated regarding
the novelty response is habituation. Similar to the novelty
response, the SOR does habituate if stimuli are presented
repeatedly.
SORs and natural movements of the Schnauzenorgan
SORs were undirected single movements of the
Schnauzenorgan, but up to seven consecutive movements
were observed. Theses were reminiscent of the rhythmic
scanning movements of the Schnauzenorgan, which these
fish perform during foraging [39,40]. Irrespective whether
a single or multiple SORs were evoked, SORs were quick,
100
100
A
B
80
Probability NR
Mean Probability
80
60
40
20
SOR
Novelty
0
10
100
1000
10 4
Resistance (Ohm)
10 5
10 6
60
40
20
N=65; r²=0.23, p<0.001
0
0
20
40
60
80
100
Probability SOR
Figure
SOR
and8 Novelty depend on the amplitude change of the EOD
SOR and Novelty depend on the amplitude change of the EOD. A. Scatter plot of the relationship between the probability of the novelty response (cirlces) and the SOR (squares) with regard to the amplitude of the switch. The baseline resistance prior to any switch was 10 Ohm. Note that both responses scale with the amplitude change of the dipole object, which
corresponds to the amount of change in the local EOD amplitude. B. Scatter plot of the relation between the mean probability
of evoking a SOR and the respective probability of the novelty response. Error bars in A give S.E.M. (N = 7). Data for both figures were obtained with the dipole-object being placed at the middle of the SO at a distance of 5 mm.
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B
100
.5
80
6.0
N=24; r²=0.63, p<0.01
60
40
20
N=24; r²=0.48, p<0.05
Probability Novelty
Probability SOR
A
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100
.5
6.0
80
60
40
20
N=24; r²=0.5, p<0.01
0
2
4
6
8
10
12
14
16
Trial
2
4
6
8
10
12
14
16
Trial
Figure 9 of the SOR
Habituation
Habituation of the SOR. A. Probability of evoking the SOR in a series of 16 consecutive trials (inter-trial interval 6 s, see
inset). The filled circles show the data for on responses, while off responses are shown as open circles. Note that stimuli were
much shorter than those used for the general description of the SOR, which is reflected in the absence of "off" responses. B.
Mean amplitude of the novelty response as a function of the number of trials for the data shown in A. In A and B, responses
were evoked by a switch that lasted 0.5 s, which was sufficiently short to evoke only a single novelty response and mainly onresponses of SORs. Error bars in B are S.E.M.
with angular velocities reaching 89.4 ± 34.3°/sec. This
value is lower than the natural scanning movement
observed in freely moving animals, where values of up to
500°/sec have been reported [28]. However, these data
were based on regular video analysis at frame rates of 40
ms and an analysis of freely moving fish using high-speed
videos (128 frame/sec) indicates that natural scanning
movements are comparable in their speed to evoked
SORs.
The chin region of Mormyrids in general is characterised
by a high density of electroreceptors, a phenomenon that
has been referred to as an electric fovea [27,39]. The rhythmic-scanning movements might help to overcome a
severe limitation of such an electrosensory fovea. Reserving highest acuity to a small portion of the sensory mosaic
requires orienting mechanisms, which allow the animal
to actively explore the environment by moving the foveal
region. In foveated vision for example, pursuit eye movements and saccades overcome this limitation. Similarly
the scanning movements of the SOR will increase the area
that is analysed by the electrosensory fovea.
Possible functions of the Schnauzenorgan-response
The platypus (Ornithorhynchus anatinus) is an passive electrosensory animal [41], which shows a scanning behaviour with its beak when searching for food. Behavioural
experiments on freely swimming platypus have shown
that they also turn their head in a reflex-like manner
towards new electrical stimuli. In most cases, this head-
turning was followed by a complete turning of the body
towards the source [42]. Similar to the Schnauzenorgan of
G. petersii, the electroreceptors of platypus are located on
the beak, with the highest receptor organ density at its
edges [43].
Yet a different example of electrosensory foveation in the
passive electrosensory system can be found in paddlefish
(Polyodon spathula), which have the highest density of
ampullary receptors on their rostrum [44]. These fish
swim in an undulatory manner that imparts a lateral oscillating motion to their rostrum. These saccade-like
motions of the rostrum are interpreted as an adaptation
for prey detection, since they increase the width of the
electrical scan field. In contrast to the SOR, however, these
movements are rather slow. If a potential prey is encountered, however, a fast and precise turning of the rostrum
takes place.
All examples mentioned above perform rhythmic scanning behaviours with an elongated part of their body covered densely with electroreceptor organs (the rostrum, the
beak, or the Schnauzenorgan). These areas can be
described as electric foveae [27,45,46], which require a
scanning mechanism to extend the range of a small aspect
of the sensory world beyond the actual aperture of the
fovea. Therefore, we consider the rhythmic scanning
movements that occur during foraging to constitute an
active extension of the area of the electric environment
that can be explored by the electric fovea. If the animal
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encounters a novel object during scanning, the undirected
oscillating movements change to active orientation
towards the new stimulus. In both the platypus and the
paddlefish, this orienting response is highly accurate and
based on passive electrolocation. This is different to the
SOR of Gnathonemus, because these fish also have an
active electric sense and therefore additionally employ
active electrolocation.
Whether the SOR is guided towards or away from a source
might be context-dependent. Alternatively, the SOR might
be non-directed because of the relatively small size of the
Schnauzenorgan. Due to the small fraction of the electrical field that can be explored with this protrusion, it could
be that a quick, source directed turning of the
Schnauzenorgan within a DC-field is not possible since it
would require an almost instantaneous computation of
the electric field in order to determine its source. In contrast to the rostral appendages of the platypus and the
paddlefish, the Schnauzenorgan of Gnathonemus might be
too short and too thin for an accurate estimation of the
source's direction. Instead, some kind of "approach algorithm", which involves the comparison of the field intensities at different positions within the field, might be
required. Independent from the above argumentation,
relative movements are know to enhance the ability to
detect DC-potentials by the ampullary system [47].
Conclusion
We here present the first report of a new motor response
to electric stimuli in the weakly electric fish, Gnathonemus
petersii. This response consists of one or several fast movements of the Schnauzenorgan which are evoked by
changes in the nearby electric environment. We show that
while both sub-modalities of the electric sense, i.e., active
and passive electrolocation, can evoke this motor
response, the contribution of the active sense dominates.
In contrast to the well-described novelty response, the
SOR is of longer latency and is restricted to electric stimuli
in the proximity of the Schnauzenorgan. The
Schnauzenorgan thus can be considered as an electric
fovea serving as an active electrical probe in environmental imaging. Previously, we could show that several adaptations exist that optimise the electric field for active
electrolocation [40,48] at this foveal [27,39] appendage.
We propose that since SORs and novelty responses can be
evoked in restrained animals, they offer a unique opportunity to extend the study of sensory-motor interaction to
electrophysiological studies comparable to the well established eye movements or the vestibular-ocular reflex
[49,50]. To this end, a better understanding of the trigeminal system and its interaction with pre-motor areas is
required.
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Methods
Twenty-four fish (Gnathonemus petersii, Günther 1862), all
purchased from Aquarium Glaser (Rodgau, Germany),
were used in this study. Fish were housed in two 100 litre
tanks of constant temperature (22-24°C) and electrical
conductivity (100 to 120 μS/cm).
General methods
Before animals could be transferred to the experimental
set-up, they were anaesthetised by immersion in MS-222
(tricaine methane sulfonate; Sigma, St. Louis, MO, USA;
concentration 306.17 μmol l-1) and transferred to a
holder. Here, the fish's trunk was lightly restrained. The
animals head was not covered from the pectoral fin to the
SO. The holder was placed in a tank (30 × 19.5 × 18.5 cm3
LxWxH) with fresh water (123 μS cm-1), where the fish
recovered from anaesthesia within a few minutes.
A video camera (Sony DCR-HC 40E) was placed above the
tank and images of the animals were acquired and stored
at 22 frames/s with a PC running Viewer2 (BIObserve,
Bonn, Germany). A pair of carbon electrodes on the inside
wall of the tank between the head and tail of the fish was
used to record the electric organ discharges (custom-built
amplifier, band pass filtered 10 Hz-10 kHz). EODs were
stored using a CED digitiser (Cambridge Electronic
Design, Micro 1401 12 bit, 200 kHz, analogue-digital converter) and Spike2 software (Cambridge Electronic Design
Ltd).
Stimuli used to obtain a general characterisation of the
SOR (standard stimulus paradigm) were delivered by two
passive dipole-objects, each consisting of two carbon
poles (diameter 5 mm distance between pools: 9 mm) in
Perspex tubing in the form of an inverted T. The carbon
poles were connected to a switch that allowed altering the
resistance or the capacitance between the poles. The
dipole objects were placed with the carbon poles oriented
perpendicular to the midline of the animal (see Fig. 1).
Except for the tip of the Schnauzenorgan, where the orientation of the dipole-object was along the rostro-caudal
axis of the animal, two such dipole-objects were placed at
equal distances at opposing sides of the animal. Distances
between dipole-object and the skin of the fish were 1, 3,
5, 7, 10, 12 and 15 mm, and placement of the objects
along the length of the animal is shown in figure 1. If at a
given position novelty responses or SOR could no longer
be evoked, we did not test the responses at further distances.
The resistance of each dipole-object was changed independently - using a manual switch - from a short circuit to
an infinitive resistance (open circuit) and back again to
the short circuit condition. These changes in resistivity of
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the object are referred to as a trial. Trials lasted between
three and six seconds and consisted of an on-stimulus (initial change in object impedance) and an off-stimulus
(return to the shunted condition). Note that "on" and
"off" refer to an increase and a decrease in the dipole
object's impedance, respectively. Between successive trials
the dipole-object was kept in the "shunted" condition for
a variable length of time (40-80 seconds). Each switch in
resistivity of an object generated a trigger pulse that was
recorded in Spike2 and Viewer2. Responses to stimuli
were tested in four fish for all object positions and distances. At each position, eight stimuli and one control
stimulus were presented. Controls consisted of no
changes in the resistive load, i.e., switching was between
two identical resistances. These controls therefore tested
for the presence of an animal's response to possible weak
mechanical or acoustic stimuli associated with switching,
as well as for possible DC-potential effects. Eight consecutive trials together with one control trial are referred to as
a session, and a maximum of six sessions were gathered
with a single fish per day. Between each session the objects
resistances were not altered for 10 minutes.
Data Analysis
Novelty responses consist of a shortening of the intervals
between consecutive EODs. Following methods that
enhances the contrast between fluctuations of EOD pulse
intervals and accelerations related to stimulation established by Hall and colleagues [19], intervals between suc-
cessive EODs (Δ) were calculated ( Δ = t EOD i − t EOD i −1 ).
The instantaneous acceleration (a) was calculated next as
the distance between intervals (a = Δi-1-Δi). The mean
acceleration ( a ) for the eight trials within one session was
calculated. Of these we subtracted the mean acceleration
of the 20 EODs prior to a switch and divided this by the
standard deviation (σ):
a −a
Z= i
s
The Z-data thus obtained provided a statistical measure of
the amplitude of the novelty responses where z-scores
below 1.96 occur above chance level (p < 0.05 see Fig. 1B).
The maximal deviation of the z-transformed data within 5
EODs after a switch was taken as the peak amplitude of a
novelty response. The latency to this peak response was
measured both with respect to the time of switching
dipole properties and with respect to the first EOD following this change in resistivity. Similarly, we measured the
latency to the first significant deviation of the transformed
data, i.e., to the beginning of the novelty response.
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The videos of the animal's movements were analysed with
custom written software (OMA; M. Hofmann, Bonn, Germany). This resulted in a frame-by-frame determination
of the displacement of the SO. These position-data were
analysed in a similar way as described for the novelty
responses, i.e. the position data of the SO were z-transformed. The baseline data used for calculating the means
and standard deviations were obtained from the 120
frames (or 4.8 s) prior to every switch. This amount of
time proved to be sufficient to make the analysis robust
against minor changes of the position of the SO.
From the z-transformed data we determined the amplitude of the Schnauzenorgan-responses (SOR), defined as
the peak of the transformed data. The latency of this peak
as measured with respect to the stimulus onset as well as
to the time of the first EOD following a stimulus. This
analysis is restricted to all laterally directed Schnauzenorgan movements, since downward movements of the
Schnauzenorgan could not be quantified from our videos.
In those cases where high-speed videos (128 frames/s)
were obtained, the latency of the response was additionally measured with respect to the start of a response, i.e.,
the first crossing of the threshold level (see Fig. 2C). The
number of individual SORs and their directions in
response to a single stimulus were noted, i.e., we determined whether the SO moved towards or away from the
dipole object. Likewise, the false-alarm rate (and its
amplitude) was calculated for a fictive switch of the
dipoles impedance 50 EODs prior to the actual changes of
the dipoles impedance.
Experiments on modalities involved in the SOR and
habituation
Controls with shunted EODs
In order to diminish the amplitude of the EOD produced
by the fish and thereby impair active electrolocation, the
tail of the fish was wrapped in aluminium foil. This
caused a short circuit of the electrical organ. In these
experiments, the two dipole objects were positioned at a
lateral distance of 3 mm at the middle of the SO, and novelty responses and SORs were evoked, investigated, and
analysed in the same manner as described for the standard
paradigm above.
Controls using capacitive objects
Experiments were similar to the standard paradigm,
except that the switch in object properties was between
two capacitances, i.e. a switch from a 1 μF to a 1 nF capacitor. This corresponded to a change from a very large to
very small object impedance, but the capacitances constituted a filter for DC currents. As in the first control, these
measurements were conducted with the dipole objects
positioned at a lateral distance of 3 mm at the middle of
the Schnauzenorgan.
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Controls applying re- and exafferent stimuli
Experiments were similar to the standard paradigm, but
the switch-duration and timing was set by an external
waveform generator (Accupulser, WPI). The duration of
switches in a range between 40 and 200 ms, depending on
the discharge rate of a fish (N = 3), and the inter-switch
interval was set to 40 seconds. Probabilities of SORs and
NR were scored with regard to whether the switch
included one ore more EODs (reafferent) or no EODs
(exafferent). As in the first control, these measurements
were conducted with the dipole objects positioned at a lateral distance of 3 mm at the middle of the Schnauzenorgan. In similar experiments the waveform generator was
used to apply weak DC-potentials using a stimulus isolation unit (WPI Linear Isolator 395) via the dipole object.
Habituation and relation to EOD properties
Experiments addressing habituation of the SOR deviated
from the standard paradigm in that switches lasted only
0.5 seconds and occurred at a fixed inter-stimulus interval
of 5.5 seconds. This ensured a single novelty response was
evoked only. These experiments were conducted with the
dipole placed 5 mm away from the medial part of the
Schnauzenorgan.
Using the same approach we tested the influence of the
amplitude of the switch on the strength and probability of
the novelty response and the SOR. In these experiments,
10 consecutive switches from 10 Ohm to defined higher
resistances were tested.
Recordings from ampullary receptors
These experiments were conducted in a separate tank (27
× 13 × 8 cm3, 100 μS cm-1) with fish that were curarized
and artificially respirated. Fish initially were anaesthetised
(MS-222, 306.17 μmol l-1) followed by an injection of 30
μl Pancuronium (solution 4 mg Pancuroniumbromid per
2 ml, thinner 1:400, Organo Teknika). Afterwards the fish
was rigidly placed in the tank where it was connected to
an artificial respiration system. Recording technique and
animal handling was similar to that described elsewhere
[51].
Statistics
If not stated otherwise, data are given as means with their
standard deviations. All data were analysed for normality
and depending on the results, parametric (ANOVA and ttests) or non-parametric test (Mann-Whitney U-test and
Kruskal-Wallis test with Dunn post hoc analysis) were performed. When distributions (tested by chi2) or means
(tested by t-test) of data for on and off responses were not
different, data were pooled. All statistics were performed
using SPSS and Matlab.
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Competing interests
The authors declare that they have no competing interests.
Authors' contributions
JE and SN carried out most of the laboratory work and
data analysis and drafted the manuscript. TR carried out
experiments comparing the novelty response and the
SOR. JE and VDE designed the study and wrote and finalized the manuscript. All authors read and approved the
final manuscript.
Acknowledgements
This work was partially supported by grants from the German Science
Foundation (DFG, EN 826/1-1; Em 43/11-1,2,3) and the European Commission (FET, ANGELS contract 231845). We thank Dr. João Bacelo as well as
three anonymous reviewers for highly valuable comments on an earlier version of this manuscript and Dr. Gabriele Uhl for advice on statistics.
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