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First published online September 5, 2008
Journal of Experimental Biology 211, 2919-2930 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016154
Multisensory enhancement of electromotor responses to a single moving object
Department of Biology, University of Virginia, Charlottesville, VA 22904, USA
* Author for correspondence (e-mail: srp3g{at}virginia.edu)
Accepted 4 July 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: electrosensory, fish, integration, mechanosensory, motion sensing, multimodal, niger, novelty response, object recognition, supralinear
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), and its influence extends across a wide range of taxa.
Humans use the optimal integration of visual and haptic information to
determine the orientation of an object
(Helbig and Ernst, 2007).
Drosophila hone visually guided compensations in flight control with
mechanosensory input from their halteres
(Sherman and Dickinson, 2004).
Barn owls integrate auditory and visual information to produce bimodal head
saccades with the shorter latency of auditory saccades and the greater
accuracy of visual saccades (Whitchurch
and Takahashi, 2006). The basic rules governing multisensory
integration are fairly well established: (1) facilitation occurs when
cross-modal stimuli are spatiotemporally aligned to a receptive field
(Meredith et al., 1987;
Meredith and Stein, 1996); (2)
the magnitude of multisensory enhancement is inversely related to the
effectiveness of its unisensory components
(Stanford et al., 2005) and
(3) the perceptual weight of each sensory modality during a multisensory
experience is inversely related to the variance in the stimulus
(Ernst and Banks, 2002).
Weakly electric fish possess three types of sensory organs structured in
arrays with overlapping receptive fields. They are the tuberous electrosense
(Tub), ampullary electrosense (Amp) and mechanosensory lateral line (LL). Each
sensory modality simultaneously encodes unique and interrelated information
about objects in the near-field environment
(Nelson et al., 2002).
Nonetheless, the importance of multisensory integration across electrosensory
and mechanosensory arrays during moving object recognition is not yet
established. Behavioral (Ciali et al.,
1997; Moller,
2002; Moller et al.,
1982; von der Emde and
Bleckmann, 1998) and neurophysiological
(Bastian, 1982;
Bleckmann and Zelick, 1993;
Prechtl et al., 1998) evidence
indicates that weakly electric fish are multisensory integrators.
Sensory modalities
Weakly electric fish are most notably recognized for their high-frequency,
active electric sense performed by the tuberous sense organs. Active
electrolocation results from the detection of localized distortions in the
self-generated electric field that are caused by nearby objects with an
electrical impedance different from the surrounding water
(Gomez et al., 2004;
Heiligenberg, 1973). The
tuberous sense is capable of determining the distance
(von der Emde et al., 1998),
3-D shape (von der Emde and Schwarz,
2000) and electrical properties of objects
(Aguilera and Caputi, 2003;
Caputi et al., 2003). Weakly
electric fish also possess a low-frequency, passive electric sense performed
by the ampullary sense organs. Passive electrolocation results from the
detection of a transdermal potential caused by the presence of objects that
possess a bioelectric field (Wilkens et
al., 2002). The ampullary sense is capable of determining prey
location (von der Emde and Bleckmann,
1998) and proximity to a shelter
(Rojas and Moller, 2002).
Weakly electric fish also have the mechanosensory lateral line system. The
lateral line is sensitive to water movement, which can be caused by a nearby
moving object (Mogdans and Bleckmann,
1998). The lateral line system is capable of discriminating an
object's directional motion, speed, size
(Vogel and Bleckmann, 2000)
and location (Coombs et al.,
2001).
Novelty response
The so-called `novelty response' (NR) in pulse-type weakly electric fishes
is a stimulus-induced transient increase in electric organ discharge (EOD)
rate (Aguilera and Caputi,
2003; Barrio et al.,
1991; Hall et al.,
1995) with psychophysical properties akin to orienting responses
in mammals (Post and von der Emde,
1999). The NR is a tractable behavior for measuring perception,
since it is reducible into scalar values and persists under curarization.
The NR may temporarily augment vigilance because it increases the sampling
rate of the tuberous electrosensory system. The energetic cost of the electric
fish brain is exceptionally high (Nilsson,
1996), and, in hypoxic environments, pulse-type electric fishes
will lower the rate and/or amplitude of their EOD
(Crampton, 1998).
Consequently, the regulation of the NR may ultimately impact the survival of
electric fishes. Therefore, the NR probably indicates the perceived value and
saliency of a stimulus. In fact, the probability and amplitude of the NR are
directly related to electric image contrast
(Caputi et al., 2003) and light
intensity (Post and von der Emde,
1999). NR habituation is inversely related to interstimulus
interval (Barrio et al., 1991;
Caputi et al., 2003;
Post and von der Emde,
1999).
The NR of the mormyrid electric fish Brienomyrus
(Brevimyrus) niger contains two components: `acceleration'
and `scallop'. Scallops and accelerations are fairly similar except that
scallops contain a short sequence (4–6 intervals) of EODs with a peak
frequency much higher than accelerations
(Carlson, 2002;
Serrier and Moller, 1989). We
utilized the NR to evaluate the role of multisensory integration in moving
object recognition. By manipulating the fish's EOD and surrounding environment
we were able to selectively stimulate three sensory modalities with a single
moving object. Principally, we discovered that multisensory NRs have a
significantly larger duration and magnitude than the linear sum of their
component unisensory NRs. Additionally, multisensory NRs have a significantly
greater amplitude, probability and rate of scallop production than their
component unisensory NRs.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Experimental setup and stimulator
The experimental tank was a 50 cm length x 50 cm wide aquarium with a
height of 15 cm. Water temperature was maintained at 26°C with a
conductivity ranging from 70 to 110µscm–1. The immobilized
fish was supported by a 12 cm-long, narrow platform with a foam strip on top
that cradled its shape. Aerated water was passed over its gills through a
fitted glass tube placed inside its mouth. In intact B. niger, EODs
occur 2.5–4.5 ms after the first negative peak of a triphasic volley of
the electromotor neuron (EMN). EMN activity was monitored by placing the
caudal peduncle inside a piece of nylon tubing containing a pair of silver
wire electrodes. The EMN signal was amplified 10,000 times, low-pass (1.6 kHz)
filtered and sent to a Schmitt trigger that drove an event timer to record the
timing of its activity with 1 µs resolution (model ET1, Tucker-Davis
Technologies, Gainesville, FL, USA). Time stamps were collected with a Matlab
program for off-line analysis.
The experiment took place in a light-shielded environment. Luminance level in the room during stimulus object presentation was 4x10–8 Wcm–2 (UDT instruments, Baltimore, MD, USA), and the experimenter's ability to even roughly visualize the experimental setup was impossible without continuous dark adaptation for approximately 30 min. To prevent the fish from dark adaptation, a large fluorescent ceiling light was turned on and, from a short distance, a 40 W lamp was directed at it between periods of object stimulation.
The stimulator consisted of a vertically oriented center axis with an L-shaped plastic arm connected to the base of the axis (Fig. 1). The vertical portion of the L-shaped arm (9 cm length, 6.5 mm diameter) served as the stimulus object. The top of the stimulus object was above the fish's dorsal surface. The horizontal portion of the L-shaped arm was approximately 6 cm below the fish's ventral body surface and extended 12 cm out from the center axis. The water surface of the tank was kept more than 1 cm above the stimulus object to minimize surface waves. A DC motor (Oriental Motor Corp., AXU series, Tokyo, Japan) rotated the center axis on ball bearings via a pulley system. Object speed was calculated from the frequency of a square pulse produced by the DC motor's speed control unit. Starting at an angle of 180 deg. from the fish's lateral body surface, each 360 deg. rotation of the stimulus object was initiated by a software-triggered square pulse and was terminated by the interruption of an infrared hardware switch.
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The local distortion of the fish's electric field caused by the plastic stimulus object was measured with the 3 mm-wide fork electrode positioned 5 mm away from the fish's lateral body wall and 1.3 cm from the stimulus object. The replacement electric field was generated by a function generator and consisted of a biphasic pulse that approximated the duration and amplitude of B. niger's EOD. The mean reduction in peak-to-peak electric field amplitude was 1.6±0.7% (N=4) at a stimulus object distance of 2.1 cm from the lateral body surface.
Two insulated silver wires with bare tips were glued to opposing sides of the stimulus object so that the tips were directly facing the fish's lateral body surface at the object's minimum lateral distance (MLD). By flipping a switch on a battery, direct current was passed into the wires to create a DC electric field. A potentiometer connected to the battery allowed the voltage supplied to the wires to be adjusted. Selective delivery of the ampullary stimulus was controlled by the mechanical switch. Different strengths of the DC field were delivered, ranging from 200 to 600 µVcm–1 at a distance of 3 cm from the fork electrode.
A 6 mm-thick acrylic frame with a rectangular opening, approximately 10 cm long and 5 cm wide was placed between the fish and the moving object (Fig. 1). The frame was firmly clamped in place. A hard agar gel (5% agarose, Sigma Chemical Co., A0576, 8 mm thick, within 10% conductivity of water) was fitted tightly inside and clamped to the frame opening to securely block hydrodynamic stimulation of the lateral line. Electrical current could readily pass through the agar wall but water movement was obstructed. The agar gel could be removed from the acrylic frame, without displacing the fish, when lateral line stimulation was desired. The object's MLD from the fish was between 2.4 and 2.8 cm. The object traveled at a speed of 4.5–5.0 cm s –1.
Stimulus protocol
Each fish was presented with a specific stimulus only once, for a maximum
of seven different stimulus types including the control
(Table 1). For each stimulus
type presented, 10 identical 360 deg. rotations of the stimulus object were
delivered with a 10 s pause between them. Ten rotations of a single stimulus
type will hereafter be referred to as a `session'. The within-session stimulus
object MLD interval was approximately 26 s. There was a 10 min pause between
each session to reduce the effect of habituation. The different stimulus type
sessions were randomly ordered within two blocks. In the first block of
stimuli, the agar wall was present, and in the second block, the agar wall was
removed for the addition of lateral line stimulation. The sessions without
lateral line stimulation occurred first because although the agar wall was
relatively easy to remove without displacing the fish, fitting it back inside
the plastic frame was difficult and could interfere with experimental
protocol. At the beginning of every experiment, a control test was conducted
in which the agar wall was present and both of the electric fields were off.
If the fish did not respond with probability (see Data analysis) greater than
30% during the control, stimulus isolation was deemed successful, and the
experiment was included in the analysis.
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Data analysis
Time stamps of fictive EOD activity were converted into a series of delta
functions. These were then convolved with a Gaussian function, with a width of
one standard deviation set to 68.75 ms, to generate a spike density function
(SDF; Fig. 2C)
(Carlson and Hopkins, 2004;
Szucs, 1998). This width of
the Gaussian function was chosen because it provided an accurate
representation of NRs (relative to instantaneous frequency,
Fig. 2A) against the background
variation in EOD intervals. The result was a continuous, low-pass filtered
(23.5 Hz) function representing the EOD rate in units of pulses
s–1. The main purpose of using the SDF was to create a
continuous function of EOD rate to allow the arithmetic summation of
unisensory responses. The mean SDF and its time derivative [spike density
derivative (SDD); Fig. 2D] were
calculated across each session of 10 rotations. The mean SDF was evaluated
instead of single SDFs because it was often problematic to accurately
determine the start time and end time of a NR during a single rotation if the
fish had a tendency to scallop or displayed frequent spontaneous
accelerations. The mean SDF and SDD will be hereafter referred to as `SDF' and
`SDD', unless specified otherwise.
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;
Caputi et al., 1998;
Hall et al., 1995;
Post and von der Emde, 1999),
the period of time immediately before the start time was chosen to determine
baseline, in order to improve the accuracy of its measurement. The baseline of
each session was defined as the mean of the SDF over the final second leading
up to the start time. The end time was defined as the time of the first
negative-to-positive zero-crossing after the maximum SDD with a corresponding
SDF below a threshold level. The within-session threshold level was baseline
plus two standard deviations during the baseline period and was used to avoid
registering local minima as end time while the SDF remained high
(Fig. 2C,D). In cases where a
local minimum did not happen before the SDF returned to baseline, the time at
which the SDF intersected the baseline was chosen as the end time. The
duration of the NR was calculated by subtracting start time from end time. The
area of the NR was calculated as the integral of the baseline-subtracted SDF
from start time to end time. To compare multisensory and unisensory SDFs,
baseline was subtracted from the SDFs. The unisensory SDFs were then
arithmetically summed to compare with multisensory SDFs. In the special case
of Fig. 5, the duration and
area of the individual NRs were calculated using the aforementioned methods
applied to mean NRs.
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, where is the mean of the
standard deviations across the 10 individual SDFs during the baseline period.
Amplitude was calculated by subtracting baseline from the maximum value of the
NR. The number of scallops near the object's MLD was calculated using the
unfiltered EOD intervals. Scallops were counted as any string of EODs with one
or more consecutive intervals less than 30 ms and located between 1 s before
or 2 s after the time of the object's MLD. To determine if differences in
within-session response variation could explain multisensory enhancement, we
compared the standard deviations and coefficients of variation of the SDFs
(between start time and end time of the mean NR) among the stimulus types. To
estimate the within-session temporal alignment of individual NRs, we
calculated the standard deviation of the time of SDF maximum within the bounds
of the mean NR. The sample mean of the standard deviation will be expressed as
the symbol 
.
Within-subject (fish) differences among stimulus types were tested using a repeated–measures analysis of variance (ANOVA) with a Bonferroni correction for individual comparisons. Non-parametric tests for scalloping among the non-tuberous stimuli were performed with a sign test. Tests for covariance between scallop rate and NR magnitude were performed by calculating Pearson's correlation coefficient. A Shapiro–Wilk test was used for determining the normality of data.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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),
thereby resembling previous descriptions of the so-called `novelty response'.
However, B. niger would also scallop
(Serrier and Moller, 1989)
quite often. Therefore, the definition of novelty response in the current
study includes both accelerations and scallops. Area and duration were most strongly affected by multimodal stimulation. Fig. 3 compares baseline-subtracted SDFs for different combinations of multisensory and unisensory stimulation. Each row of graphs is from a different fish. In each example, the duration and area of the multisensory NRs are larger than their component unisensory NRs. Overall, the mean area and duration of multisensory NRs were 3.17 and 1.72 times larger than unisensory NRs, respectively. Multisensory NRs from each stimulus type had a significantly greater area than their component unisensory NRs (P<0.01, N=13–21; Fig. 4A). A significant difference existed for NR duration as well, except when comparing Tub+LL to LL (P>0.05, N=16; Fig. 4C). To help address response variation, Fig. 5 compares the within-session distribution of NR duration and area among three stimulus types from a representative fish. In this example, there is a clear distinction between the distributions of multisensory and unisensory responses. For this session, 6 responses to the Tub+Amp stimulation had a duration greater than 2 s (Fig. 5A). By contrast, only three responses to the Tub and zero responses to the Amp unisensory stimuli were of equivalent duration. Similarly, four of the responses to Tub+Amp stimulation had an area of more than seven pulses, while only one response to Tub and zero responses to Amp unisensory stimulation had an equivalent area (Fig. 5B).
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Fig. 3B,D,F compare the actual multisensory NR to the calculated sum of its component unisensory NRs. In each example, the actual multisensory NRs have a larger duration and area than the calculated sums of their component unisensory responses. On average, the actual multisensory NRs have a 1.59 and 1.62 times larger area and duration, respectively, than their summed component unisensory NRs. The summary data comparing the area and duration of actual multisensory NRs to the area and duration of their calculated summed NRs are plotted in bar graphs according to stimulus type (Fig. 4B,D). The actual multisensory NRs had a significantly greater duration and area than the calculated summed NRs (P<0.05, N=13-21; Fig. 4B,D). However, the difference in area between the actual Tub+LL response and calculated Tub+LL response was not significant (P>0.08, N=16; Fig. 4B). Interestingly, one fish failed to demonstrate an NR to any of the unimodal stimuli but responded to each multimodal stimulus (Fig. 6). In this example, the supralinear multisensory enhancement of duration and area was most evident.
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Although the time of NR maximum was stable across stimulus type (P>0.4, N=13–21), NR amplitude varied significantly. The unimodal Amp stimuli had the weakest effect (1.65±0.90 pulses s–1, N=21) on amplitude, while the trimodal Tub+Amp+LL stimuli had the strongest effect (6.75±3.28 pulses s–1, N=13). The largest unisensory amplitude (3.32±1.92 pulses s–1, N=16) was elicited by the LL stimuli. The multisensory NRs had significantly greater amplitude than their component unisensory NRs (Fig. 7; P<0.05, N=13–21). The difference between the actual multisensory amplitudes and the amplitudes of the summed unisensory responses was not as great. The amplitude of the actual Tub+Amp NR (5.11±2.11 pulses s–1) was significantly greater than the amplitude of the calculated Tub+Amp NR (3.89±2.64 pulses s–1, P<0.05, N=21). However, the amplitudes of the actual Tub+LL (5.87±2.62 pulses s–1) and Tub+Amp+LL (6.72±3.30 pulses s–1) NRs were not significantly greater than the amplitudes of their summed component unisensory responses (4.89±2.96 pulses s–1, P>0.05, N=16 and 5.59±3.67 pulses s–1, P>0.05, N=13, respectively).
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The scallop of B. niger is a stereotypical EOD burst pattern that
is characterized by a high instantaneous frequency with a fast rise and fall
(Carlson, 2002;
Serrier and Moller, 1989).
Across all of the sessions of stimulus presentation without the EOD
substitute, the probability of having at least one scallop near (1 s before or
2 s after) the object's MLD was only 13.5%. During stimulus presentations with
the EOD substitute, the probability increased to 84.5%. The distribution of
scallop production during unimodal Amp and unimodal LL stimulation was highly
skewed relative to stimulus types containing tuberous input
(Fig. 9A). Hence, without the
EOD substitute, scallop production was not normally distributed
(P<0.001). Sign tests show that the rate of scallop production
from unimodal Tub stimulation is significantly greater than unimodal Amp
(P<0.001, N=21) and LL (P<0.01,
N=16) stimulation. However, there was no significant difference
between Amp and LL unimodal stimuli (P>0.3, N=16).
Interestingly, the number of scallops near the object's MLD for each
multimodal stimulus was significantly greater than the number of scallops
during its component unimodal Tub stimulation
(Fig. 9B, P<0.05,
N=13–21). Fig.
9C,D shows an example of an increase in scallop production near
the object's MLD due to the addition of LL stimulation. Due to the short
duration (4–6 intervals), yet high frequency, of a scallop's signature
burst, the rate of their occurrence was only significantly correlated to NR
amplitude. Table 2 shows the
correlation coefficient between scallop rate and NR amplitude, duration and
area across each stimulus type that contains the EOD substitute.
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Within-session standard deviations of the SDFs between the start time and end time of the mean NR were significantly different when comparing stimulus types with EOD replacement to stimulus types without EOD replacement (P<0.05). Importantly, the standard deviations are approximately equal among all stimulus types with EOD replacement (P>0.05). The same is true when comparing stimulus types without EOD replacement (Amp and LL). The average standard deviation in EOD rate for stimulus types with EOD replacement is 3.19±1.36 pulses s–1. The average standard deviation in EOD rate for stimulus types without EOD replacement is 1.77±0.91 pulses s–1. Interestingly, the CVs among all stimulus types were approximately equal (P>0.05). Therefore, the significant difference among standard deviations is likely to be caused by the significantly larger scallop rate with EOD replacement compared with trials without EOD replacement. Since the CV is normalized, the effect of the jump in NR amplitude caused by scalloping is reduced. The average CV in EOD rate for stimulus types with EOD replacement is 0.47±0.18. The average CV in EOD rate for stimulus types without EOD replacement is 0.47±0.24. Therefore, differences in within-session variation cannot explain differences in response magnitude among stimulus types.
Overall, the within-session temporal alignment () of SDF maxima was
found to be approximately equal between multisensory responses and their
component unisensory responses (P>0.05). Temporal alignment to
Tub+Amp stimulation (=0.60, N=21) was not different from that
obtained with either Tub (=0.47, N=21) or Amp (=0.38,
N=21) stimulation (P>0.05). Unimodal LL stimulation,
however, elicited relatively tight temporal alignment (=0.30,
N=16). This, coupled with the prevalence of scalloping during EOD
replacement, led to significant differences when responses to Tub+Amp+LL
(=0.60, N=13) or Tub+LL (=0.51, N=16) were
compared with responses to LL stimulation (P<0.05). Scallops
spread the temporal alignment of SDF maxima because the occurrence of their
signature burst is not limited to a specific phase of the NR.
We were able to determine a rudimentary relationship between stimulus strength and NR magnitude before arriving at the stimulus parameters used in the main body of evidence of the present study. During a set of experiments where the MLD was 1.8–2.0 cm and the DC voltage was greater than 600µVcm–1, much larger and more consistent unisensory responses were elicited that integrated linearly or sublinearly with the other sensory modality (Fig. 10A–D). To allow for the possibility of elucidating supralinear multisensory enhancement, the stimuli were weakened. Eventually, we discovered that a stimulus object distance of 2.4–2.7 cm often elicited relatively weak and/or inconsistent unisensory tuberous NRs. After this distance was determined, we discovered that unimodal Amp stimuli of approximately 200–400 µVcm–1 generally elicited weak and/or inconsistent NRs. The vast majority of the statistically analyzed data in the current paper is within these parameters. The relationship between stimulus strength and response strength was directly related during unimodal Amp stimulation (Fig. 10E). However, during LL stimulation, the relationship seemed less plastic and susceptible to response suppression (Fig. 10F).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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NR duration and area provide logical indications to the perceived value or
saliency of a stimulus. Intuitively, they represent the length and the sum of
increased energy expenditure in the currency of EODs. If the function of the
NR, like other orienting responses, is to augment sensory acquisition
(Spinks et al., 1985), then
the fish would logically expend greater energy augmenting sensory information
that has a greater perceived value. In the natural environment, common moving
objects such as fish or crustaceans, are likely to stimulate more sensory
modalities than stationary inanimate objects. For example, a stationary fish
would seldom, if ever, encounter a nearby moving object that stimulates the
Amp electrosense and not the LL or Tub electrosense. Therefore, supralinear
multisensory enhancement may be driven by the ecological significance or
qualitative relevance of multimodal stimuli. However, it is not clear whether
a nonlinear relationship between stimulus strength and NR duration can explain
supralinear enhancement. Post and von der Emde showed what appears to be the
beginning of a sigmoidal response curve in the visual sense but a decaying
curve in the auditory sense as stimulus strength increases
(Post and von der Emde, 1999).
LL stimulation stronger (closer object distance) than that applied in the
current paper often caused the fish to suppress its pulsing behavior; however,
unisensory ampullary responses remained directly related to DC voltage
(Fig. 10F). Therefore, the
relationship between stimulus strength and NR magnitude is likely to be
different between mechanosensory and electrosensory modalities. Nonetheless,
it is clear from the main results of the present study that adding
electrosensory stimulation to LL stimulation (i.e. Tub+Amp+LL), which
effectively increases overall `stimulus strength', does not mimic LL response
suppression, but causes response enhancement. However, a multimodal stimulus
containing an NR suppressing LL component and a 100% effective bimodal Tub+Amp
component still causes response suppression
(Fig. 10E). Perhaps a
hierarchy exists, whereby the relative weight of each sensory modality
dictates the dynamics of the multisensory response curve. Nonetheless, as the
strength of the unisensory stimuli cross a threshold level, additional
stimulus modalities become less influential to NR magnitude
(Fig. 10A–D).
The augmentation of perception from the integration of two sub-threshold
unimodal stimuli (Ramos-Estebanez et al.,
2007) is virtually unexplored in electric fish. However, in the
current study, some fish gave a weak or undetectable NR to one or all of the
unimodal stimuli but responded fairly well to their multimodal combination
(Fig. 6 and
Fig. 3C). Perhaps these data
offer additional support for the multimodal stimulus object having a greater
ecological significance or some form of qualitative uniqueness. It is also
possible that these particular fish required a combination of stimulus
modalities to satisfy a higher than normal NR threshold. Nonetheless, a
physiological counterpart to this form of gating was discovered in the optic
tectum of the rattlesnake, whereby certain neurons were virtually unresponsive
to unimodal stimuli but responded to the bimodal visual–infrared
combination (Newman and Hartline,
1981). For a predator like the rattlesnake that specializes in
endothermic prey, the ecological significance of such a neuron is evident.
In weakly electric fish, multisensory neurons have been identified in the
tectum mesencephali (Bastian,
1982; Bleckmann and Zelick,
1993; Heiligenberg and Rose,
1987) as well as in the cerebral pallium
(Prechtl et al., 1998). While
the NR is ultimately regulated by output from the EOD command nucleus
(Carlson, 2002), the relative
importance of either the tectum or pallium to NR magnitude is unknown. Future
research in our lab will focus on exploring whether multisensory integration
in mid-brain neurons can, at least partially, explain the supralinear
enhancement to the NR discussed in the present study. The cerebral pallium may
also be involved because the ablation of two association cortices precludes
the development of multisensory enhancement of behavioral
(Jiang et al., 2007) and
neuronal responses (Jiang et al.,
2006) in the cat. Therefore, it is similarly possible that
multisensory enhancement of the NR is derived from a sensory process formed
from the interaction between the mid-brain and cerebral pallium.
Multisensory integration had a significant, positive effect on the amplitude of the NR (Fig. 7). The amplitude of each multisensory NR was significantly greater than the amplitude of its component unisensory NRs. However, only the amplitude of the Tub+Amp NR was significantly greater than the amplitude of its arithmetically summed unisensory components. Therefore, the level of LL stimulation applied in the present study was probably too close to saturation of NR amplitude for additional stimuli to elicit a supralinear increase. Under curare, the EOD rates during a typical NR acceleration normally had a ceiling around 10 pulses s–1. EOD bursts above this rate were typically in the form of the high-frequency (30–80 Hz) burst component found within a scallop. However, due to the brevity (4–6 intervals) of this burst component, it contributed little to the overall amplitude of the SDF (Fig. 2A). Therefore, the lack of supralinear enhancement in NR amplitude may result from a short behavioral ceiling on acceleration-like changes, since all stimuli greater than or equal to causing this ceiling effect would elicit approximately equal NR amplitudes.
The rate of the NR's occurrence near the MLD of the stimulus object was dependent upon stimulus type. Probability to unimodal Tub and unimodal Amp stimuli was relatively low while being relatively high for unimodal LL stimuli (Fig. 8B). Bimodal Tub+Amp stimulation yielded a significantly higher probability than its component unimodal stimuli. However, NR probability was approximately equal between all stimuli containing the LL modality. Therefore, unimodal LL stimulation had a strong effect on probability and could not be augmented by the addition of electrosensory input. It is interesting that the same strength of LL influence did not extend to NR magnitude. Perhaps the centers of LL sensation in the brain are tightly linked to the NR decision process but, to a lesser extent, to the determination of NR magnitude (Fig. 8B,D). Therefore, the relationship between LL stimulus strength and NR probability might be fairly steep.
NR duration, area and amplitude were recalculated after removing the within-session trials below the probability threshold. No significant change occurred in NR duration. Therefore, it is likely that the multisensory enhancement of NR duration is not simply caused by an increase in response probability. Not surprisingly, a significant inflation of NR amplitude and area occurred in all but the most consistent responses. Therefore, multisensory enhancement of NR area can be partially explained by an increase in NR probability.
Although an individual's tendency to scallop may be relevant to social
interactions (Moller et al.,
1989; Serrier and Moller,
1989), the current study provides evidence that scalloping is
involved in electrolocation. With the EOD substitute, scallop production
regularly occurred when the object was near its MLD. Scallop production
between 1 s before and 2 s after the object's MLD was significantly greater
during each multimodal stimulus than its component unimodal tuberous stimulus
(Fig. 9B). However, scallop
production was very rare without the EOD substitute and had a highly skewed
distribution among subjects (Fig.
9A). In fact, during unimodal LL stimulation, only one of the 16
fish scalloped during the aforementioned time window. Therefore, the rate of
scallop production significantly increased during multimodal stimulation and
relied heavily on tuberous stimulation. Even though the rate of scalloping
significantly varied with stimulus type, it had no correlation to NR duration.
Not surprisingly, scallop rate was significantly correlated to NR amplitude
(Table 2). The scallop's
signature burst may function as a complementary method of electrosensory
scanning that provides a higher temporal resolution than accelerations but
with minimal cost due to its brevity.
Our `single object' experimental paradigm provides evidence that the
spatial and temporal congruence of multiple stimuli is sufficient to induce
multisensory enhancement in electric fish. However, are the spatial
determinants to multisensory enhancement for electro-mechanically and
audio-visually elicited orienting responses
(Stein et al., 1988;
Whitchurch and Takahashi,
2006) similar? The Tub, Amp, and LL (canal) modalities are
interesting because they are all confined to the near field. By contrast,
vision and audition both work over a much broader spatial range. Therefore,
electrosensory and lateral line systems are less likely than the visual and
auditory systems to integrate spatially incongruent stimuli segregated by two
unrelated, yet temporally coincident events. Additionally, a small, point
source visual stimulus, such as a flying insect, produces a relatively diffuse
auditory stimulus. Yet, a similarly sized Daphnia would produce
electrosensory and mechanosensory stimuli that attenuate at equal rates
(Coombs et al., 2002;
Nelson et al., 2002). This
natural distinction may have a functional significance to the spatial
determinants of multisensory enhancement. Perhaps multisensory neurons in
electric fish have much narrower receptive fields. Yet, in the mid-brain of
electric fishes, nothing is known about the receptive field of multisensory
neurons. Moreover, very little is known about the relationship between the
spatial registration and convergence of electrosensory and mechanosensory
sensory space in neurons of the pallium of electric fish
(Prechtl et al., 1998).
Therefore, it is not clear how combining `spatially incongruent'
electrosensory and mechanosensory stimuli would affect sensory integration and
perception. The NR could possibly serve as a probe in determining the spatial
boundaries of multisensory enhancement by studying the relationship between NR
magnitude and the physical disparity between sensory stimuli.
The current study provides evidence that B. niger predictably increases its NR magnitude according to the number of sensory modalities present in a single moving object. Since the NR has energetic costs and theoretically improves electrolocation, it is logical to speculate that a multimodal moving object is perceived as more valuable than a moving object comprised of one of its unimodal components. Since this increase in stimulus value, measured by NR magnitude, was supralinear, multimodal object stimuli may cause a qualitative change in perception not elicited by unimodal object stimuli, which likely lack the same ecological significance.
LIST OF ABBREVIATIONS
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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P>0.1). Area (B) and duration (D) of
the actual vs calculated multisensory NRs. The actual NRs have a
significantly greater area and duration than the calculated linear sum of
their component unisensory NRs (except for T+LL area; P>0.08).
*P<0.05, error bars equal ± 2 s.e.m. Tub,
tuberous electrosense; Amp, ampullary electrosense; LL, mechanosensory lateral
line.
