Pre-receptor profile of sensory images and primary afferent neuronal representation in the mormyrid electrosensory system
1 Departamento de Biología Celular y Molecular, Facultad de Ciencias,
Universidad de la Republica, Montevideo, Uruguay
2 Unité de Neurosciences Intégratives et Computationnelles,
CNRS-UPR 2191, Gif sur Yvette, France
3 División de Neurofisiología Comparada (Unidad Asociada a la
Facultad de Ciencias, Universidad de la Republica) IIBCE, Montevideo,
Uruguay
* Author for correspondence (e-mail: angel{at}iibce.edu.uy)
Accepted 27 April 2004
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Summary |
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Stimulus intensity is encoded in the latency and number of action potentials in the response of primary afferent fibers. It is also reflected in changes in the amplitude and area of extracellular field potentials recorded in the deep granular layer of the electrosensory lobe. Since the object image consists of a redistribution of current density over the receptive surface, its presence is coded by change in the activity of receptors over an area much larger than the skin surface facing the object. We conclude that each receptor encodes information coming from the whole scene in a manner that may seem ambiguous when seen from a single point and that, in order to extract specific object features, the brain must process the electric image represented over the whole sensory surface.
Key words: Mexican hat, electric fish, latency code, electric image, electrolocation, electrosensory lobe, distributed sensory representation
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Introduction |
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Mormyromast electroreceptors are innervated by two types of primary
afferent fibers (types A and B), which project centrally to different regions
of the electrosensory lobe (ELL). Stimulus intensity is related to action
potential latency in both types of primary afferents (Bell,
1990a,b
),
but it has been suggested that type A primary afferents exclusively code
stimulus amplitude (von der Emde and Bleckmann,
1992
,
1997
), while the firing of
type B afferents is probably related to the coding of the waveform of the
local electric organ discharge (LEOD), allowing the fish to perceive the
impedance-related `qualia' (Lewis,
1929
) of the object (i.e. `electric color';
von der Emde, 1990
;
von der Emde and Ronacher,
1994
; Budelli and Caputi,
2000
).
The present paper deals specifically with the spatial coding of electrosensory images and therefore with primary afferent input arising from Type A mormyromast electroreceptor cells. We tested the following hypotheses: (1) the latency code transmits most of the information about the intensity of the sensory signal; (2) there is distributed coding of object position and other properties at the primary afferent level and (3) the spatial coding pattern of images conforms to the opposing center-surround `Mexican hat' distribution, as described in previous studies. These issues were explored by recording the LEOD simultaneously with the population field potentials and unitary activity of primary afferents at their terminal region in the granular layer of the ELL, in discharging fish in the presence and absence of stimulus objects.
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Materials and methods |
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Fig. 1A shows the experimental paradigm. Experiments were performed under etomidate anesthesia (Hypnomidate; Janssen-Cilag, Issy les Moulineaux, France; 2 mg l-1 for induction, 1 mg l-1 during surgery, 450500 µg l-1 during recording, dissolved in aerated water at 22°C, conductivity 170 µS cm-1, perfused through the gills at a rate of 40 ml min-1). Experimental measurement (K. Grant, unpublished observation) has shown that this dose of etomidate does not alter the form or the strength of the natural EOD, although the discharge rhythm is slower and more regular than in the awake state.
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The fish's head was immobilized by a plastic rod attached to the skull, which held only the dorsal surface above the water level in the recording tank. The fish's body was submerged, supported against a sponge with three strands of soft cotton thread (diameter 1 mm). A section of the skull above the ELL was removed and the valvula cerebelli overlying the electrosensory lobe was reflected laterally, to allow visual guidance of electrode placement.
Averaged field potentials (N=10) and unitary activity were
recorded from the Type A mormyromast primary afferent terminal region in the
granular and intermediate layers of the medial zone of the ELL using glass
micropipettes (3 M, filled with 3 mol l-1 NaCl, for field
potentials; 150200 M
, filled with 2 mol l-1
KCH3SO4, for intracellular or extracellular unit
recordings) connected to a high-input impedance amplifier (Axoclamp 2A; Axon
Instruments, Union City, CA, USA) used in Bridge mode. Signals were digitized
using a Labmaster interface (Scientific Solutions, Mentor, OH, USA) and
processed with a computer running Acquis1 (Gérard Sadoc, C.N.R.S.,
France) and Matlab (Scientific Solutions) software.
Microelectrodes were positioned using the depth from the surface of the ELL
and the characteristic shape of the field potentials as landmark guides
(Bell et al., 1992). In two
experiments, electrode position in the granular layer was verified by
iontophoretic deposit of pontamine sky blue
(Hellon, 1971
), identified
histologically following postmortem fixation and sectioning. For each
electrode track, the cutaneous receptive fields of primary afferent fibers
recorded in the granular and intermediate layers of the ELL were identified by
applying local electrical stimulation (100 µs constant current square
pulses) in the water close to the skin via a pair of silver ball
electrodes placed 2.5 cm apart, oriented perpendicular to the skin. Sensory
responses to the fish's own EOD were then examined in the presence of
different types of objects positioned at different distances from the
cutaneous receptive field center: (1) aluminum and Teflon cylinders (16 mm
diameter, 50 mm length) with the long axis perpendicular to the skin surface;
(2) an aluminum plate (3 mmx23 mmx50 mm) with the long axis
perpendicular to the skin surface; (3) aquatic plants; (4) a stone and (5) a
piece of water-saturated mangrove root. The last three natural objects were
similar in volume to the aluminum and Teflon cylinders, although more
irregular in shape.
Primary afferent input to the ELL is organized in a topographically ordered
manner. EOD-related field potentials recorded in the granular and intermediate
layers of the ELL (Fig. 1) are
generated by integration of reafferent electrosensory input with a corollary
discharge signal driven by the electromotor command
(Bell et al., 1992). The
modulation of this complex field potential by reafferent electrosensory input
(representing the object image) was calculated by subtraction. To make this
calculation, reafferent sensory input could be removed in two ways, revealing
the electric organ corollary discharge (EOCD) field potential alone. The first
method was to inject intramuscularly 100 µg of d-tubocurarine chloride
(Sigma, St Louis, MO, USA), which blocked cholinergic neurotransmission
between electromotoneurons and the electric organ, thus abolishing the EOD,
while the central motor command and the EOCD remained intact. An alternative
and reversible block of reafferent sensory input was obtained by
short-circuiting the electric organ with a metal plate (3 mmx23
mmx50 mm) placed parallel and very close to the electric organ. The
resulting isolated EOCD field potential recorded in the ELL was similar using
either of the two methods. A similar procedure in which a plastic plate was
placed parallel to the electric organ also allowed us to modulate global field
distribution and increase the LEOD in anterior regions of the body, in
experiments whose aim was to correlate LEOD amplitude with primary afferent
spike timing.
The reafferent electrosensory input could then be calculated by subtraction of the EOCD-alone field potential from the field potential evoked when the EOD was present. We have called this difference the field potential change corresponding to the sensory response (FPSR). Using this measure it was then possible to make quantitative comparison of the neural images of sensory input obtained in the absence of an object (control) and in the presence of any of the objects mentioned above.
In 21 cases we also recorded the effect of objects on the unitary spiking
activity of primary afferent fibers. These were identified by their
characteristic patterns of discharge consisting of a short-latency
(5.57 ms) train of two or three spikes rising from the baseline with
only small variability for a given stimulus (Bell,
1990a,b
).
Natural stimulus intensity at the receptive surfaces was quantified from the LEOD recorded close to the skin, using a pair of steel wire electrodes (exposed tips 1.5 mm long, separated by 2.5 mm). The LEOD signal was recorded with a Tektronix 5A22N differential amplifier in a Tektronix 5223 digital oscilloscope, connected via a GPIB interface to a computer running Acquis1 software (Gérard Sadoc, C.N.R.S.). This gave sufficient resolution in A/D conversion to reproduce the rapid signal of the EOD without attenuation or distortion.
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Results |
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When an object interferes with the EOD-generated electric field, this causes a change in the basal neural response recorded in the ELL. A maximum change is observed when the object faces the zone of the skin from which primary afferents project to the recorded point of the ELL. Here, we define this region of the skin as the center of the receptive field. The following sections deal with the neural response when (1) the object faces the center of the receptive field and (2) the object position is changed.
The neural response at the center of the receptive field
The left column of Fig. 1C
shows LEODs recorded at the center of the peripheral receptive field for five
different objects of similar volume and shape but of different materials. The
LEOD in the presence of a piece of water-saturated dead wood was similar to
the LEOD in the absence of any object (control). The peak-to-peak amplitude of
the LEOD was diminished in the presence of the plastic cylinder and the stone
and increased in the presence of the living plant and the metal cylinder.
These measurements show that the natural stimuli produced by plants, stones or
wood fall within the range of those produced by the aluminum and Teflon
cylinders used in the experiments described here.
The middle column in Fig. 1C illustrates the field potentials recorded in the ELL granular layer in the presence of the same objects (red traces) and compares them with the field potentials evoked at the same recording site by the corollary discharge input alone (black traces) when the EOD and the consequent reafferent input had been blocked by shunting the EOD with a metal plate placed parallel to the body very close to the electric organ. The contribution of the reafferent sensory input can be calculated as the difference between these traces, illustrated in the right column of Fig. 1C (FPSR).
Despite the differences in object characteristics, all the FPSR traces had an initial sharp negative wave followed by a broader positive wave. An increment in LEOD amplitude was associated with reduced latency and increased amplitude of the early sharp negative wave of the FPSR (e.g. compare traces for metal and plastic objects in Fig. 1C). Reductions in LEOD amplitude were associated with opposite changes in the FPSR.
The FPSR is, however, a complex response that corresponds to the activity of primary afferent input as well as several different types of neurons of the ELL excited by the afferent input in the presence of the corollary discharge signal. Records of spiking activity show that reafferent primary electrosensory input arrives in the ELL 512 ms after the beginning of spinal electromotoneuron activity (i.e. 29 ms after the EOD whose artifact can be observed in the records), corresponding to the early negative component of the FPSR. The results described below focus on the early processing of the reafferent sensory image and therefore will deal only with this part of the FPSR. The later positive wave of the FPSR represents later stages of activity in the intrinsic network, which will be the subject of future publication.
Change in amplitude of the LEOD causes changes in the amplitude, number and latency of the multiple peaks of the field potential response produced by the activity of a population of afferent fibers. Larger LEODs reduce the latency and increase the number of primary afferent action potentials and also increase the probability that more fibers fire at the same time. As a consequence, the negative peak of the field potential starts earlier and increases in area. Thus, the early negative component of the FPSR is also a sensitive index by which to estimate primary afferent activity.
In order to study the relationship between LEOD amplitude and FPSR modulation in greater detail, the amplitude of the LEOD was modified by placing a large metal plate in the tail region, orientated parasagittally, first close to the electric organ and then at different distances lateral to the fish's tail (Fig. 2A). Close to the electric organ, this produces a large reduction in external resistance, equivalent to a local short-circuit at the current source. The consequence is a redistribution of currents within the global field: the fraction of current flowing into the anterior regions of the fish's body is reduced, and in this case the rostral part of the body is in the `surround' region of the Mexican hat. As the plate is moved further away from the tail, the local short-circuit effect at the current source diminishes and the metal plate starts to behave as any conductive object placed far away. With increasing distance between the metal plate and the electric organ, the object image becomes wider (see Fig. 6), and at a distance of several centimeters the whole ipsilateral surface of the fish falls within the central region of the Mexican hat, producing an increase in the current flowing through the whole ipsilateral receptive surface. A plastic plate close to the tail produced opposite effects. Fig. 2A illustrates the changes in the FPSR as the LEOD amplitude was modulated in this manner.
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The area and the latency of the early negative peak of the FPSR are also
related to the latency and the number of spikes of the primary afferent
unitary response. Extracellular or intracellular records of unit activity
examined as a function of LEOD amplitude confirmed observations made using
artificial stimuli. As stimulus intensity is increased, the latency of the
first spike of the response is reduced and the number of spikes in the
response burst increases (Szabo and
Hagiwara, 1967; Bell,
1990b
; von der Emde and
Bleckmann, 1992
).
Fig. 2C shows a raster
diagram of spike timing for a single afferent fiber recorded as a metal object
was moved steadily along the body, passing across the receptive field. The
latency of the first spike reached its minimum at the center of the receptive
field (zero on the ordinate) and changed smoothly with object position on
either side of that point. In addition, the interval between the first and
second spikes was a precise function of the latency of the first spike
(Fig. 2D), showing that the
timing of the second spike is predictable from the latency of the first one.
These observations strengthen the interpretation that a single parameter,
probably peak-to-peak amplitude of the LEOD, is coded by the latency of the
primary afferent spike train (Bell et al.,
1992) and similarly by the area or latency of the negative peak of
the sensory field potential.
Sensory responses as a function of the position of the object
The increasing relationship between the LEOD amplitude and responses
recorded in the ELL suggests strongly that the opposing `center-surround'
(Caputi et al., 1998;
von der Emde et al., 1998
)
structure of the object image projected on the sensory surface is conserved in
the response of primary afferents.
To go further in understanding how the sensory image is formed, it is first necessary to know how the stimulus driving the afferents projecting to the recording region changes with the position of the object. Instead of recording the complete set of responses at different points of the ELL, we took the alternative step of recording at a single point in the ELL as an object was moved in successive steps past the center of the receptive field. Fig. 3 shows schematically the expected stimulus variations in the case of a metal object. Because the energy source for the stimulus is located caudally (i.e. at the electric organ), the Mexican hat profile of the sensory image is asymmetric, with a deeper trough on the rostral front. This means that the contrast is greater at the rostral border of the image. Thus, when a metal object is situated caudally to the center of the receptive field (Fig. 3A, red), the electroreceptors will see the deep rostral trough of the Mexican hat image profile (Fig. 3B, red trace), where the LEOD is significantly decreased compared with the basal value (Fig. 3C, red dot). When the object is rostral to the center of the receptive field (Fig. 3A, blue), the center of the receptive field will see the more shallow caudal trough of the image profile (Fig. 3B, blue trace) producing a relatively smaller surround effect (Fig. 3C, blue dot).
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The local electric field generated by the EOD decays with distance from the tail towards the head. The spatial attenuation of this decay depends on the relative conductivity of the water and the internal fish tissues (for any given experiment this was constant). Because of this caudal-to-rostral decay of the electric field generated by the EOD (the signal carrier), the image of a given object is less intense when it is situated towards the head of the fish (Fig. 3B, blue line) than when it is located caudally (Fig. 3B, red line). This effect increases still further the difference between the rostral trough of a caudal object image and the caudal trough of a rostral object image (compare red and blue dots in Fig. 3C). As shown in the graph of Fig. 3C, the net dynamic effect seen at the receptive field as an object moves past is also a Mexican hat profile but is a `mirror' image of the stationary object image. The asymmetry of the image is increased and the surround effect is greater at the caudal margin than at the rostral edge. In mathematical terms, as an object moves from caudal to rostral, passing through the receptive field, the dynamic record obtained at a given point in the electrosensory network is the convolution of the basal local EOD (the signal carrier) and the asymmetrical Mexican hat profile of the electric image (the signal).
Fig. 4 illustrates the progress of the FPSR early negative peak as conducting and non-conducting objects are moved from rostral to caudal through the center of the receptive field, following the body profile at a distance of 2 mm from the skin. Metal and plastic cylindrical objects produced opposite modulation of the field potentials recorded in the ELL. A peak modulation of the FPSR early negative wave was found when the center of the object was at the center of the cutaneous receptive field (Fig. 4, gray bar at position 0 mm). Rostral to the receptive field center, the modulation of the sensory response decayed to close to the control situation. When the object was caudal to the cutaneous receptive field, the modulation of the sensory response was opposite to that observed when the object was in line with the center of the cutaneous receptive field.
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Plastic objects produced a relatively smaller, spatially narrower
modulation of the sensory response than metal objects. These results fit with
previous simulations, predicting that metal objects would produce a larger
modulation of the LEOD than plastic objects
(Sicardi et al., 2000). This
asymmetry of the images formed by conductive and non-conductive objects is
because the difference between the conductivity of the plastic and the water
is much smaller than the difference between the metal and the water. In
addition, the asymmetry of the images formed by conductive and non-conductive
objects is enhanced because the strength of the source equivalent to the field
distortion produced by the object is non-linearly dependent on object
conductivity.
It is also interesting to note that the curves for plastic and metal objects have a different shape when the object is in the caudal region of the fish's body. Here, a metal object produces increasing attenuation as it moves closer to the electric organ source. This is because a metal object short-circuits the electric organ output, significantly reducing the sensory stimulus in all rostral regions. In the extreme case when a large metal object is exactly aligned with the electric organ, reafferent sensory input is absent and the field potential recorded in the ELL is similar to that generated by the EOCD alone, for instance recorded in a curarized fish in the absence of an EOD.
Fig. 5 illustrates this Mexican hat phenomenon coded in the primary afferent firing pattern (top) and field potential color maps (bottom). The two upper raster diagrams show the timing of action potentials fired by a single primary afferent fiber in response to the EOD, when a plastic object and a metal object were positioned at 10 successive points passing through the center of the cutaneous receptive field.
The primary afferent fiber fired two or three action potentials, depending on the nature of the object (plastic or metal) and its location relative to the receptive field center. For a metal object, the latency of the first spike was shortest when it was positioned in the center of the receptive field (ordinate 0 mm). When the metal object was either caudal or rostral to the receptive field center, the latency of the primary afferent action potentials was longer and the variability of the timing of the second and third action potentials of the train increased. At 15 mm caudal to the receptive field center, the third action potential dropped out of the response. In the presence of the plastic object, the latency of primary afferent action potentials varied in an opposite manner. Latency was longest when the plastic object was in line with the receptive field center, and here the EOD evoked only two action potentials. In each series, the timing of the three action potentials evoked by the EOD in the absence of any object is shown by the dotted red lines. It can be seen that in both cases the effect of the object on action potential timing inverted between 10 and 15 mm caudal to the receptive field center and that this effect was larger for the metal object.
These results confirm the findings of earlier work in mormyrids
(Szabo and Hagiwara, 1967) and
in gymnotid electric fish (Hagiwara and
Morita, 1963
; Scheich and
Bullock, 1974
; Bastian,
1981a
,b
)
that showed that, for individual afferent fibers, the latency of spikes
generated when a conductive stimulus object was present in the surround region
of the receptive field was greater than latencies of spikes generated by the
EOD alone in the absence of any object. Here, we have demonstrated how both
highly conductive and poorly conductive objects modulate the reafferent
sensory response to the EOD, in a manner that is compatible with the Mexican
hat profile of the object image, and produce effects of opposite sign
depending on object conductivity.
The lower panels of Fig. 5 show field potential responses as a function of object position along the fish. [This section uses a different time scale, showing the period from 5 to 20 ms following the firing of the electromotoneurons (conventional 0 of the system).] The horizontal axis indicates time, while the vertical axis shows the position of the object relative to the fish's body illustrated on the left; voltage above or below zero is color coded, as shown in the vertical calibration bar to the right. The basal field potential response recorded in the absence of objects is shown as a separate strip at the top. These field potential diagrams show darker blue regions indicating the negative peaks in the response. The red region indicates the slow positive wave that follows the negative peak (see Fig. 1). For a metal cylinder (right), the blue region increased in size and decreased in latency when the conductive object moved towards the center of the receptive field. The opposite pattern was seen for a plastic cylinder in different positions relative to the center of the receptive field (left).
To address how sensory responses depend on the distance between the fish
and the object, we repeated the experimental protocol of
Fig. 5, placing a metal object
at successive rostrocaudal positions, making several passes through the
receptive field at different distances lateral to the skin
(Fig. 6). In this case, we used
a metal plate oriented perpendicular to the skin surface, whose profile was
narrower than the face of the cylindrical objects, in order to generate a
sharper object image. In the upper section of
Fig. 6, rasters of single
primary afferent spike timing show the modulation of the pattern of discharge
when the metal plate was moved along the fish's body in sequential 5 mm steps,
first at 2 mm from the skin (left) and then at a lateral distance of 7 mm
(right). Close to the fish's body, the effect of the object was greater in
amplitude and more sharply contrasted than when the object was further away.
This is also illustrated in field potential responses, shown in color maps in
Fig. 6 (bottom) as the same
object was moved along the fish's body at distances of 1, 7 and 17 mm from the
skin. As the distance between the object and the fish was increased, the
changes in reafferent responses decreased in intensity. The width of the
sensory image also increased with distance and the image became more blurred,
in agreement with previous theoretical predictions
(Caputi et al., 1998;
Budelli and Caputi, 2000
).
These results indicate that both the primary afferent spiking response and the (more complex) field potential records from the granular layer of ELL are related directly to the local modulation of the EOD seen at the receptive surface in the presence of an object and code the center surround profile of the object image.
However, when recording centrally, it is possible that lateral inhibition
might also be involved in the Mexican hat effect observed in the FPSR.
Previous experimental studies have shown that the neural phenomenon of lateral
inhibition does indeed exist in the electrosensory lobe
(Bell et al., 1997;
Meek et al., 2001
). The
experiment illustrated in Fig.
7 was carried out in order to distinguish the effects of the
Mexican hat profile of the stimulus from effects due potentially to lateral
inhibition. First, an artificial electric stimulus (100 µs pulse) was
applied synchronously with the EOD, at points rostral or caudal to the center
of the receptive field (Fig.
7A). This resulted in facilitation of the reafferent sensory
response evoked by the EOD when the stimulus was applied from 25 mm rostral up
to 10 mm caudal to the center of the receptive field.
Fig. 7B illustrates (in blue
and red) the difference between the facilitated response and the basal
reafferent sensory response at the center of the receptive field. The plot in
Fig. 7A shows this effect as a
function of the distance to the center of the electric field. When the
additional stimulus was applied at a distance greater than 10 mm caudal to the
receptive field center, there was no change in the reafferent sensory
response. This shows the extent over which excitatory input from the surround
region can facilitate the neuronal response in the granular layer of the ELL.
Surround inhibition was not seen in these experiments when the additional
artificial stimulus and the EOD were synchronous. However, lateral inhibitory
interactions have been observed in other experiments using curarized
preparations, applying two artificial stimuli: lateral inhibition appears most
clearly when using non-synchronous stimulation paradigms, where the
conditioning stimulus precedes the test stimulus by at least 2 ms
(Kröther et al.,
2001
).
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Next, either a metal or a plastic object (cylinder) was placed 40 mm caudal to the center of the receptive field, facing an area of skin on the fish's lateral flank that bears no electroreceptors (see position in Fig. 7A). In the presence of a metal object, the reafferent sensory response was nevertheless dramatically reduced (Fig. 7C). Since the object was facing skin lacking electroreceptors, this effect could not have been due to inhibition originating from the area immediately facing the metal object. It was more likely due to the surround effect intrinsic to the Mexican hat physical profile of the object image itself. Similarly, when presenting a plastic object at the same position 40 mm caudal to the receptive field center, the latency of the reafferent response decreased and the amplitude of the FPSR increased (Fig. 7C), indicating a stronger stimulus at the center of the receptive field. These results again corroborate the Mexican hat effect as a purely pre-receptor phenomenon. They do not exclude, however, that lateral inhibition probably plays an additional role in sharpening receptive field properties of neurons in the central nervous system, and this will be explored fully in future experiments.
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Discussion |
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However, our results show that all three of these parameters encode the
same variable of the object image, raising the question of why it should be
useful to have such signal redundancy. The latency of the first spike of the
primary afferent response is closely related to the intervals between this and
subsequent spikes of the response, and both are tightly dependent on LEOD
amplitude. It has been suggested that the gate created by EOCD-generated
excitatory input to granule cells is critical for reading the timing of the
first spike of the reafferent train (Bell,
1986; Gómez,
2001
). As the latency of the first spike diminishes, it approaches
the peak of the excitatory post-synaptic potential (EPSP) produced by the EOCD
in the granule cells. This facilitates the responses of the granule cells, in
this way amplifying the reafferent input. If more than one granule cell spike
is needed to drive the next postsynaptic neuron, as for example in the case of
the proposed ephaptic interactions with large myelinated inhibitory
interneurons (Han et al.,
2000
; Meek et al.,
2001
) or the deep granular layer large fusiform cells
(Meek et al., 2004
), the
number and frequency of spikes might be important. This speculation suggests
how an apparently redundant mechanism of coding may be important in sensory
integration in the ELL: different neurons of the intrinsic network of the ELL
may extract and address the same information using different information
codes.
Distributed nature of electrosensory image processing
Here, we provide evidence that there is a distributed coding of
electrosensory images in the early stages of electroreception. Recorded
responses of primary afferent activity and field potentials in the ELL
indicate that this is based on the Mexican hat pattern intrinsic to the nature
of the stimulus, enhanced by the difference between the conductivities of the
fish body and the water and probably further shaped by lateral inhibitory
neuronal mechanisms in the primary afferent projections and granule cell layer
and the interaction with the EOCD.
A common reference for the study and design of image processing mechanisms is mammalian vision. In this sensory system, all points along the same line passing through the optical center of the eye are mapped on a single point of the retina. By the same reasoning, different points of the retina receive information from different zones of space. Thus, we can say that in such a system the physical image results from the apposition of different independent stimuli.
The case for electroreception is different because the finite source of
energy is contained within the fish's body. An elementary point object
modulates current distribution with a center-surround opposition pattern and
distorts the entire electric field. This gives contrast at the level of the
sensory surface itself, and the information generated by the elementary object
(a single point in space) is contained not only in input from the skin
receptors facing the object but also in the overall pattern of transcutaneous
current perceived over the whole sensory surface. This phenomenon describes a
physical property intrinsic to the nature of the electrosensory stimulus. Such
`distributed' imaging procedures are also present in some other sensory
systems (Coombs et al., 1996,
2002
). Here, we have confirmed
the theoretical prediction that the Mexican hat effect present at the physical
image is translated at the primary afferent level and is therefore significant
for the electrosensory system. Both physical measurements
(Caputi et al., 1998
) and
theoretical simulation (Sicardi et al.,
2000
) indicate that the relative slope (slope/maximum amplitude)
of the object image varies little with size and conductance of the object and
is thus the best indicator of object distance. For example, the latency of the
first action potential of the primary afferent response
(Fig. 6) increases with the
distance of a metal object from the center of the receptive field. Thus, as
for the physical object image, the neural response pattern spreads out with
distance from the fish's body. Despite the differences between patterns of
response to metal and plastic objects, similarities in the relative slopes of
their Mexican hat profiles are preserved in the neural response at the primary
afferent level. This provides additional support to the hypothesis that fish
discriminate object distance by measuring the relative slope of the sensory
image (Caputi et al., 1998
;
von der Emde et al., 1998
;
von der Emde, 1999
).
We also found that in the case of metal objects, the center-surround
contrast observed at the primary afferent level is much larger than that at
the skin. This is in part due to the asymmetry of the afferent response,
caused by the hyperbolic relationship between stimulus amplitude and afferent
spike latency (Bell, 1989):
reductions in the LEOD result in larger changes in latency (and even failure
to produce afferent firing) than corresponding increases in the LEOD. It
should also be noted that the spatial profile produced by objects that were
similar in shape but of different conductivities were not exact mirror images.
For metal objects, the surround response observed centrally at the afferent
terminal site is relatively enhanced, but for plastic objects the same
hyperbolic relationship tends to diminish the surround effect centrally.
Conclusions
The Mexican hat profile of the stimulus is a physical property of the
object image at the level of the receptors and is separate and different from
neural lateral inhibition. Because the electric organ is a discrete, finite
source located in the fish's body, objects in the nearby environment will
always project an image with a center-surround structure, whatever their size.
This is because conducting objects locally facilitate the flow of current,
with the corresponding subtraction of current from the surrounding region.
Plastic objects produce the opposite effect. Because the conductivity of the
fish's body is higher than that of water, the opposing center-surround pattern
is enhanced, and contrast is locally increased, at the electroreceptive
surface. This stimulation pattern is preserved in the primary afferent
activity, encoded in the hyperbolic stimulus intensity versus spike
latency response pattern described by Szabo and Hagiwara
(1967) and Bell
(1990a
). In the presence of an
object, the latency of primary afferents firing is decreased or increased with
respect to the set-point corresponding to the unperturbed electric field. This
is functionally significant since latencies vary within the non-linear gate
created by the corollary discharge (Bell,
1989
). As a function of this gating mechanism, advances or delays
of primary afferent activity produce different responses in the principal
cells of the ELL (Gómez,
2001
; L. Gómez et al., personal observations).
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