Comparative Biochemistry and Physiology Part A 136 (2003) 821–825
Electrolocation in the platypus—some speculations"
Uwe Proske*, Ed Gregory
Department of Physiology, P.O. Box 13F, Monash University VIC 3800, Melbourne, Australia
Received 12 March 2003; received in revised form 22 May 2003; accepted 29 May 2003
Abstract
In the platypus, electroreceptors are located in rostro-caudal rows in skin of the bill, while mechanoreceptors are
uniformly distributed across the bill. The electrosensory area of the cerebral cortex is contained within the tactile
somatosensory area, and some cortical cells receive input from both electroreceptors and mechanoreceptors, suggesting
a close association between the tactile and electric senses. Platypus can determine the direction of an electric source,
perhaps by comparing differences in signal strength across the sheet of electroreceptors as the animal characteristically
moves its head from side to side while hunting. The cortical convergence of electrosensory and tactile inputs suggests a
mechanism for determining the distance of prey items which, when they move, emit both electrical signals and
mechanical pressure pulses. Distance could be computed from the difference in time of arrival of the two signals. Much
of the platypus’ feeding is done by digging in the bottom of streams with the bill. Perhaps the electroreceptors could
also be used to distinguish animate and inanimate objects in this situation where the mechanoreceptors would be
continuously stimulated. Much of this is speculation, and there is still much to be learned about electroreception in the
platypus and its fellow monotreme, the echidna.
! 2003 Elsevier Science Inc. All rights reserved.
Keywords: Platypus; Electroreception; Cerebral cortex; Electrolocation; Monotreme
1. Introduction
The two outstanding features that raise the
monotremes into the category of being extraordinary animals are their reproductive biology and
their electrosensory system. The presence of an
electric sense was first reported in the platypus by
Scheich et al., 1986. (For reviews see Proske et
al., 1998; Pettigrew, 1999.) Here, we would like
to discuss how the platypus might use its electro" This paper is based on a presentation at Monotreme
Biology, a satellite symposium of the sixth International
Congress of Comparative Physiology and Biochemistry, held
at Lemonthyme, Tasmania, February 13–15, 2003.
*Corresponding author. Tel.: q61-3-9905-2526; fax: q613-9905-2531.
E-mail address:
[email protected] (U. Proske).
sensory system in prey capture. We know that the
platypus is an efficient hunter, being able to catch
half of its body weight of live prey in one night’s
forage (Burrell, 1927).
The primary electrosensory organ is the bill.
Skin of the bill is a mosaic of electroreceptors and
mechanoreceptors. The mechanoreceptors are clustered at the base of a mobile column of flattened
keratinised cells called push-rods. The idea is that
the column moves upwards and downwards to
stimulate the receptors at its base. It is a little bit
like the movement of a cat’s whisker stimulating
the receptors at its base. The push-rods are distributed uniformly across the surface of the bill. By
contrast, the large mucous glands, now identified
as the electroreceptors (Gregory et al., 1988), are
aligned in a series of rostro-caudally directed rows
1095-6433/03/$ - see front matter ! 2003 Elsevier Science Inc. All rights reserved.
doi:10.1016/S1095-6433Ž03.00160-0
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Fig. 1. Distribution of large mucous sensory glands (upper
drawings) and push-rods (lower drawings) in the bill, viewed
from the dorsal (left) and ventral (right) aspects. The large
mucous glands are arranged in longitudinal stripes (shaded)
alternating with stripes where there are none, while the pushrods have a more uniform distribution, with a higher concentration towards the edge of the bill. (Modified from Andres
and von During, 1984.)
(Fig. 1). The electroreceptors respond to DC and
alternating voltages, cathodal excitatory, anodal
inhibitory (Gregory et al., 1989a). They do not
respond to mechanical stimulation unless it is
strong enough to cause damage. The mechanoreceptors do not respond to weak electrical pulses
and need very large voltages to evoke a response,
probably from direct stimulation of the receptor
axon.
In the platypus, the electroreceptors, like the
push-rods, are restricted to the bill (Fig. 1). In
bony fishes, where electroreceptors are distributed
over the entire body surface and along the lateral
line, the arrangement is rather different. In the
platypus, the afferent pathway to the brain is a
part of the trigeminal system, involving the 5th
cranial nerve. In the electrosensory systems of
fishes and anuran amphibians, the pathway is a
part of the acoustico-lateralis system, involving
the 8th cranial nerve. The significance of this is
that the trigeminal system is known to carry all of
the afferent information from the skin of the face,
and in the platypus, skin of the bill. The pathway
in the acoustico-lateralis system is associated with
central processing of auditory information.
The close association between cutaneous sensory information and electroreceptor activity is
further emphasised by the location of the central
projection zone. Some years ago Bohringer and
Rowe (1977) drew the boundaries of the central
somatosensory projection area from the bill. Subsequently we showed that the central projection
area for electroreceptors in the bill lay within that
boundary. So the same part of the brain is concerned with tactile and electrosensory processing
(Iggo et al., 1992).
In our own study of the central projection of
electroreceptor and mechanoreceptor information,
we made an observation whose significance we,
perhaps, did not fully appreciate at the time. We
studied the cortical activity evoked by combined
electrosensory and mechanosensory inputs from
the bill. When the two stimuli were delivered
successively, with a 45 ms interval between them,
cell discharges of comparable size were evoked.
When they were brought closer, to 20 ms, only
one of the stimuli evoked activity, regardless of
which way round it was done, but with no evidence
of summation between the two inputs (Fig. 2). It
suggested convergence, at the cortical level, of
electrosensory and mechanosensory information. If
so, it meant that electroreception was not associated with a unique sensation, rather some modified
form of tactile sensation. All of this again emphasised the closeness of the electrosensory and
mechanosensory systems in the platypus.
One additional clue about the function of the
electrosensory system was provided by Langner
and Scheich (1986). They used the metabolic
marker, deoxyglucose to show that, in response to
electrical stimulation of the bill, the rostro-caudal
stripes of electroreceptors were reproduced by
similar stripes of cells in the cortex. Jack Pettigrew
used these findings together with some observations of his own to put together a picture of how
the electrosensory system might be used by the
platypus to locate prey (Pettigrew et al., 1998).
U. Proske, E. Gregory / Comparative Biochemistry and Physiology Part A 136 (2003) 821–825
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Fig. 2. Interactions between electrosensory and tactile inputs to the cortex, recorded with an extracellular microelectrode. In the top
trace, a localised electrical stimulus (E) produced the first burst of impulses, while a mechanical stimulus delivered 45 ms later at the
same location on the bill surface (M, solid line) produced the second burst. In the trace below, when the mechanical stimulus (M,
dashed line) was delivered only 25 ms after the electrical, there was very little response to the mechanical stimulus. (Re-drawn from
Iggo et al., 1992.)
Here we describe the main points of this proposal
and add some speculations of our own.
2. Directionality
Unlike Gymnotid fish, which can only tell the
direction of the local electric field (Hopkins,
1993), platypus may be able to determine the
direction of the electric source. The evidence for
this is that, when presented with an electric field,
platypus make an immediate, rapid head movement towards the source of the field, always in the
correct direction, whether it is below or above the
bill or to the left or right of it (Pettigrew et al.,
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1998). However, for close objects, the direction of
the field and the source of the signal are probably
the same and it is not certain which of them the
platypus is detecting. This behaviour of orienting
to an electric source has also been interpreted as
the animal exposing the most sensitive part of its
sensory epithelium to the stimulus, in an attempt
to locate the prey. The platypus continues to make
side-to-side head movements as it approaches the
prey. As it does this, it may be able to remember
and compare signal strength differences between
the receptor rows across the bill. The subtractive
signal will switch sign as the head moves from
side to side. When the difference signal is zero,
the bill is aimed directly in the direction of the
local electric field, which is then followed to the
target, in a similar way to that proposed by
Hopkins for Hypopomus. Another speculation is
that the side-to-side head movements are a means
of converting a DC into an AC signal to aid in
detecting weak electric fields.
3. Distance
The proposed mechanism for distance computation is based on the presence in the cortex of
bimodal, electrosensory and mechanosensory neurones. Jack Pettigrew has speculated that these
bimodal cells are tuned to respond preferentially
to a select interval between the incoming electrosensory and mechanosensory signals. When a prey
item such as the freshwater shrimp flicks its tail,
the electrical signal, generated by the muscle
electromyogram, reaches the bill first, to stimulate
electroreceptors. At a delay, determined by the
water propagation velocity of the pressure wave
accompanying the tail flick, the mechanoreceptors
will be stimulated. Subsequently cortical neurones,
preferentially responsive to the two inputs at the
given delay, will become active, providing a direct
readout of how far away the shrimp is. An additional distance cue might be the decay of electric
field strength across the bill. For distant electric
sources, the difference in potential between different parts of the bill would be relatively less than
for close sources. The side-to-side head movements the platypus makes while swimming could
also perhaps aid in distance detection, because the
change in field strength at a point on the bill as it
sweeps from side to side would be greater for
close sources than that for distant sources.
4. Close-range operation
Watching a platypus fossicking about on the
bottom of a stream or lake, gives the impression
that it most commonly uses its bill receptor apparatus for close-range detection of prey. Presumably
as it digs amongst stones and detritus, the mechanosensory system will be continuously stimulated
by both animate and inanimate objects. It may be
that detection of electrical signals at close range
allows the platypus to distinguish between the two.
The location of animate objects very close to the
bill could be signalled by simple place coding,
using the electroreceptors.
Perhaps a similar role can be assigned to the
electroreceptors known to be present in the snout
of the echidna (Gregory et al., 1989b). Electroreception in this terrestrial animal has remained
something of a puzzle, since it is uncertain whether
there are electric fields in the echidna’s natural
environment strong enough to stimulate the electroreceptors. Perhaps field strength in the immediate vicinity of some prey items is sufficient to
activate the receptors, which in this short-range
mode could help identify living prey as the echidna
pushes its snout into and through the soil while
searching for food (Griffiths, 1968). In other
words, it may be that the close-range mode of
operation of the electroreceptors is available to
both the platypus and echidna while the detection
of more distant electric sources may be unique to
the platypus.
5. Conclusions
The above discussions raise the question of how
the platypus uses its electrosensory system, whether in close-range mode, or for detection of prey at
a distance. Probably it is able to do both. Platypus
catch their prey at night, often in murky water, so
that visual detection by the prey of the approaching
platypus is unlikely. It means that the platypus can
get quite close without being detected.
But this remains speculation and some of these
ideas should, in the future, be the subject of
experiments. Questions for consideration are as
follows: Why is the activity evoked in the cortex
from stimulation of the bill edge so much greater
than from the upper surface of the bill? Why is
the frequency response of cortical electroreceptive
neurones (30 Hz) so much higher than for mechanosensory neurones (-10 Hz)? Are there distinct
U. Proske, E. Gregory / Comparative Biochemistry and Physiology Part A 136 (2003) 821–825
central projection pathways for electrosensory and
mechanosensory information? Such a parallel projection pathway is a necessary prerequisite for any
distance detection system based on central processing of stimulus intervals. All of these questions
remind us of how much there is still to learn about
the function of this unique system in a very
remarkable animal.
References
Andres, K.H., von During, M., 1984. The platypus bill. A
structural and functional model of a pattern-like arrangement
of different cutaneous sensory receptors. Sensory Receptor
Mechanisms. World Scientific, Singapore.
Bohringer, R.C., Rowe, M.J., 1977. The organization of the
sensory and motor areas of cerebral cortex in the platypus
(Ornithorhynchus anatinus). J. Comp. Neurol. 174, 1–14.
Burrell, H., 1927. The Platypus. Angus & Robertson, Sydney,
Australia.
Gregory, J.E., Iggo, A., McIntyre, A.K., Proske, U., 1988.
Receptors in the bill of the platypus. J. Physiol. 400,
349–366.
825
Gregory, J.E., Iggo, A., McIntyre, A.K., Proske, U., 1989.
Responses of electroreceptors in the platypus bill to steady
and alternating potentials. J. Physiol. 408, 391–404.
Gregory, J.E., Iggo, A., McIntyre, A.K., Proske, U., 1989.
Responses of electroreceptors in the snout of the echidna.
J. Physiol. 414, 521–538.
Griffiths, M., 1968. Echidnas. Pergamon, Oxford.
Hopkins, C.D., 1993. Neuroethology of passive electrolocation.
J. Comp. Physiol. 173, 689–695.
Iggo, A., Gregory, J.E., Proske, U., 1992. The central projection
of electrosensory information in the platypus. J. Physiol.
447, 449–465.
Langner, G., Scheich, H., 1986. Electroreceptive cortex of
platypus marked by 2-deoxyglucose. First Int. Cong. Neuroethol. 63.
Pettigrew, J.D., 1999. Electroreception in monotremes. J. Exp.
Biol. 202, 1447–1454.
Pettigrew, J.D., Manger, P.R., Fine, S.L., 1998. The sensory
world of the platypus. Philos. Trans. R. Soc. Lond. B Biol.
Sci. 353, 1199–1210.
Proske, U., Gregory, J.E., Iggo, A., 1998. Sensory receptors in
monotremes. Phil. Trans. R. Soc. B 353, 1187–1198.
Scheich, H., Langner, G., Tidemann, C., Coles, R.B., Guppy,
A., 1986. Electroreception and electrolocation in the platypus. Nature 319, 401–402.