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Phil. Trans. R. Soc. B (2011) 366, 3016–3025
doi:10.1098/rstb.2011.0128
Review
The sense of touch in the star-nosed mole:
from mechanoreceptors to the brain
Kenneth C. Catania*
Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA
Star-nosed moles are somatosensory specialists that explore their environment with 22 appendages
that ring their nostrils. The appendages are covered with sensory domes called Eimer’s organs. Each
organ is associated with a Merkel cell – neurite complex, a lamellated corpuscle, and a series of 5– 10
free nerve endings that form a circle of terminal swellings. Anatomy and electrophysiological recordings suggest that Eimer’s organs detect small shapes and textures. There are parallels between the
organization of the mole’s somatosensory system and visual systems of other mammals. The centre
of the star is a tactile fovea used for detailed exploration of objects and prey items. The tactile fovea
is over-represented in the neocortex, and this is evident in the modular, anatomically visible representation of the star. Multiple maps of the star are visible in flattened cortical preparations
processed for cytochrome oxidase or NADPH-diaphorase. Star-nosed moles are the fastest
known foragers among mammals, able to identify and consume a small prey item in 120 ms.
Together these behavioural and nervous system specializations have made star-nosed moles an
intriguing model system for examining general and specialized aspects of mammalian touch.
Keywords: somatosensory; tactile; skin; neocortex; evolution
1. INTRODUCTION
Important advances in our understanding of nervous
system function and organization have often come from
studies of specialized species. Perhaps, the best-known
example is the use of the squid giant axon by Hodgkin
& Huxley [1] to determine the ionic basis of action potential conduction. Other well-known examples include
studies of barn owls for determining the neural substrate
of auditory localization [2], investigations of the bird
song system for exploring the interaction between
environmental stimuli and brain development [3,4],
and use of electric fish for determining the computational
rules that underlie motor responses [5–7]. In the case of
mammalian touch, the landmark study by Woolsey &
Van der Loos [8] identifying cortical barrels in the
mouse somatosensory system led to the development
of rats and mice as important model systems
for understanding mechanosensation and brain organization in mammals. This system, in particular, continues
to provide new insights spanning the fields of molecular
biology, neurosciences and robotics [9–14]. Each of
the species listed above is particularly good at some
behaviour—rapidly escaping from a host of predators
(squid), detecting prey based on sound (owls) or exploring and navigating dark surroundings through touch
(rodents).
A glance at the astonishing face of a star-nosed mole
suggests that it too may be an expert at some task
(figure 1a). The nose of this species is ringed by
*[email protected]
One contribution of 18 to a Theo Murphy Meeting Issue ‘Active
touch sensing’.
22 fleshy appendages that are in constant motion as
the mole explores its environment. But the function
of the star is not immediately obvious and it is natural
to wonder what this structure is for, how and why it
evolved, and what it might tell us about mammalian
sensory systems. These questions are addressed by
drawing on evidence ranging from the mole’s habitat
and behaviour to single unit neuronal recordings.
The picture that emerges suggests that star-nosed
moles are an extreme in mammalian evolution, with
perhaps the most sensitive mechanosensory system to
be found among mammals. As might be expected,
the star projects to greatly expanded areas of the somatosensory neocortex and these areas are organized into
modules that correspond to the sensory appendages in
the periphery, much like the barrel system in rodents.
But unlike the rodent somatosensory system, details
of the mole’s brain maps are more typical of a visual
system than a somatosensory system, and this in turn
can be explained by star-nosed mole behaviour. Comparative studies across species reveal intermediate
forms that link the star to other mammalian skin surfaces, suggesting how this structure evolved from the
more common configurations of mammalian skin.
2. STRUCTURE AND EVOLUTION OF THE STAR
Star-nosed moles are relatively small mammals, weighing 40 – 50 g. The star itself is roughly a centimetre
across (figure 1), and thus has a diameter slightly smaller than a typical human fingertip. Examination of the
star under the scanning electron microscope (SEM),
or in tissue sections, reveals a remarkably specialized
epidermis consisting entirely of small raised domes
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Review. Touch in the star-nosed mole
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(c)
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Merkel-cell
lamellated corpuscle
free nerve ending
epidermis
Eimer’s organs
star-nosed
mole
(Condylura)
coast mole
(Scapanus)
eastern mole
(Scalopus)
opossum
(Didelphis)
50 µm
Figure 1. Sensory specializations of moles. (a) The front of a star-nosed mole emerging from a tunnel. The nose is ringed by 22
appendages that surround the nostrils. (b) Scanning electron micrograph of the star showing the numbered appendages [1–11]
covered with thousands of small Eimer’s organs. (c) A single Eimer’s organ from the star-nosed mole at higher magnification
showing the domed shape and circle representing the top of an epidermal cell column in the centre. (d ) A coast mole (Scapanus
orarius) showing a less-specialized nose. (e) The coast mole nose under the scanning electron microscope showing the Eimer’s
organ arrayed in a series of modular subdivisions. This configuration resembles an early developmental stage of the star,
suggesting the star’s ancestral condition. ( f ) A single Eimer’s organ of the coast mole under the scanning microscope. (g)
A comparison of Eimer’s organs and similar structures—all shown at the same scale. The left two cases show the internal
organization of Eimer’s organs of the star-nosed mole and coast mole. The eastern mole has degenerated Eimer’s organs,
most likely due to drier, more abrasive soil in its habitat. The far right example is a reconstruction of the anatomy and associated sensory receptors of an opossum. This illustrates the similarity of Eimer’s organ to receptor arrays found in a wider range
of species.
approximately 30– 50 mm in diameter (figure 1c).
These domes are Eimer’s organs, a sensory structure
found in nearly all of the approximately 30 species of
mole [15]. Each organ appears as a dome or papilla
containing a central column of epidermal cells.
Under the SEM, the top of the cell column is often visible on the outer surface of each organ as a small circle.
There are approximately 25 000 Eimer’s organs on a
typical star, and each organ is associated with a
Merkel cell – neurite complex at the base of the cell
Phil. Trans. R. Soc. B (2011)
column, a lamellated corpuscle in the dermis just
below the column, and a series of free nerve endings
that originate from myelinated fibres in the dermis
and run through the central column, ending in a ring
of terminal swellings just below the outer keratinized
skin surface (figure 1g, left side). In addition, a ring
of thinner free nerve endings is usually found at the
margins of each Eimer’s organ.
From these observations some important conclusions
can be drawn. For example, the star is devoted entirely
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Review. Touch in the star-nosed mole
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Figure 2. Mechanosensory receptive fields on the snouts of moles. (a) Examples of receptive fields on the star as determined by
multi-unit microelectrode recording from the primary somatosensory cortex (from data in Sachdev & Catania [18]). The mean
receptive field size for the 11th appendage (0.59 mm2, n ¼ 25) was significantly smaller than for the appendages 1 –10
(0.82 mm2 n ¼ 30). (b) Receptive fields on the coast mole snout determined by single unit recording from the trigeminal
ganglion (from data in Marasco & Catania [19]).
to Eimer’s organs and no other receptor organs (e.g.
taste buds, ampullary organs, hair cell, etc.) are present.
Thus, although the star is unique in its shape and size,
the epidermis that comprises the structure is similar to
that found in a wide range of other moles (figure 1d,e).
The star is therefore a variation on a more common
theme—the existence of sensitive epidermal sensory
organs (Eimer’s organs) on the tip of the snout. A further
comparison to shrews (the closely related sister group to
moles) suggests the major overall difference between
moles and other small mammals that led to the evolution
of the star [15]. Shrews and rodents (and many other
small mammals) rely primarily on facial whiskers to
gather tactile information, whereas moles use direct contact of the glabrous skin to explore their environment
(in addition to using whiskers). Once the ‘tactile shift’
from whiskers to glabrous skin began in ancestral
moles, selection could act on the nose to produce more
and more elaborate skin surfaces and ultimately the
star. This scenario is supported by the examination of
the diversity of epidermal sensory organs in moles,
including the existence of one species with a ‘protostar’
configuration (figure 1d,e). Adults of the latter species
(genus Scapanus) have a snout that resembles the star
during embryonic development [16].
In a sense, the star may be to glabrous skin what
whiskers are to hair—an extension and expansion of
an already sensitive structure. If so, why do not more
species of mammals—moles in particular—have elaborate sensory appendages? It is difficult to identify
the many selective pressures and tradeoffs that might
lead to such a structure. But one factor is obvious—
thin skin is delicate. The two most obvious functions
of skin are to act as a sensory surface and to protect
the underlying tissues from desiccation and abrasion.
These two functions are at odds with one another in
the case of Eimer’s organs. In wild caught moles of
many species, the Eimer’s organs show obvious signs
of wear and abrasion [15]. The constant and repeated
contact with the soil apparently takes a toll on the sensory organs, which have a thin keratinized epidermis.
Star-nosed moles are the only species that live in the
moist, muddy soil of wetlands. The high humidity
Phil. Trans. R. Soc. B (2011)
and soft mud in this particular niche may have lessened a major constraint on how elaborate the skin
surface could become. These issues are less of a constraint on whiskers, which consist of long, keratinized
extensions with the mechanoreceptors embedded in
the skin at the base, well protected from the environment. In the case of star-nosed moles, another factor
that probably led to elaboration of the snout was the
small prey that can be found in wetlands [17]. Exploiting this resource requires a higher resolution sensory
surface than is typical of other moles. Thus, a shift
to the wetland environment may have provided both
a selective advantage for a more elaborate sensory
structure, and the release of a constraint (less abrasive
soil) that allowed this structure to evolve.
3. FUNCTION OF EIMER’S ORGANS
Evidence for the mechanosensory function of Eimer’s
organs comes from a number of sources. Mole behaviour suggests that Eimer’s organs are mechanosensory
organs. But more direct evidence comes from electrophysiological recordings and from anatomical
investigations of the central and peripheral nervous
systems. In the case of star-nosed moles, recordings
from somatosensory cortex [18] show that each appendage is sensitive to very light tactile stimulation, and
neurons have tiny receptive fields that must be defined
under microscopic examination (figure 2). Unit
recordings from 145 spontaneously active neurons in
primary somatosensory cortex (S1) revealed that
97 per cent responded to tactile stimulation of the
star with a mean latency of 11.6 ms. A fairly large proportion of these neurons (41%) were inhibited by
stimulation of nearby Eimer’s organs outside of their
excitatory receptive field. The small receptive fields
and inhibitory surrounds for cortical neurons with
short latency responses are consistent with a role
for the star in rapidly determining the location and
identity of objects in the environment.
Additional evidence of Eimer’s organ function
comes from recordings of primary afferents innervating Eimer’s organ in the coast mole (Scapanus
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(a)
(b)
texture 1
(c)
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texture 2
Figure 3. A hypothetical role for Eimer’s organ in detecting shapes and textures. (a) Confocal microscopy of fluorescently
labelled (DiI) terminal nerve fibres at the apex of the cell column in the star-nosed mole Eimer’s organ as viewed from
above. The fibres terminate in a concise geometric ‘hub-and-spoke’ pattern that may provide for differential transduction of
directional deflection. (b,c) Side view schematics of Eimer’s organ cell columns and associated nerve terminals being deflected
by two different stimuli. The circles at the bottom represent the proposed stimulation patterns (light circles) for the ring of
nerve terminals in each case. Rougher textures and small shapes (b) result in nerve terminals at different radial positions in
the ring being maximally stimulated, whereas smoother textures more often result in similar radial positions being stimulated
in adjacent organs.
orarius). This study made use of a dedicated ‘Chubbuck’ mechanosensory stimulator [20] and revealed
three main classes of receptor [19]. These included
one slowly adapting type and two apparently different
rapidly adapting types. The slowly adapting responses
were similar to the typical response profile of a Merkel
cell – neurite complex and are consistent with the large
number of this receptor class evident from the anatomy of Eimer’s organ (figure 1g). The rapidly
adapting responses included a Pacinian-like response
profile with maximum sensitivity to sinusoidally compressive stimuli at a frequency of 250 Hz. These
responses are also consistent with anatomical findings,
as each Eimer’s organ is associated with one or more
lamellated corpuscles in the dermis just under the central cell column. These receptors appear much like
small Pacinian corpuscles and are probably rapidly
adapting receptors. A second class of rapidly adapting
responses required greater compression amplitude and
was maximal at lower frequencies of simulation. These
may correspond to the free nerve endings that terminate in swellings just below the keratinized epidermis at
the apex of the cell column (see Marasco & Catania
[19] for discussion). In addition to these findings,
neuroanatomical details suggest a mechanosensory
role for some, but not all, components of Eimer’s
organ. Marasco et al. [21] found that the nerve endings
associated with the central cell column in coast moles
are immunoreactive for neurofilament 200, consistent
with a mechanosensory role. In contrast, a ring of
thinner fibres on the margins of each Eimer’s organ
(figure 1g) was immunoreactive for substance P,
indicating a role in nociception.
An additional important finding from afferent
responses was directional sensitivity for many isolated
units. This was explored using a computer-controlled
piezo bending element [19], and significant directional
sensitivity was found for 15 of 17 isolated units. Previous investigators have speculated that the
conspicuous ring of free nerve endings at the apex of
each Eimer’s organ—also found in the apparently
independently derived push-rod in monotremes
[22]—may transduce directional information [23].
The data from afferent responses support this possibility; however, it is important to keep in mind that
Phil. Trans. R. Soc. B (2011)
moles do not slide Eimer’s organs over objects when
exploring them. Rather the unit of behaviour is
repeated brief touches that compress the organs
against objects or the substrate. In the course of natural behaviours, the directional sensitivity may be an
important component of Eimer’s organ function.
Indeed, incorporating this component of the response
into a relatively simple model suggests one way in
which Eimer’s organs may function to allow rapid discrimination of objects in the mole’s environment.
Figure 3 provides a basic outline of how these
responses, integrated across an array of Eimer’s
organs, could code for different shapes and textures.
The main feature of this proposal is the differential
deflection of the terminal neurites (figure 3a) at the
apex of each cell column. In this model, an important
variable is the number of terminal neurites deflected in
opposition to one-another relative to the number of
neurites deflected in the same direction (figure 3b,c).
Presumably, rough surfaces would predominantly
elicit the former response, whereas smooth surfaces
would elicit the latter. But are the Eimer’s organs
deflected as suggested in this model?
One way to address this question is to compress the
star against an object (post-mortem) and fix the skin
surface, so that the positions of organs can be directly
observed under the SEM. This was done using a fine
wire with a diameter of 120 mm (figure 4). The results
reveal how the Eimer’s organs were mechanically
deformed by the stimulus and suggest that the central
cell columns containing the array of terminal neurite
swellings would indeed be compressed as suggested
in figure 3. This is emphasized by illustrating the top
of each cell column independently (the circular disc
at the apex of each organ is a single epidermal cell
that can be traced). Figure 4c shows this, carefully
drawn from a high-resolution image of figure 4b,
with the resulting surfaces individually scaled by 200
per cent to aid visualization. The tops of the cell columns are clearly deflected by the cylindrical shape
such that contacted areas change their position and
angle relative to one another (centre of figure 4b),
whereas un-contacted cell columns (left and right of
figure 4b) remain more uniform with surfaces roughly
tangential to the skin surface.
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(a)
100 µm
(b)
100 µm
(c)
100 µm
Figure 4. Scanning electron micrograph of Eimer’s organs
deflected by a 120 mm cylindrical object (wire) during the
fixation process and the resulting deflection of Eimer’s
organs. (a) One hundred and twenty micrometre wire used
to contact the skin surface, at the same scale as the Eimer’s
organs. (b) Deformation of the skin surface caused by compression against the wire during the fixation process. (c)
Illustration of how the individual cell columns in ‘(b)’ were
deflected. For each Eimer’s organ in (b), the top of the cell
column was outlined as a black disc. To aid visualisation,
each disc was then doubled in size. A clear pattern of
Eimer’s organ deflection is evident where contact was
made with the wire, whereas surrounding areas (left and
right) remain more uniform.
Phil. Trans. R. Soc. B (2011)
4. ORGANIZATION OF SOMATOSENSORY
CORTEX
Investigation of the star and the very dense innervation
of associated sensory organs immediately suggested
that interesting correlates of this sensory surface
might be found in the mole’s somatosensory cortex.
This possibility followed from the landmark findings
of Woolsey & Van der Loos [8] showing that each
whisker on the face of a mouse is represented by a histologically visible cortical barrel. To explore this
possibility in moles, maps of the star and other sensory
surfaces (figure 5) were determined with microelectrode recordings and later correlated with flattened
sections of the neocortex processed for the metabolic
enzyme cytochrome oxidase (CO). The results
revealed a remarkable pattern of stripes and modules
in layer 4 that correspond to the star and other sensory
surfaces on the mole [24]. We have since found that a
number of histological stains of the cortex reveal such
modules in mole cortex. For example, figure 5b shows
the modular organization of the mole’s layer 4 cortex
as revealed by NADPH-diaphorase histochemistry.
A number of striking specializations were apparent
from both the electrophysiological recordings and
the anatomical sections of flattened cortex. Most
obviously, the star representation in primary somatosensory cortex is patently visible as a series of dark
stripes, each stripe representing an appendage from
the nose. A second obvious and apparently unique
feature of star-nosed mole somatosensory cortex is
the presence of additional, visible maps. Just lateral to S1, in secondary somatosensory cortex (S2), a
second, large visible map of the star is evident. Electrophysiolgical mapping shows that this representation,
like that in S1, processes inputs from only the contralateral side of the star. This map is distinct from S1 in
its cyto and chemo architecture (figure 5). Finally, a
third, smaller map of the star is visible caudal to the
S2 representation (S3 in figure 5). Thus unlike
rodents, which have a series of barrels visible only in
S1, star-nosed mole neocortex contains three visible
maps of the star. The most medial and rostral map
of the star clearly corresponds to S1. This conclusion
is based on many features, including its location relative to the other areas, its prominent architecture and
size, its continuity with the body representation
found more medially in the typical position of S1 in
most mammals and its ‘handedness’. The latter
refers to the topographic relationships of the star
appendages in the representation, which are appropriate for S1 [25]. In contrast, the S2 star representation
is a mirror image of the S1 pattern, and cannot be
superimposed on the S1 pattern by translation or
rotation. Thus S2’s star topography is inconsistent
with S1 ‘handedness’ as found in other mammals.
The third star representation has been termed S3
(star 3) as it is apparently not homologous to any
area in other moles nor to areas in the sister group of
shrews, which appear to have only S1 and S2 representing the face and body parts. Therefore, the most
parsimonious conclusion is that the third star-map
has evolved independently in the star-nosed mole, perhaps as a result of the need to process high volumes of
complex sensory information from the star. Injections
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(a)
star-nosed mole (C. cristata)
tail
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Figure 5. Anatomical modules and septa in layer 4 cortex of the star-nosed mole as revealed by processing sections for NADPHdiaphorase and cytochrome oxidase (CO) histochemistry. (a) Summary of cortical organization in the star-nosed mole based on
multi-unit electrophysiological mapping. Two relatively large somatosensory areas (primary, S1, and secondary, S2) contain
complete maps of the contralateral body and large representations of the star. A third, apparently new representation of the star
(S3) is found in lateral cortex. (b) A series of modules and stripes correspond to different body parts in flattened sections processed
for NADPH-diaphorase histochemistry. The most obvious part of the pattern corresponds to the S1 star representation [1–11].
(c) A different case processed for CO also reveals the three different, visible representations of the contralateral star.
Phil. Trans. R. Soc. B (2011)
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of neuroanatomical tracers into the S1 representation of
the star have shown that all three representations are
topographically interconnected, forming a processing
network for somatosensory inputs from the star [26].
The specific role of these different star maps has yet
to be elucidated; however all three areas are responsive
to tactile stimulation of the contralateral star.
An additional intriguing finding is evident from even
casual inspection of the flattened cortical sections. The
11th, central appendage of the star is greatly overrepresented, taking up approximately 25 per cent of the
S1 star map, despite its relatively small size on the snout
and comparatively few sensory organs (figure 1b). A similar expansion of the 11th is evident in S2 (figure 5c). The
representation of the 11th appendage is so greatly
enlarged relative to its proportions on the star that the
first views of the flattened cortex were hard to interpret.
It did not seem possible that such a large anatomical
module could correspond to such a small appendage.
Yet, electrophysiological recording clearly showed that
this was the case. The reason for this mismatch was
suggested by observing mole behaviour.
5. A TACTILE FOVEA IN THE STAR-NOSED MOLE
When star-nosed moles explore their environment or
search for food, the star is constantly touched to different objects or prey items. This behaviour is extremely
fast such that moles may touch between 10 and
15 different places every second. High-speed video of
this behaviour reveals that the 11th appendage acts as
a tactile fovea and is used to repeatedly explore objects
of interest—particularly potential prey. When foraging,
moles search in what appears to be a random pattern
of touches until contact is made to a potential prey
item with any part of the star. Each touch is a discrete
unit of behaviour lasting 20 – 30 ms. Once contact is
made—usually with some part of the large appendages
1 through 9—the star is quickly shifted, so that one
or more touches are made with appendage 11 before
prey is eaten. In the case of small prey, this entire
sequence is remarkably fast. A mole can detect potential prey with the peripheral appendages, foveate to
the central 11th appendage for an additional contact,
take the food into its mouth, and begin to search for
more prey in as little as 120 ms, although the average
time is 227 ms [17]. The sequence just described constitutes ‘handling time’ as defined in foraging theory
paradigms [27]. In all of hundreds of trials analysed
with high-speed video, the mole always foveated to
the 11th appendage when exploring a food item [28].
In a number of trials, moles foveated to rubber distractors before rejecting them. The use of the 11th
appendage as the tactile fovea was surprisingly similar
to the manner in which eyes are used to explore details
of a visual scene [29]. For example, the rapid foveation
movements of the star have a time-course and form
similar to foveating eye movements (saccades). It is
quite appropriate to refer to these star movements as
saccades, given the analogous ‘foveating’ function of
the behaviour in moles and the meaning of saccade—a
jerky movement [30].
With these behavioural observations in mind, the
expanded representation of the 11th, foveal appendage
Phil. Trans. R. Soc. B (2011)
is less surprising, and might be predicted. However,
these findings raise additional fundamental questions
about how central representations of sensory surfaces are
organized. For example, previous studies in mouse
somatosensory cortex have convincingly shown that the
size of a cortical barrel in S1 is directly proportional to
the number of primary afferents innervating the corresponding whisker on the face [31,32]. This suggests the
possibility that afferent number determines cortical representational size generally, and (if so) that cortical
magnification is perhaps more appropriately referred to
as a ‘peripheral scaling factor’—as suggested by Lee &
Woolsey [33] for the barrel system. But in the case of
the primate visual system, the same question was asked
with varying results coming from different laboratories.
Some investigators concluded that the representation
of the retinal fovea was proportional to the number of
ganglion cells in the retina [34–36], whereas others
reported a preferential expansion of the fovea [37–40].
These different results from different studies are a testament to the difficulty of making such measurements in
the visual system of primates. Azzopardi & Cowey [41]
ultimately resolved this issue by making injections of a
retrograde transneuronal tracer into the visual cortex,
and reported a preferential expansion of the foveal representation. They found that ganglion cells from the
retinal foveal were allocated an average of three to six
times more cortical territory in V1 than ganglion cells
at more peripheral locations in the retina.
Star-nosed moles are a particularly convenient and
interesting case for similar investigations because
measurements of afferent number and cortical area
can be made with comparative ease. A single large
branch of the trigeminal nerve innervates each appendage, and the corresponding representation of the
appendage is visible in the cortical anatomy (as is the
case for mouse whiskers). In addition, the number of
sensory organs on each star appendage can be counted
to provide another dimension of analysis—revealing
how the sensory periphery is differentially specialized
across the star [42].
As expected from its size, the 11th appendage
has comparatively few Eimer’s organs on its surface
(figure 6). Most of the appendages have over 1000
organs, whereas appendage 11 has an average of 870
on its surface (only appendage 10 has fewer). When
these counts of Eimer’s organs are compared with the
numbers of primary afferents innervating each appendage, a clear trend is evident. The two values covary
almost precisely for appendages 1–9—with an average
of four afferents per organ (figure 6d). But appendages
10 and 11 stand out with higher ratios of afferents per
organ with an average of 5.5 and 7, respectively. Thus,
appendage 11 has almost twice the innervation density
of most other appendages. This shows that the tactile
fovea is specialized in the periphery in a manner that
can be compared with a retinal fovea.
From these data, it might be guessed that the higher
innervation density accounts for the larger representation of no. 11 in the cortex. But closer consideration
of the numbers shows this is not possible. Although
appendage 11 has a higher innervation density per sensory organ, this is largely explained by its having a fairly
typical number of afferents (11% of the afferents
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average fibres per
Eimer’s organs
(d)
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2
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0
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7000
6000
5000
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ray number
(e)
average area of cortex
per afferent (mm2)
Eimer’s organs
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area of cortex in S1
(10 000 mm2)
(a)
K. C. Catania
1 2 3 4 5 6 7 8 9 10 11
ray number
80
70
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50
40
30
20
10
0
1 2 3 4 5 6 7 8 9 10 11
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60
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ray number
Figure 6. Graphical representation of the relationships of sensory organ number, afferent number and cortical area in S1 for
each of the 11 appendages (rays) of the star (means from four animals). (a) Total number of Eimer’s organ for each appendage.
(b) Total number of myelinated afferents for each appendage. (c) Cortical area representing each appendage in S1. (d) Average
number of fibres per sensory organ. Note the tactile fovea and nearby appendage 10 have greater innervation densities (dark
bars). (e) Average amount of S1 cortical area per fibre. In star-nosed moles, the area of cortex devoted to a sensory surface is
not dictated by innervation density. Data from Catania & Kaas [42].
innervating the star), but comparatively few total sensory
organs owing to its small size. Yet, the representation of
the 11th appendage takes up 25 per cent of the S1 star
representation. When the number of afferents from
each appendage is compared directly with the size of
each central representation, it is clear that the somatosensory fovea is preferentially over-represented in the cortex
(figure 6e). There is a general trend that the appendages
nearest the fovea have larger cortical areas per afferent
than the more peripheral appendages. The 11th appendage has the greatest over-representation, and the degree
of this expansion (three to four times greater than the
most peripheral appendages) is similar to that reported
for the retinal fovea in primates [41]. The overall organization of the mole’s somatosensory system and
behaviour, therefore, shares a number of surprising
similarities with visual systems in other mammals.
6. CONCLUSIONS AND FUTURE DIRECTIONS
Star-nosed moles provide many interesting new insights
into the organization, function and evolution of somatosensory systems and corresponding brain areas. The
existence of a tactile fovea in the star-nosed mole can
be compared with the well-known retinal fovea in other
mammals, and also with the acoustic fovea of bats.
Moustached bats have a well-characterized acoustic
fovea evident from the level of the cochlea [43] to the
auditory cortex [44], and Doppler shift compensation
behaviour [45] can be considered functionally equivalent
to a foveation movement. The existence of a foveaperiphery division of sensory surfaces in the visual,
auditory and somatosensory systems of different mammals suggests that this organizational scheme is an
Phil. Trans. R. Soc. B (2011)
efficient general solution to producing a very highresolution sensory system. An obvious benefit is that
only a small portion of the sensory surface need be
high-resolution, and only its corresponding representation in the central nervous system need have a large
representation for enhanced processing. A cost of this
organizational scheme is the requirement of constant
reorientation of the fovea to explore the environment
(or movement of the outgoing frequency of echolocation
calls in the case of bats [45]). But this is apparently a
small cost relative to the alternative of investing in
larger areas of high-resolution sensory surfaces in both
the periphery and corresponding central nervous
system representations.
In addition to extending evidence for this common
theme of sensory system organization to touch, starnosed moles provide potential insights into a number of
other areas of mammalian brain organization and behaviour. For example, it is clear in data from star-nosed
moles that cortical representational space is not always
directly proportional to peripheral innervation density.
Rather, as is true in visual systems, behaviourally important inputs may be allocated more territory. On a larger
scale, it appears that star-nosed moles have added a
somatosensory processing area to the cortical network
(compared with other moles and shrews). As in the
case of sensory foveas, this may also reflect a general organizing principle for efficient processing of sensory
information. Animals with particularly well-developed
senses often have many corresponding cortical areas,
and this is thought to underlie computational ability
and behavioural complexity. The subdivision of primate
visual cortex into many different areas provides a wellknown example [46–49]. In terms of auditory cortex,
Downloaded from http://rstb.royalsocietypublishing.org/ on June 18, 2017
3024
K. C. Catania
Review. Touch in the star-nosed mole
echolocating moustached bats have many auditory areas,
but appear to have few visual areas. A number of similar
examples could be suggested, but the significance of cortical areas may be difficult to interpret across species with
drastically different brain sizes or having distant phylogenetic relationships. In the case of the star-nosed mole, the
apparently new somatosensory area (S3, figure 6) not
found in close relatives [50] allows us to suggest more confidently that the modification was related to the expansion
of the star and corresponding search behaviours. This in
turn supports the proposal that adding cortical areas, in
general, may enhance sensory processing.
As a final example, the shapes of the modules in starnosed mole cortical maps indicate that not all sensory
surfaces are represented in the form of a traditional
cortical column [51]. Numerous investigators have
suggested that the fundamental unit of the cortex is a
cylindrical cortical column, sometimes called a macrocolumn, 300–600 mm in diameter with discrete
borders. The circular barrels described by Woolsey &
Van der Loos [8] have often been cited as anatomical
reflections of this general principle. But an alternative
explanation (also pointed out by Woolsey & Van der
Loos [8]) is that barrels simply reflect the somatotopic
mapping of mechanoreceptors that are organized into a
circular array around the whisker [52,53]. If so, one
would predict that mechanoreceptors organized into
different, non-circular arrangements would not appear
as columns. This is the case for star-nosed moles,
where the appendage representations appear as a series
of bands or stripes reflecting the anatomy of the star. A
similar, non-circular series of modules has also been
identified corresponding to the primate hand [54],
suggesting that a topographic, rather than strictly columnar, reflection of mechanoreceptor arrays is a widespread
phenomenon.
These examples indicate some ways that very
specialized star-nosed moles may provide new information about how mammalian sensory systems are
organized. These studies are still in their early stages,
and many questions remain to be explored. Some
obvious future questions include: (i) how the star is
represented in the trigeminal nuclei and thalamus,
(ii) what functional roles the different cortical maps
may play in processing tactile information, (iii) how
the Eimer’s organs quickly transduce information
about shape and texture, (iv) what role behaviour
might play in shaping the developing cortical maps,
and, (v) what transduction channels may be expressed
in mechanoreceptors of the star [55]. There is little
doubt that future studies of star-nosed moles will
provide a wealth of information about touch.
Supported by NSF grant no. 0844743.
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