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Phil. Trans. R. Soc. B (2011) 366, 3016–3025

doi:10.1098/rstb.2011.0128

Review

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One contouch se

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 appendagesthat ring their nostrils. The appendages are covered with sensory domes called Eimer’s organs. Eachorgan is associated with a Merkel cell–neurite complex, a lamellated corpuscle, and a series of 5–10free nerve endings that form a circle of terminal swellings. Anatomy and electrophysiological record-ings suggest that Eimer’s organs detect small shapes and textures. There are parallels between theorganization of the mole’s somatosensory system and visual systems of other mammals. The centreof the star is a tactile fovea used for detailed exploration of objects and prey items. The tactile foveais over-represented in the neocortex, and this is evident in the modular, anatomically visible rep-resentation of the star. Multiple maps of the star are visible in flattened cortical preparationsprocessed for cytochrome oxidase or NADPH-diaphorase. Star-nosed moles are the fastestknown 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 anintriguing model system for examining general and specialized aspects of mammalian touch.

Keywords: somatosensory; tactile; skin; neocortex; evolution

1. INTRODUCTIONImportant advances in our understanding of nervoussystem function and organization have often come fromstudies of specialized species. Perhaps, the best-knownexample is the use of the squid giant axon by Hodgkin& Huxley [1] to determine the ionic basis of action poten-tial conduction. Other well-known examples includestudies of barn owls for determining the neural substrateof auditory localization [2], investigations of the birdsong system for exploring the interaction betweenenvironmental stimuli and brain development [3,4],and use of electric fish for determining the computationalrules that underlie motor responses [5–7]. In the case ofmammalian touch, the landmark study by Woolsey &Van der Loos [8] identifying cortical barrels in themouse somatosensory system led to the developmentof rats and mice as important model systemsfor understanding mechanosensation and brain organiz-ation in mammals. This system, in particular, continuesto provide new insights spanning the fields of molecularbiology, neurosciences and robotics [9–14]. Each ofthe species listed above is particularly good at somebehaviour—rapidly escaping from a host of predators(squid), detecting prey based on sound (owls) or explor-ing and navigating dark surroundings through touch(rodents).

A glance at the astonishing face of a star-nosed molesuggests that it too may be an expert at some task(figure 1a). The nose of this species is ringed by

h.catania@vanderbilt.edu

tribution of 18 to a Theo Murphy Meeting Issue ‘Activensing’.

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22 fleshy appendages that are in constant motion asthe mole explores its environment. But the functionof the star is not immediately obvious and it is naturalto wonder what this structure is for, how and why itevolved, and what it might tell us about mammaliansensory systems. These questions are addressed bydrawing on evidence ranging from the mole’s habitatand behaviour to single unit neuronal recordings.The picture that emerges suggests that star-nosedmoles are an extreme in mammalian evolution, withperhaps the most sensitive mechanosensory system tobe found among mammals. As might be expected,the star projects to greatly expanded areas of the som-atosensory neocortex and these areas are organized intomodules that correspond to the sensory appendages inthe periphery, much like the barrel system in rodents.But unlike the rodent somatosensory system, detailsof the mole’s brain maps are more typical of a visualsystem than a somatosensory system, and this in turncan be explained by star-nosed mole behaviour. Com-parative studies across species reveal intermediateforms that link the star to other mammalian skin sur-faces, suggesting how this structure evolved from themore common configurations of mammalian skin.

2. STRUCTURE AND EVOLUTION OF THE STARStar-nosed moles are relatively small mammals, weigh-ing 40–50 g. The star itself is roughly a centimetreacross (figure 1), and thus has a diameter slightly smal-ler than a typical human fingertip. Examination of thestar under the scanning electron microscope (SEM),or in tissue sections, reveals a remarkably specializedepidermis consisting entirely of small raised domes

This journal is q 2011 The Royal Society

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Figure 1. Sensory specializations of moles. (a) The front of a star-nosed mole emerging from a tunnel. The nose is ringed by 22appendages 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 magnificationshowing the domed shape and circle representing the top of an epidermal cell column in the centre. (d) A coast mole (Scapanusorarius) 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 internalorganization 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 associ-

ated sensory receptors of an opossum. This illustrates the similarity of Eimer’s organ to receptor arrays found in a wider rangeof species.

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approximately 30–50 mm in diameter (figure 1c).These domes are Eimer’s organs, a sensory structurefound in nearly all of the approximately 30 species ofmole [15]. Each organ appears as a dome or papillacontaining a central column of epidermal cells.Under the SEM, the top of the cell column is often vis-ible on the outer surface of each organ as a small circle.There are approximately 25 000 Eimer’s organs on atypical star, and each organ is associated with aMerkel cell–neurite complex at the base of the cell

Phil. Trans. R. Soc. B (2011)

column, a lamellated corpuscle in the dermis justbelow the column, and a series of free nerve endingsthat originate from myelinated fibres in the dermisand run through the central column, ending in a ringof terminal swellings just below the outer keratinizedskin surface (figure 1g, left side). In addition, a ringof thinner free nerve endings is usually found at themargins of each Eimer’s organ.

From these observations some important conclusionscan be drawn. For example, the star is devoted entirely

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Figure 2. Mechanosensory receptive fields on the snouts of moles. (a) Examples of receptive fields on the star as determined bymulti-unit microelectrode recording from the primary somatosensory cortex (from data in Sachdev & Catania [18]). The meanreceptive 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 trigeminalganglion (from data in Marasco & Catania [19]).

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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 tothat found in a wide range of other moles (figure 1d,e).The star is therefore a variation on a more commontheme—the existence of sensitive epidermal sensoryorgans (Eimer’s organs) on the tip of the snout. A furthercomparison to shrews (the closely related sister group tomoles) suggests the major overall difference betweenmoles and other small mammals that led to the evolutionof the star [15]. Shrews and rodents (and many othersmall mammals) rely primarily on facial whiskers togather tactile information, whereas moles use direct con-tact of the glabrous skin to explore their environment(in addition to using whiskers). Once the ‘tactile shift’from whiskers to glabrous skin began in ancestralmoles, selection could act on the nose to produce moreand more elaborate skin surfaces and ultimately thestar. This scenario is supported by the examination ofthe 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 starduring embryonic development [16].

In a sense, the star may be to glabrous skin whatwhiskers are to hair—an extension and expansion ofan already sensitive structure. If so, why do not morespecies of mammals—moles in particular—have elab-orate sensory appendages? It is difficult to identifythe many selective pressures and tradeoffs that mightlead to such a structure. But one factor is obvious—thin skin is delicate. The two most obvious functionsof skin are to act as a sensory surface and to protectthe underlying tissues from desiccation and abrasion.These two functions are at odds with one another inthe case of Eimer’s organs. In wild caught moles ofmany species, the Eimer’s organs show obvious signsof wear and abrasion [15]. The constant and repeatedcontact with the soil apparently takes a toll on the sen-sory organs, which have a thin keratinized epidermis.Star-nosed moles are the only species that live in themoist, muddy soil of wetlands. The high humidity

Phil. Trans. R. Soc. B (2011)

and soft mud in this particular niche may have les-sened a major constraint on how elaborate the skinsurface could become. These issues are less of a con-straint on whiskers, which consist of long, keratinizedextensions with the mechanoreceptors embedded inthe skin at the base, well protected from the environ-ment. In the case of star-nosed moles, another factorthat probably led to elaboration of the snout was thesmall prey that can be found in wetlands [17]. Exploit-ing this resource requires a higher resolution sensorysurface than is typical of other moles. Thus, a shiftto the wetland environment may have provided botha selective advantage for a more elaborate sensorystructure, and the release of a constraint (less abrasivesoil) that allowed this structure to evolve.

3. FUNCTION OF EIMER’S ORGANSEvidence for the mechanosensory function of Eimer’sorgans comes from a number of sources. Mole behav-iour suggests that Eimer’s organs are mechanosensoryorgans. But more direct evidence comes from elec-trophysiological recordings and from anatomicalinvestigations of the central and peripheral nervoussystems. In the case of star-nosed moles, recordingsfrom somatosensory cortex [18] show that each append-age is sensitive to very light tactile stimulation, andneurons have tiny receptive fields that must be definedunder microscopic examination (figure 2). Unitrecordings from 145 spontaneously active neurons inprimary somatosensory cortex (S1) revealed that97 per cent responded to tactile stimulation of thestar with a mean latency of 11.6 ms. A fairly large pro-portion of these neurons (41%) were inhibited bystimulation of nearby Eimer’s organs outside of theirexcitatory receptive field. The small receptive fieldsand inhibitory surrounds for cortical neurons withshort latency responses are consistent with a rolefor the star in rapidly determining the location andidentity of objects in the environment.

Additional evidence of Eimer’s organ functioncomes from recordings of primary afferents innerv-ating Eimer’s organ in the coast mole (Scapanus

(a) (b) texture 1 texture 2(c)

Figure 3. A hypothetical role for Eimer’s organ in detecting shapes and textures. (a) Confocal microscopy of fluorescentlylabelled (DiI) terminal nerve fibres at the apex of the cell column in the star-nosed mole Eimer’s organ as viewed fromabove. The fibres terminate in a concise geometric ‘hub-and-spoke’ pattern that may provide for differential transduction ofdirectional deflection. (b,c) Side view schematics of Eimer’s organ cell columns and associated nerve terminals being deflectedby 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 inthe ring being maximally stimulated, whereas smoother textures more often result in similar radial positions being stimulatedin adjacent organs.

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orarius). This study made use of a dedicated ‘Chub-buck’ mechanosensory stimulator [20] and revealedthree main classes of receptor [19]. These includedone slowly adapting type and two apparently differentrapidly adapting types. The slowly adapting responseswere similar to the typical response profile of a Merkelcell–neurite complex and are consistent with the largenumber of this receptor class evident from the anat-omy of Eimer’s organ (figure 1g). The rapidlyadapting responses included a Pacinian-like responseprofile with maximum sensitivity to sinusoidally com-pressive stimuli at a frequency of 250 Hz. Theseresponses are also consistent with anatomical findings,as each Eimer’s organ is associated with one or morelamellated corpuscles in the dermis just under the cen-tral cell column. These receptors appear much likesmall Pacinian corpuscles and are probably rapidlyadapting receptors. A second class of rapidly adaptingresponses required greater compression amplitude andwas maximal at lower frequencies of simulation. Thesemay correspond to the free nerve endings that termin-ate in swellings just below the keratinized epidermis atthe apex of the cell column (see Marasco & Catania[19] for discussion). In addition to these findings,neuroanatomical details suggest a mechanosensoryrole for some, but not all, components of Eimer’sorgan. Marasco et al. [21] found that the nerve endingsassociated with the central cell column in coast molesare immunoreactive for neurofilament 200, consistentwith a mechanosensory role. In contrast, a ring ofthinner 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 afferentresponses was directional sensitivity for many isolatedunits. This was explored using a computer-controlledpiezo bending element [19], and significant directionalsensitivity was found for 15 of 17 isolated units. Pre-vious investigators have speculated that theconspicuous ring of free nerve endings at the apex ofeach Eimer’s organ—also found in the apparentlyindependently derived push-rod in monotremes[22]—may transduce directional information [23].The data from afferent responses support this possi-bility; however, it is important to keep in mind that

Phil. Trans. R. Soc. B (2011)

moles do not slide Eimer’s organs over objects whenexploring them. Rather the unit of behaviour isrepeated brief touches that compress the organsagainst objects or the substrate. In the course of natu-ral behaviours, the directional sensitivity may be animportant component of Eimer’s organ function.Indeed, incorporating this component of the responseinto a relatively simple model suggests one way inwhich Eimer’s organs may function to allow rapid dis-crimination of objects in the mole’s environment.Figure 3 provides a basic outline of how theseresponses, integrated across an array of Eimer’sorgans, could code for different shapes and textures.The main feature of this proposal is the differentialdeflection of the terminal neurites (figure 3a) at theapex of each cell column. In this model, an importantvariable is the number of terminal neurites deflected inopposition to one-another relative to the number ofneurites deflected in the same direction (figure 3b,c).Presumably, rough surfaces would predominantlyelicit the former response, whereas smooth surfaceswould elicit the latter. But are the Eimer’s organsdeflected as suggested in this model?

One way to address this question is to compress thestar against an object (post-mortem) and fix the skinsurface, so that the positions of organs can be directlyobserved under the SEM. This was done using a finewire with a diameter of 120 mm (figure 4). The resultsreveal how the Eimer’s organs were mechanicallydeformed by the stimulus and suggest that the centralcell columns containing the array of terminal neuriteswellings would indeed be compressed as suggestedin figure 3. This is emphasized by illustrating the topof each cell column independently (the circular discat the apex of each organ is a single epidermal cellthat can be traced). Figure 4c shows this, carefullydrawn from a high-resolution image of figure 4b,with the resulting surfaces individually scaled by 200per cent to aid visualization. The tops of the cell col-umns are clearly deflected by the cylindrical shapesuch that contacted areas change their position andangle relative to one another (centre of figure 4b),whereas un-contacted cell columns (left and right offigure 4b) remain more uniform with surfaces roughlytangential to the skin surface.

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deflected by a 120 mm cylindrical object (wire) during thefixation process and the resulting deflection of Eimer’sorgans. (a) One hundred and twenty micrometre wire usedto contact the skin surface, at the same scale as the Eimer’s

organs. (b) Deformation of the skin surface caused by com-pression against the wire during the fixation process. (c)Illustration of how the individual cell columns in ‘(b)’ weredeflected. For each Eimer’s organ in (b), the top of the cellcolumn was outlined as a black disc. To aid visualisation,

each disc was then doubled in size. A clear pattern ofEimer’s organ deflection is evident where contact wasmade with the wire, whereas surrounding areas (left andright) remain more uniform.

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4. ORGANIZATION OF SOMATOSENSORYCORTEXInvestigation of the star and the very dense innervationof associated sensory organs immediately suggestedthat interesting correlates of this sensory surfacemight be found in the mole’s somatosensory cortex.This possibility followed from the landmark findingsof Woolsey & Van der Loos [8] showing that eachwhisker on the face of a mouse is represented by a his-tologically visible cortical barrel. To explore thispossibility in moles, maps of the star and other sensorysurfaces (figure 5) were determined with microelec-trode recordings and later correlated with flattenedsections of the neocortex processed for the metabolicenzyme cytochrome oxidase (CO). The resultsrevealed a remarkable pattern of stripes and modulesin layer 4 that correspond to the star and other sensorysurfaces on the mole [24]. We have since found that anumber of histological stains of the cortex reveal suchmodules in mole cortex. For example, figure 5b showsthe modular organization of the mole’s layer 4 cortexas revealed by NADPH-diaphorase histochemistry.

A number of striking specializations were apparentfrom both the electrophysiological recordings andthe anatomical sections of flattened cortex. Mostobviously, the star representation in primary somato-sensory cortex is patently visible as a series of darkstripes, each stripe representing an appendage fromthe nose. A second obvious and apparently uniquefeature of star-nosed mole somatosensory cortex isthe presence of additional, visible maps. Just later-al to S1, in secondary somatosensory cortex (S2), asecond, large visible map of the star is evident. Electro-physiolgical mapping shows that this representation,like that in S1, processes inputs from only the contra-lateral side of the star. This map is distinct from S1 inits cyto and chemo architecture (figure 5). Finally, athird, smaller map of the star is visible caudal to theS2 representation (S3 in figure 5). Thus unlikerodents, which have a series of barrels visible only inS1, star-nosed mole neocortex contains three visiblemaps of the star. The most medial and rostral mapof the star clearly corresponds to S1. This conclusionis based on many features, including its location rela-tive to the other areas, its prominent architecture andsize, its continuity with the body representationfound more medially in the typical position of S1 inmost mammals and its ‘handedness’. The latterrefers to the topographic relationships of the starappendages in the representation, which are appropri-ate for S1 [25]. In contrast, the S2 star representationis a mirror image of the S1 pattern, and cannot besuperimposed on the S1 pattern by translation orrotation. Thus S2’s star topography is inconsistentwith S1 ‘handedness’ as found in other mammals.The third star representation has been termed S3(star 3) as it is apparently not homologous to anyarea in other moles nor to areas in the sister group ofshrews, which appear to have only S1 and S2 repre-senting the face and body parts. Therefore, the mostparsimonious conclusion is that the third star-maphas evolved independently in the star-nosed mole, per-haps as a result of the need to process high volumes ofcomplex sensory information from the star. Injections

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multi-unit electrophysiological mapping. Two relatively large somatosensory areas (primary, S1, and secondary, S2) containcomplete 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 processedfor 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.

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of neuroanatomical tracers into the S1 representation ofthe star have shown that all three representations aretopographically interconnected, forming a processingnetwork for somatosensory inputs from the star [26].The specific role of these different star maps has yetto be elucidated; however all three areas are responsiveto tactile stimulation of the contralateral star.

An additional intriguing finding is evident from evencasual inspection of the flattened cortical sections. The11th, central appendage of the star is greatly over-represented, taking up approximately 25 per cent of theS1 star map, despite its relatively small size on the snoutand comparatively few sensory organs (figure 1b). A simi-lar expansion of the 11th is evident in S2 (figure 5c). Therepresentation of the 11th appendage is so greatlyenlarged relative to its proportions on the star that thefirst views of the flattened cortex were hard to interpret.It did not seem possible that such a large anatomicalmodule could correspond to such a small appendage.Yet, electrophysiological recording clearly showed thatthis was the case. The reason for this mismatch wassuggested by observing mole behaviour.

5. A TACTILE FOVEA IN THE STAR-NOSED MOLEWhen star-nosed moles explore their environment orsearch for food, the star is constantly touched to differ-ent objects or prey items. This behaviour is extremelyfast such that moles may touch between 10 and15 different places every second. High-speed video ofthis behaviour reveals that the 11th appendage acts asa tactile fovea and is used to repeatedly explore objectsof interest—particularly potential prey. When foraging,moles search in what appears to be a random patternof touches until contact is made to a potential preyitem with any part of the star. Each touch is a discreteunit of behaviour lasting 20–30 ms. Once contact ismade—usually with some part of the large appendages1 through 9—the star is quickly shifted, so that oneor more touches are made with appendage 11 beforeprey is eaten. In the case of small prey, this entiresequence is remarkably fast. A mole can detect poten-tial prey with the peripheral appendages, foveate tothe central 11th appendage for an additional contact,take the food into its mouth, and begin to search formore prey in as little as 120 ms, although the averagetime is 227 ms [17]. The sequence just described con-stitutes ‘handling time’ as defined in foraging theoryparadigms [27]. In all of hundreds of trials analysedwith high-speed video, the mole always foveated tothe 11th appendage when exploring a food item [28].In a number of trials, moles foveated to rubber dis-tractors before rejecting them. The use of the 11thappendage as the tactile fovea was surprisingly similarto the manner in which eyes are used to explore detailsof a visual scene [29]. For example, the rapid foveationmovements of the star have a time-course and formsimilar to foveating eye movements (saccades). It isquite appropriate to refer to these star movements assaccades, given the analogous ‘foveating’ function ofthe behaviour in moles and the meaning of saccade—ajerky movement [30].

With these behavioural observations in mind, theexpanded 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 questionsabout how central representations of sensory surfaces areorganized. For example, previous studies in mousesomatosensory cortex have convincingly shown that thesize of a cortical barrel in S1 is directly proportional tothe number of primary afferents innervating the corres-ponding whisker on the face [31,32]. This suggests thepossibility that afferent number determines cortical rep-resentational size generally, and (if so) that corticalmagnification is perhaps more appropriately referred toas a ‘peripheral scaling factor’—as suggested by Lee &Woolsey [33] for the barrel system. But in the case ofthe primate visual system, the same question was askedwith varying results coming from different laboratories.Some investigators concluded that the representationof the retinal fovea was proportional to the number ofganglion cells in the retina [34–36], whereas othersreported a preferential expansion of the fovea [37–40].These different results from different studies are a testa-ment to the difficulty of making such measurements inthe visual system of primates. Azzopardi & Cowey [41]ultimately resolved this issue by making injections of aretrograde transneuronal tracer into the visual cortex,and reported a preferential expansion of the foveal rep-resentation. They found that ganglion cells from theretinal foveal were allocated an average of three to sixtimes more cortical territory in V1 than ganglion cellsat more peripheral locations in the retina.

Star-nosed moles are a particularly convenient andinteresting case for similar investigations becausemeasurements of afferent number and cortical areacan be made with comparative ease. A single largebranch of the trigeminal nerve innervates each append-age, and the corresponding representation of theappendage is visible in the cortical anatomy (as is thecase for mouse whiskers). In addition, the number ofsensory organs on each star appendage can be countedto provide another dimension of analysis—revealinghow the sensory periphery is differentially specializedacross the star [42].

As expected from its size, the 11th appendagehas comparatively few Eimer’s organs on its surface(figure 6). Most of the appendages have over 1000organs, whereas appendage 11 has an average of 870on its surface (only appendage 10 has fewer). Whenthese counts of Eimer’s organs are compared with thenumbers of primary afferents innervating each append-age, a clear trend is evident. The two values covaryalmost precisely for appendages 1–9—with an averageof four afferents per organ (figure 6d). But appendages10 and 11 stand out with higher ratios of afferents perorgan with an average of 5.5 and 7, respectively. Thus,appendage 11 has almost twice the innervation densityof most other appendages. This shows that the tactilefovea is specialized in the periphery in a manner thatcan be compared with a retinal fovea.

From these data, it might be guessed that the higherinnervation density accounts for the larger represen-tation of no. 11 in the cortex. But closer considerationof the numbers shows this is not possible. Althoughappendage 11 has a higher innervation density per sen-sory organ, this is largely explained by its having a fairlytypical number of afferents (11% of the afferents

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(b) Total number of myelinated afferents for each appendage. (c) Cortical area representing each appendage in S1. (d) Averagenumber of fibres per sensory organ. Note the tactile fovea and nearby appendage 10 have greater innervation densities (darkbars). (e) Average amount of S1 cortical area per fibre. In star-nosed moles, the area of cortex devoted to a sensory surface isnot dictated by innervation density. Data from Catania & Kaas [42].

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innervating the star), but comparatively few total sensoryorgans owing to its small size. Yet, the representation ofthe 11th appendage takes up 25 per cent of the S1 starrepresentation. When the number of afferents fromeach appendage is compared directly with the size ofeach central representation, it is clear that the somatosen-sory fovea is preferentially over-represented in the cortex(figure 6e). There is a general trend that the appendagesnearest the fovea have larger cortical areas per afferentthan the more peripheral appendages. The 11th append-age has the greatest over-representation, and the degreeof this expansion (three to four times greater than themost peripheral appendages) is similar to that reportedfor the retinal fovea in primates [41]. The overall organ-ization of the mole’s somatosensory system andbehaviour, therefore, shares a number of surprisingsimilarities with visual systems in other mammals.

6. CONCLUSIONS AND FUTURE DIRECTIONSStar-nosed moles provide many interesting new insightsinto the organization, function and evolution of somato-sensory systems and corresponding brain areas. Theexistence of a tactile fovea in the star-nosed mole canbe compared with the well-known retinal fovea in othermammals, and also with the acoustic fovea of bats.Moustached bats have a well-characterized acousticfovea evident from the level of the cochlea [43] to theauditory cortex [44], and Doppler shift compensationbehaviour [45] can be considered functionally equivalentto a foveation movement. The existence of a fovea-periphery division of sensory surfaces in the visual,auditory and somatosensory systems of different mam-mals suggests that this organizational scheme is an

Phil. Trans. R. Soc. B (2011)

efficient general solution to producing a very high-resolution sensory system. An obvious benefit is thatonly a small portion of the sensory surface need behigh-resolution, and only its corresponding represen-tation in the central nervous system need have a largerepresentation for enhanced processing. A cost of thisorganizational scheme is the requirement of constantreorientation of the fovea to explore the environment(or movement of the outgoing frequency of echolocationcalls in the case of bats [45]). But this is apparently asmall cost relative to the alternative of investing inlarger areas of high-resolution sensory surfaces in boththe periphery and corresponding central nervoussystem representations.

In addition to extending evidence for this commontheme of sensory system organization to touch, star-nosed moles provide potential insights into a number ofother areas of mammalian brain organization and behav-iour. For example, it is clear in data from star-nosedmoles that cortical representational space is not alwaysdirectly proportional to peripheral innervation density.Rather, as is true in visual systems, behaviourally import-ant inputs may be allocated more territory. On a largerscale, it appears that star-nosed moles have added asomatosensory processing area to the cortical network(compared with other moles and shrews). As in thecase of sensory foveas, this may also reflect a general or-ganizing principle for efficient processing of sensoryinformation. Animals with particularly well-developedsenses often have many corresponding cortical areas,and this is thought to underlie computational abilityand behavioural complexity. The subdivision of primatevisual cortex into many different areas provides a well-known example [46–49]. In terms of auditory cortex,

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echolocating moustached bats have many auditory areas,but appear to have few visual areas. A number of similarexamples could be suggested, but the significance of cor-tical areas may be difficult to interpret across species withdrastically different brain sizes or having distant phylogen-etic relationships. In the case of the star-nosed mole, theapparently new somatosensory area (S3, figure 6) notfound in close relatives [50] allows us to suggest more con-fidently that the modification was related to the expansionof the star and corresponding search behaviours. This inturn supports the proposal that adding cortical areas, ingeneral, may enhance sensory processing.

As a final example, the shapes of the modules in star-nosed mole cortical maps indicate that not all sensorysurfaces are represented in the form of a traditionalcortical column [51]. Numerous investigators havesuggested that the fundamental unit of the cortex is acylindrical cortical column, sometimes called a macro-column, 300–600 mm in diameter with discreteborders. The circular barrels described by Woolsey &Van der Loos [8] have often been cited as anatomicalreflections of this general principle. But an alternativeexplanation (also pointed out by Woolsey & Van derLoos [8]) is that barrels simply reflect the somatotopicmapping of mechanoreceptors that are organized into acircular array around the whisker [52,53]. If so, onewould predict that mechanoreceptors organized intodifferent, non-circular arrangements would not appearas columns. This is the case for star-nosed moles,where the appendage representations appear as a seriesof bands or stripes reflecting the anatomy of the star. Asimilar, non-circular series of modules has also beenidentified corresponding to the primate hand [54],suggesting that a topographic, rather than strictly colum-nar, reflection of mechanoreceptor arrays is a widespreadphenomenon.

These examples indicate some ways that veryspecialized star-nosed moles may provide new infor-mation about how mammalian sensory systems areorganized. These studies are still in their early stages,and many questions remain to be explored. Someobvious future questions include: (i) how the star isrepresented in the trigeminal nuclei and thalamus,(ii) what functional roles the different cortical mapsmay play in processing tactile information, (iii) howthe Eimer’s organs quickly transduce informationabout shape and texture, (iv) what role behaviourmight play in shaping the developing cortical maps,and, (v) what transduction channels may be expressedin mechanoreceptors of the star [55]. There is littledoubt that future studies of star-nosed moles willprovide a wealth of information about touch.

Supported by NSF grant no. 0844743.

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