Stars and Stripes in the Cortex

Star-nosed moles have an exceptionally well-developed somatosensory system allowing them to identify and consume small prey items faster than any other mammal (Catania and Remple, 2005). This ability stems from the densely innervated mechanosensory star covered by tens of thousands of tactile Eimer's organs (Catania, 1995). As occurs for whiskers in rodents, the specialized glabrous

Figure 1 Cortical barrels in the mouse as revealed by cytochrome oxidase histochemistry. In many rodents, the cortical representation, or map, of various body parts in primary soma-tosensory cortex (S1) can be made visible with a range of cellular stains when the cortex is flattened out and sectioned from the top down to reveal layer IV. a, The face of a mouse showing the prominent facial vibrissae. b, A section of flattened right cortex processed for the metabolic enzyme cytochrome oxidase to reveal the prominent cortical barrels in layer IV. Rostral is to the right and medial is up. The large facial vibrissae correspond to the barrels visible in the lower left quadrant, whereas the smaller facial whiskers are represented by the smaller, more rostral barrels.

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Figure 2 The relationship and pathways between the sensory vibrissae on the rodent snout and their representation in cortex by a series of barrels. Note the extra whisker illustrated on the left face of the mouse (right bottom side of figure) and the corresponding extra barrel in the contralateral somatosensory cortex. This observation inspired Van der Loos and Dorfl (1978) to suggest that the skin surface tells the somatosensory cortex how to construct a map of the sensory periphery.

Figure 2 The relationship and pathways between the sensory vibrissae on the rodent snout and their representation in cortex by a series of barrels. Note the extra whisker illustrated on the left face of the mouse (right bottom side of figure) and the corresponding extra barrel in the contralateral somatosensory cortex. This observation inspired Van der Loos and Dorfl (1978) to suggest that the skin surface tells the somatosensory cortex how to construct a map of the sensory periphery.

skin surface of the mechanosensory star is represented in somatosensory cortex by a series of modules that reflect the topographic arrangement of mechanosensors in the periphery. The modules appear as a series of stripes visible in flattened brain sections processed for the metabolic enzyme cyto-chrome oxidase (Figure 3; Catania et al., 1993). In star-nosed moles, histologically visible representations of the mechanosensory appendages are found in three separate cortical areas (S1, S2, and a third area we have called S3). Similar modular representations of skin surfaces (including the primate hand) have since been identified in other species as well (for review, see Catania, 2002).

The elaborate mechanosensory star and its multiple, modular representations in cortex are the result of comparatively recent selective pressure for the expansion of the somatosensory system (Catania, 2000; Catania and Remple, 2005). As a result this is a particularly useful species to examine when searching for clues to how peripheral receptor arrays and central brain organization have co-evolved to produce complex sensory systems that are functionally integrated.

Star-nosed moles usually have a complement of 22 appendages ringing the snout. These occur as 11 symmetric pairs that are numbered from 1 to 11 on each side, starting with the dorsal-most appendage (Figure 3). As is the case for laboratory rodents, star-nosed moles are sometimes born with an abnormal configuration of the snout. This often includes the loss or addition of an appendage to one side of the nose and, when this occurs, the contralateral somatosensory cortex (Figure 4) invariably reflects the topography of the abnormal star (Catania and Kaas, 1997a).

There are a number of interesting implications of this result. Most obviously, this finding parallels the results of Van der Loos and Dorfl (1978) supporting the contention that skin surfaces play an instructive

Figure 3 The sensory system of the star-nose mole. As occurs for the whiskers of rodents, the cortical representation of the mechanosensory appendages of the star-nosed mole is visible in various histological stains of the cortex. a, A front view of the star-nosed mole emerging from its underground burrow. Note the 22 appendages ringing the nostrils. b, A scanning electron micrograph of half of the star, rotated to match the representation in cortex in plate (c) below. The dark ring in the middle is the nostril. Dorsal (appendage 1) is to the left. c, A section of the flattened somatosensory cortex processed for the metabolic enzyme cytochrome oxidase to show the 11 modules where information from each of the 11 nasal appendages projects in primary somatosensory cortex (S1). Note the greatly overrepresented (enlarged) representation of the 11th appendage. The 11th appendage is the somatosensory fovea of the star (see text). Scale bars: b, 1 mm; c, 500 mm. b and c, Reproduced from Catania, K. C. 2001. Early development of a somatosensory fovea: A head start in the cortical space race? Nat. Neurosci. 4, 353-354, with permission.

role in guiding the formation of topographic maps in the CNS, and demonstrating the generality of this instructive relationship beyond the whisker-barrel system of rodents. It also shows that these variations are occurring in wild populations of mammals upon which natural selection is currently acting to shape the sensory periphery, and therefore the brains, of natural populations. Finally, the relatively frequent occurrence of these abnormalities is interesting. We have found as much as 5% of the population may have an abnormal number of appendages. This can be contrasted with the much lower rate of abnormalities for other appendages (Castilla et al., 1996; Zguricus et al., 1998). Darwin (1859) suggested an explanation for this kind of observation in On the Origin of Species, stating that ''in those cases in which the modification has been comparatively recent and extraordinarily great ... we ought to find the generative variability still present to a high degree.'' The argument is that selection has had less time to fix characteristics of recently evolved complex structures which are the product of selection for variations. This is exactly what we find in wild populations of star-nosed moles and this is not surprising given that the star, and its modular reflection in cortex, are ''comparatively recent and extraordinarily great'' modifications of the mole's snout.

The conclusion that can be drawn from the observations in laboratory rodents and star-nosed moles is that the sensory periphery and corresponding neocor-tical areas are developmentally linked in such a manner that variations in the periphery, which may be the result of small, local changes in the expression patterns of morphogenetic genes, are communicated to the brain through inductive cascades. As a consequence minor (and perhaps major) alterations to receptor arrays result in functional representations in the CNS upon which natural selection can act to modify sensory systems efficiently. For instance, it is hard to examine variations of the nose and cortex in star-nosed moles (Figure 4) without imagining ancestral stars with fewer and perhaps shorter appendages similarly reflected in the somatosensory cortex, or even a potential future mole with 24 or more appendages ringing the snout.

So far I have emphasized evidence that sudden changes to discrete structures in the sensory periphery can be communicated to the CNS during development to produce matching cortical representations. However, we have also found intriguing evidence that the sizes of cortical sensory representations may be influenced by differential timing of development in the sensory periphery. This may be a convenient mechanism by which behaviorally important sensory surfaces capture the most cortical territory.

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