Supernumerary Whiskers Revisited

Van der Loos and Dorfl (1978) published a short paper posing the provocative question: does the skin tell the somatosensory cortex how to construct a map of the sensory periphery? The focus of their investigation was the relationship between the whisker pattern on the face of mice and the visible, isomorphic reflection of this pattern in the primary somatosensory face region by a series of cortical barrels (Figure 1). The authors suggested three alternative possibilities for how this relationship becomes established: (1) the brain imposes a map on the periphery, (2) the periphery imposes its spatial organization on the brain, and (3) brain maps and the periphery develop independently.

Their paper revolved around the observation that some of the mice in their colonies were born with extra whiskers, and in these cases there were invariably corresponding extra barrels in the cortical representation in the correct spatial location. The central question was how the cortex became matched to the altered sensory periphery (Figure 2). The possibility that the brain imposes a pattern on the periphery was ruled out on the basis of clear developmental evidence showing that the sensory periphery develops well before the map in the somatosensory cortex and thus the sensory representation does not have an opportunity to direct the development of whiskers (for review, see Killackey et al., 1995). At the same time, the peripheral-to-central developmental sequence provides at least the opportunity for the sensory periphery to guide the formation of somatosensory cortex

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.

through cascades of inductive events that are communicated from the skin, to the brainstem nuclei, to the thalamus, and finally to the developing neocortex.

The last possibility, that the brain and periphery make their debut independently, was considered unlikely. Van der Loos and Dorfl (1978) argued that it would be an extraordinary task for the genome to code for these changes independently, and concluded that the answer to the question in their title was yes - the skin tells the somatosensory cortex how to construct a map of the periphery.

Yet despite the well-reasoned argument from supernumerary barrels, it was not possible to rule out completely a genetic code for their representation in the brain. A recent investigation by Ohsaki et al. (2002) provides new evidence for the role of the skin surface in guiding the developing barrel cortex by selectively altering early gene expression specifically at the whiskerpad to induce the development of extra whiskers. By transfecting the follicular skin surface of early mouse embryos (E9.5-E11.5) with an adenovirus containing the Sonic hedgehog gene from chicken, various configurations of supernumerary whiskers were induced. The supernumerary whiskers were represented in the contralateral somatosensory cortex by extra barrels in the correct topographic position. This elegant separation of gene expression in the skin surface and CNS seems to provide conclusive support for the extrinsic nature of the signal to cortex for producing an extra barrel, as originally suggested by Van der Loos and Dorfl (1978).

The whisker-barrel system in rodents has thus been a critical model system for investigating the instructive relationship between the sensory periphery and the brain. This was possible because of the clear reflection of peripheral receptor topography in the architectural organization of rodent somatosen-sory cortex (Woolsey and Van der Loos, 1970). But how general is this kind of relationship between sensory organs and modules in the brain, and what kinds of variations of receptors arrays are found outside laboratory rodents?

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