Figure 4 The nasal appendages and cortical representations of the half-nose for two abnormal star-nosed moles. a, Scanning electron micrograph of 12 appendages of an abnormal star. b, Section of flattened cortex processed for cytochrome oxidase to reveal the corresponding 12 modules in the primary somatosensory area. c, Scanning electron micrograph of 10 appendages of an abnormal star. d, Section of flattened cortex processed for cytochrome oxidase to reveal the corresponding 10 modules in the primary somatosensory area.
central tactile fovea (the 11th appendage) used for detailed exploration of objects of interest, whereas the larger peripheral appendages (1 through 10) are used to scan for potentially interesting objects or food items (Catania and Kaas, 1997b). This functional division is apparent in star-nosed mole behavior, which includes frequent saccadic movements of the star that bring the high-resolution tactile fovea into contact with objects of interest. In addition, the preferential use of the fovea is reflected in the organization of somatosensory cortex (Figure 3). The 11th foveal appendage is greatly over-represented, occupying approximately 25% of the star representation in primary somatosensory cortex (S1). The enlargement of the 11th appendage is not simply a reflection of a higher innervation density (Catania and Kaas, 1997b), as suggested by previous investigations in rodents (Welker and Van der Loos, 1986), but rather is an overrepresentation of the primary afferent input - much like the retinal fovea is overrepresented in cortex relative to the number of ganglion cells concentrated in the fovea (Perry and Cowey, 1985; Silveira et al., 1989; Azzopardi and Cowey, 1993; Quevedo et al., 1996).
An obvious question is how afferents capture more than their share of somatosensory cortex relative to behaviorally less important inputs. The observation that star-nosed moles preferentially use the 11th appendage for tactile investigations, coupled with previous studies that indicate cortical representational areas may expand as a result of preferential stimulation and use (Recanzone et al., 1992a, 1992b; Xerri et al., 1999), suggest that behavior patterns may play an important role in establishing this relationship. However, our developmental studies suggest an alternative and perhaps surprising explanation for how the periphery may drive the expansion of the fovea representation in cortex.
In the course of investigating how the appendages of the star develop (Catania et al., 1999) an unusual discrepancy in the relative sizes of embryonic and adult appendages on the star was noticed. In contrast to the small size of the 11th appendage in adult star-nosed moles, this appendage was comparatively large in embryos (Figure 5). In fact, the relative sizes of the star appendages in embryos reflect the relative sizes of the cortical representations seen later in adults (Figure 6a). Over the course of subsequent development, the proportion of the star taken up by the fovea gradually changes until, in adults, the 11th appendage takes up only a small fraction of the star (and contains only a relatively small proportion of the mechanosensory Eimer's organs), and thus the adult star proportions no longer reflect the magnification factors seen in cortex.
Figure 5 Embryonic star-nosed mole compared to an adult, showing the relatively large 11th appendage early in development. a, An embryonic mole showing the developing nasal appendages numbered 1-11. In early embryos the 11th appendage of the nose (the tactile fovea) is the largest and has the greatest innervated surface area. Inset shows a front view of the ventral star from the same specimen to illustrate the large 11th appendage. b, An adult star-nosed mole emerges from its tunnel. In adults the 11th appendage takes up only a relatively small proportion (7%) of the star, despite its important role as the tactile fovea. c, Scanning confocal microscopy of Dil-labeled fibers innervating the developing star. The 11th appendage (boxed area) takes up the largest area of the star and has the largest innervated surface area. The more lateral appendages have only begun to form at this stage. Scale bars: a and c, 500 mm; b, 1 mm. 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.
A more detailed examination of the developing appendages, associated sensory organs, and their innervation suggests the explanation for the changing relative proportions of the different appendages during development - the 11th, foveal appendage leads the development of the star. It is not only large earliest, but also has the largest innervated surface area in embryos and develops mature nerve terminals and associated sensory organs first in newborn moles (Catania, 2001). Finally, these patterns of development, with the 11th appendage in the lead, are reflected in the cortex by the early emergence of a cytochrome oxidase-rich zone representing the 11th appendage (Catania, 2001).
This developmental sequence provides the fovea with a strong basis for competitive advantages during development and suggests that foveal afferents may outcompete their neighbors in an activity-dependent race for cortical territory. The mechanism for this outcome is suggested by previous investigations in the visual and somatosensory systems. For example, when activity from one eye is reduced by suturing the lid shut during critical periods, ocular dominance columns devoted to the open eye develop expanded representations at the expense of the closed eye (Hubel et al., 1977). Activity-dependent expansions have also been documented for the barrel system in rodents (Schlaggar et al., 1993).
The suggestion is that the skin surface can provide not only instructions to the cortex regarding the arrangement and number of sensory surfaces but also information about the optimal size for these representations in later adults. Presumably the larger area for foveal representation allows for more efficient and perhaps faster sensory processing for these important inputs. The developmental sequence observed for the star suggests that evolutionary processes can change the size of representations in the brain by selectively altering the relative timing of developmental events in the periphery. It is significant in this regard that the fovea leads development in the primate retina (Rapaport and Stone, 1984) and is also overrepresented in cortex relative to the peripheral part of the retina.
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