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A star in the brainstem reveals the first step of cortical magnification.

Catania KC, Leitch DB, Gauthier D - PLoS ONE (2011)

Bottom Line: These measures were compared to fiber counts and primary cortical areas from a previous investigation.Our results indicate that PrV provides the first step in magnifying CNS representations of important afferents, but additional magnification occurs at higher levels.The early development of the 11(th), foveal appendage could provide a mechanism for the most important afferents to capture the most CNS space.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America. ken.catania@vanderbilt.edu

ABSTRACT
A fundamental question in the neurosciences is how central nervous system (CNS) space is allocated to different sensory inputs. Yet it is difficult to measure innervation density and corresponding representational areas in the CNS of most species. These measurements can be made in star-nosed moles (Condylura cristata) because the cortical representation of nasal rays is visible in flattened sections and afferents from each ray can be counted. Here we used electrophysiological recordings combined with sections of the brainstem to identify a large, visible star representation in the principal sensory nucleus (PrV). PrV was greatly expanded and bulged out of the brainstem rostrally to partially invade the trigeminal nerve. The star representation was a distinct PrV subnucleus containing 11 modules, each representing one of the nasal rays. The 11 PrV ray representations were reconstructed to obtain volumes and the largest module corresponded to ray 11, the mole's tactile fovea. These measures were compared to fiber counts and primary cortical areas from a previous investigation. PrV ray volumes were closely correlated with the number of afferents from each ray, but afferents from the behaviorally most important, 11(th) ray were preferentially over-represented. This over-representation at the brainstem level was much less than at the cortical level. Our results indicate that PrV provides the first step in magnifying CNS representations of important afferents, but additional magnification occurs at higher levels. The early development of the 11(th), foveal appendage could provide a mechanism for the most important afferents to capture the most CNS space.

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Comparison of myelinated fiber counts, PrV ray volumes, and cortical ray areas.A–B. A section of the principal nucleus (PrV) containing the star representation compared to a flattened section of cortex showing the primary somatosensory representation of the star (S1 Cortex), both processed for cytochrome oxidase. The areas of the ray representations in “A” are similar to the total PrV volumes of the ray representations from reconstructions of serial sections. Thus these images illustrate the general finding that ray 11, the tactile fovea, is more greatly over-represented at the level of the cortex (B) than in the brainstem (A). C. The mean PrV volumes for each ray representation (1–11) from the 4 reconstructed cases. D. Myelinated fiber counts for the 11 rays of 4 moles from a previous study [17]. E. Areas of cortex representing the rays of 4 moles from a previous study [17]. F. The mean volume of each ray representation in PrV per fiber (ratio of C to D). G. The mean S1 cortex per fiber for each ray representation (ratio of E to D). Note that D, E, and G (darker histograms) are from a previous investigation in 4 moles (adapted from[17]), whereas C and F are from the present study in 4 different moles. Bars in C–G are SEM.
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pone-0022406-g006: Comparison of myelinated fiber counts, PrV ray volumes, and cortical ray areas.A–B. A section of the principal nucleus (PrV) containing the star representation compared to a flattened section of cortex showing the primary somatosensory representation of the star (S1 Cortex), both processed for cytochrome oxidase. The areas of the ray representations in “A” are similar to the total PrV volumes of the ray representations from reconstructions of serial sections. Thus these images illustrate the general finding that ray 11, the tactile fovea, is more greatly over-represented at the level of the cortex (B) than in the brainstem (A). C. The mean PrV volumes for each ray representation (1–11) from the 4 reconstructed cases. D. Myelinated fiber counts for the 11 rays of 4 moles from a previous study [17]. E. Areas of cortex representing the rays of 4 moles from a previous study [17]. F. The mean volume of each ray representation in PrV per fiber (ratio of C to D). G. The mean S1 cortex per fiber for each ray representation (ratio of E to D). Note that D, E, and G (darker histograms) are from a previous investigation in 4 moles (adapted from[17]), whereas C and F are from the present study in 4 different moles. Bars in C–G are SEM.

Mentions: All serial sections of 4 different PrV star subnuclei were photographed, aligned, and reconstructed (see materials and methods) to obtain the volume of each ray representation. The mean total volume of the star subnucleus from the 4 cases was 7.1 mm3. The mean volume of each ray representation is shown in Figure 6C. Ray 11, the tactile fovea, had the largest representation in the star subnucleus. The other ray representations were variable in size, with rays 1–5 generally having larger representations than 6–10. The overall pattern for the mean volumes of each ray representation in PrV was similar to the pattern observed in the single section in Figure 6A. Comparison of this visible PrV pattern to the representation visible in S1 (Figure 6B) suggests ray 11 is much more greatly magnified in the neocortex than in the brainstem.


A star in the brainstem reveals the first step of cortical magnification.

Catania KC, Leitch DB, Gauthier D - PLoS ONE (2011)

Comparison of myelinated fiber counts, PrV ray volumes, and cortical ray areas.A–B. A section of the principal nucleus (PrV) containing the star representation compared to a flattened section of cortex showing the primary somatosensory representation of the star (S1 Cortex), both processed for cytochrome oxidase. The areas of the ray representations in “A” are similar to the total PrV volumes of the ray representations from reconstructions of serial sections. Thus these images illustrate the general finding that ray 11, the tactile fovea, is more greatly over-represented at the level of the cortex (B) than in the brainstem (A). C. The mean PrV volumes for each ray representation (1–11) from the 4 reconstructed cases. D. Myelinated fiber counts for the 11 rays of 4 moles from a previous study [17]. E. Areas of cortex representing the rays of 4 moles from a previous study [17]. F. The mean volume of each ray representation in PrV per fiber (ratio of C to D). G. The mean S1 cortex per fiber for each ray representation (ratio of E to D). Note that D, E, and G (darker histograms) are from a previous investigation in 4 moles (adapted from[17]), whereas C and F are from the present study in 4 different moles. Bars in C–G are SEM.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3139641&req=5

pone-0022406-g006: Comparison of myelinated fiber counts, PrV ray volumes, and cortical ray areas.A–B. A section of the principal nucleus (PrV) containing the star representation compared to a flattened section of cortex showing the primary somatosensory representation of the star (S1 Cortex), both processed for cytochrome oxidase. The areas of the ray representations in “A” are similar to the total PrV volumes of the ray representations from reconstructions of serial sections. Thus these images illustrate the general finding that ray 11, the tactile fovea, is more greatly over-represented at the level of the cortex (B) than in the brainstem (A). C. The mean PrV volumes for each ray representation (1–11) from the 4 reconstructed cases. D. Myelinated fiber counts for the 11 rays of 4 moles from a previous study [17]. E. Areas of cortex representing the rays of 4 moles from a previous study [17]. F. The mean volume of each ray representation in PrV per fiber (ratio of C to D). G. The mean S1 cortex per fiber for each ray representation (ratio of E to D). Note that D, E, and G (darker histograms) are from a previous investigation in 4 moles (adapted from[17]), whereas C and F are from the present study in 4 different moles. Bars in C–G are SEM.
Mentions: All serial sections of 4 different PrV star subnuclei were photographed, aligned, and reconstructed (see materials and methods) to obtain the volume of each ray representation. The mean total volume of the star subnucleus from the 4 cases was 7.1 mm3. The mean volume of each ray representation is shown in Figure 6C. Ray 11, the tactile fovea, had the largest representation in the star subnucleus. The other ray representations were variable in size, with rays 1–5 generally having larger representations than 6–10. The overall pattern for the mean volumes of each ray representation in PrV was similar to the pattern observed in the single section in Figure 6A. Comparison of this visible PrV pattern to the representation visible in S1 (Figure 6B) suggests ray 11 is much more greatly magnified in the neocortex than in the brainstem.

Bottom Line: These measures were compared to fiber counts and primary cortical areas from a previous investigation.Our results indicate that PrV provides the first step in magnifying CNS representations of important afferents, but additional magnification occurs at higher levels.The early development of the 11(th), foveal appendage could provide a mechanism for the most important afferents to capture the most CNS space.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America. ken.catania@vanderbilt.edu

ABSTRACT
A fundamental question in the neurosciences is how central nervous system (CNS) space is allocated to different sensory inputs. Yet it is difficult to measure innervation density and corresponding representational areas in the CNS of most species. These measurements can be made in star-nosed moles (Condylura cristata) because the cortical representation of nasal rays is visible in flattened sections and afferents from each ray can be counted. Here we used electrophysiological recordings combined with sections of the brainstem to identify a large, visible star representation in the principal sensory nucleus (PrV). PrV was greatly expanded and bulged out of the brainstem rostrally to partially invade the trigeminal nerve. The star representation was a distinct PrV subnucleus containing 11 modules, each representing one of the nasal rays. The 11 PrV ray representations were reconstructed to obtain volumes and the largest module corresponded to ray 11, the mole's tactile fovea. These measures were compared to fiber counts and primary cortical areas from a previous investigation. PrV ray volumes were closely correlated with the number of afferents from each ray, but afferents from the behaviorally most important, 11(th) ray were preferentially over-represented. This over-representation at the brainstem level was much less than at the cortical level. Our results indicate that PrV provides the first step in magnifying CNS representations of important afferents, but additional magnification occurs at higher levels. The early development of the 11(th), foveal appendage could provide a mechanism for the most important afferents to capture the most CNS space.

Show MeSH
Related in: MedlinePlus