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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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A star pattern visible in PrV.A. Half of the star rotated 90 degrees counterclockwise showing the 11 rays that ring the nostril. The relatively small 11th ray acts as the tactile fovea. B. When the brainstem is properly oriented (see materials and methods) sections reveal 11 distinct modules in PrV.
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pone-0022406-g003: A star pattern visible in PrV.A. Half of the star rotated 90 degrees counterclockwise showing the 11 rays that ring the nostril. The relatively small 11th ray acts as the tactile fovea. B. When the brainstem is properly oriented (see materials and methods) sections reveal 11 distinct modules in PrV.

Mentions: A favorable cutting angle (see materials and methods) revealed the entire set of 11 PrV modules in single sections of tissue. Figure 3 shows PrV and a rotated half of the star aligned to demonstrate how the PrV stripes correspond to the rays. This correspondence was determined by recording from PrV while stimulating the star with hand-held probes and calibrated von Frey hairs. Receptive fields were recorded and selected penetrations were marked with microlesions in 8 moles (see Figures 4 and 5 for two cases). The consistent finding was that ray number one was located rostro-medially in PrV (and at the deepest levels in the brainstem), followed by rays 2–8 (at shallower depths) as the electrode progressed laterally and caudally, and then rays 9–11 as the electrode was moved further caudally and back medially again. Details of this representation matched the topography of the star – for example rays 1 and 11 were aligned with one another on the star and in the brainstem representation (Figure 3). The differences in depth for the different ray representations corresponded to the angled orientation of the entire PrV nucleus in the brainstem. During the recordings, there was an obvious difference in the character of the responses from nasal rays, between penetrations in the trigeminal nerve and Sp5O, compared to PrV. The latter responded with greater magnitude and crisp, distinct single units compared to the former.


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

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

A star pattern visible in PrV.A. Half of the star rotated 90 degrees counterclockwise showing the 11 rays that ring the nostril. The relatively small 11th ray acts as the tactile fovea. B. When the brainstem is properly oriented (see materials and methods) sections reveal 11 distinct modules in PrV.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3139641&req=5

pone-0022406-g003: A star pattern visible in PrV.A. Half of the star rotated 90 degrees counterclockwise showing the 11 rays that ring the nostril. The relatively small 11th ray acts as the tactile fovea. B. When the brainstem is properly oriented (see materials and methods) sections reveal 11 distinct modules in PrV.
Mentions: A favorable cutting angle (see materials and methods) revealed the entire set of 11 PrV modules in single sections of tissue. Figure 3 shows PrV and a rotated half of the star aligned to demonstrate how the PrV stripes correspond to the rays. This correspondence was determined by recording from PrV while stimulating the star with hand-held probes and calibrated von Frey hairs. Receptive fields were recorded and selected penetrations were marked with microlesions in 8 moles (see Figures 4 and 5 for two cases). The consistent finding was that ray number one was located rostro-medially in PrV (and at the deepest levels in the brainstem), followed by rays 2–8 (at shallower depths) as the electrode progressed laterally and caudally, and then rays 9–11 as the electrode was moved further caudally and back medially again. Details of this representation matched the topography of the star – for example rays 1 and 11 were aligned with one another on the star and in the brainstem representation (Figure 3). The differences in depth for the different ray representations corresponded to the angled orientation of the entire PrV nucleus in the brainstem. During the recordings, there was an obvious difference in the character of the responses from nasal rays, between penetrations in the trigeminal nerve and Sp5O, compared to PrV. The latter responded with greater magnitude and crisp, distinct single units compared to the former.

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