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Corticofugal projection patterns of whisker sensorimotor cortex to the sensory trigeminal nuclei.

Smith JB, Watson GD, Alloway KD, Schwarz C, Chakrabarti S - Front Neural Circuits (2015)

Bottom Line: We confirmed our anterograde tracing results by injecting retrograde tracers at various rostro-caudal levels within the trigeminal sensory nuclei to determine the position of retrogradely labeled cortical cells with respect to S1 barrel cortex.Our results demonstrate that S1 and S2 projections terminate in largely overlapping regions but show some significant differences.Contrary to the view that sensory gating could be mediated by differential activation of inhibitory interconnections between the spinal trigeminal subnuclei, we observed that projections from S1 and S2 are largely overlapping in these subnuclei despite the differences noted earlier.

View Article: PubMed Central - PubMed

Affiliation: Department of Engineering Science and Mechanics, Pennsylvania State University University Park, PA, USA ; Center for Neural Engineering, Huck Institute of Life Sciences, Pennsylvania State University University Park, PA, USA.

ABSTRACT
The primary (S1) and secondary (S2) somatosensory cortices project to several trigeminal sensory nuclei. One putative function of these corticofugal projections is the gating of sensory transmission through the trigeminal principal nucleus (Pr5), and some have proposed that S1 and S2 project differentially to the spinal trigeminal subnuclei, which have inhibitory circuits that could inhibit or disinhibit the output projections of Pr5. Very little, however, is known about the origin of sensorimotor corticofugal projections and their patterns of termination in the various trigeminal nuclei. We addressed this issue by injecting anterograde tracers in S1, S2 and primary motor (M1) cortices, and quantitatively characterizing the distribution of labeled terminals within the entire rostro-caudal chain of trigeminal sub-nuclei. We confirmed our anterograde tracing results by injecting retrograde tracers at various rostro-caudal levels within the trigeminal sensory nuclei to determine the position of retrogradely labeled cortical cells with respect to S1 barrel cortex. Our results demonstrate that S1 and S2 projections terminate in largely overlapping regions but show some significant differences. Whereas S1 projection terminals tend to cluster within the principal trigeminal (Pr5), caudal spinal trigeminal interpolaris (Sp5ic), and the dorsal spinal trigeminal caudalis (Sp5c), S2 projection terminals are distributed in a continuum across all trigeminal nuclei. Contrary to the view that sensory gating could be mediated by differential activation of inhibitory interconnections between the spinal trigeminal subnuclei, we observed that projections from S1 and S2 are largely overlapping in these subnuclei despite the differences noted earlier.

No MeSH data available.


Related in: MedlinePlus

A representative example of a case receiving dual anterograde tracer deposits into the M1 and S1 cortices. (A) Nissl stained coronal section through the cortex showing the track of the pipette used to inject FR into M1. (B) Injection site of FR into vibrissal representation of the M1 cortex. (C) Coronal section through S1 barrel cortex processed for CO labeling. (D) Adjacent section, processed for visualization of BDA showing injection site in S1 and associated anterograde labeling. Anterograde labeling can be seen in ventral posterior medial nucleus (VPM). (E) Coronal section through the brainstem at the level of Pr5 stained for CO for better visualization of nuclear boundaries and neural tracts. (F) Adjacent section processed for visualization of FR terminals showing lack of any labeled terminals. (G) Adjacent section processed for visualization of BDA labeled terminals showing the presence of labeled varicosities in Pr5. (G′) Inset from (G) shown at greater magnification. (H–J′) Identical photomicrographs from the brainstem at the rostrocaudal level of Sp5o. (K–M′) Sections from the level of Sp5ic. (N–P′) Sections from the level of Sp5c.
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Figure 9: A representative example of a case receiving dual anterograde tracer deposits into the M1 and S1 cortices. (A) Nissl stained coronal section through the cortex showing the track of the pipette used to inject FR into M1. (B) Injection site of FR into vibrissal representation of the M1 cortex. (C) Coronal section through S1 barrel cortex processed for CO labeling. (D) Adjacent section, processed for visualization of BDA showing injection site in S1 and associated anterograde labeling. Anterograde labeling can be seen in ventral posterior medial nucleus (VPM). (E) Coronal section through the brainstem at the level of Pr5 stained for CO for better visualization of nuclear boundaries and neural tracts. (F) Adjacent section processed for visualization of FR terminals showing lack of any labeled terminals. (G) Adjacent section processed for visualization of BDA labeled terminals showing the presence of labeled varicosities in Pr5. (G′) Inset from (G) shown at greater magnification. (H–J′) Identical photomicrographs from the brainstem at the rostrocaudal level of Sp5o. (K–M′) Sections from the level of Sp5ic. (N–P′) Sections from the level of Sp5c.

Mentions: In the retrograde tracing experiments, irrespective of the rostro-caudal location of the tracer deposit in the brainstem, we did not see any labeled cells in M1 cortex. Although this has been mentioned in the literature before (Miyashita et al., 1994; Desbois et al., 1999; Urbain and Deschênes, 2007; Alloway et al., 2010), we sought to confirm this by analyzing data from three animals from an earlier study which had received anterograde tracer deposits in M1 and S1. Figure 9 illustrates corticofugal projections from M1 and S1 to the trigeminal sensory nuclei whisker representations. In this case, a FR tracer deposit was made in the M1 whisker representation (Figures 9A,B), and BDA was placed in S1 barrel cortex (Figures 9C,D). Labeling in the ventral posterior medial nucleus (VPM) and posteromedial nucleus (POm) in thalamus confirmed that the tracer had been deposited in the S1 barrel field (Figure 9D). S1 corticofugal projections, as shown before, targeted mainly Pr5, Sp5ic and dorsal Sp5c (Figures 9G,J,M,P) whereas M1 corticofugal projections could not be seen in any of the trigeminal nuclei (Figures 9F,I,L,O). M1 labeling was however observed in other mescencephalic and brainstem structures such as the superior colliculus, the periaqueductal gray, the basal pons, the deep mescencephalic nucleus, the interstitial nucleus of the medial longitudinal fasciculus and the gigantocellular, parvocellular and intermediate reticular nuclei, consistent with previous reports (Hattox et al., 2002; Takatoh et al., 2013; Sreenivasan et al., 2014). For a detailed analysis of M1 projections to brainstem readers are referred to a previous study (Alloway et al., 2010).


Corticofugal projection patterns of whisker sensorimotor cortex to the sensory trigeminal nuclei.

Smith JB, Watson GD, Alloway KD, Schwarz C, Chakrabarti S - Front Neural Circuits (2015)

A representative example of a case receiving dual anterograde tracer deposits into the M1 and S1 cortices. (A) Nissl stained coronal section through the cortex showing the track of the pipette used to inject FR into M1. (B) Injection site of FR into vibrissal representation of the M1 cortex. (C) Coronal section through S1 barrel cortex processed for CO labeling. (D) Adjacent section, processed for visualization of BDA showing injection site in S1 and associated anterograde labeling. Anterograde labeling can be seen in ventral posterior medial nucleus (VPM). (E) Coronal section through the brainstem at the level of Pr5 stained for CO for better visualization of nuclear boundaries and neural tracts. (F) Adjacent section processed for visualization of FR terminals showing lack of any labeled terminals. (G) Adjacent section processed for visualization of BDA labeled terminals showing the presence of labeled varicosities in Pr5. (G′) Inset from (G) shown at greater magnification. (H–J′) Identical photomicrographs from the brainstem at the rostrocaudal level of Sp5o. (K–M′) Sections from the level of Sp5ic. (N–P′) Sections from the level of Sp5c.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4588702&req=5

Figure 9: A representative example of a case receiving dual anterograde tracer deposits into the M1 and S1 cortices. (A) Nissl stained coronal section through the cortex showing the track of the pipette used to inject FR into M1. (B) Injection site of FR into vibrissal representation of the M1 cortex. (C) Coronal section through S1 barrel cortex processed for CO labeling. (D) Adjacent section, processed for visualization of BDA showing injection site in S1 and associated anterograde labeling. Anterograde labeling can be seen in ventral posterior medial nucleus (VPM). (E) Coronal section through the brainstem at the level of Pr5 stained for CO for better visualization of nuclear boundaries and neural tracts. (F) Adjacent section processed for visualization of FR terminals showing lack of any labeled terminals. (G) Adjacent section processed for visualization of BDA labeled terminals showing the presence of labeled varicosities in Pr5. (G′) Inset from (G) shown at greater magnification. (H–J′) Identical photomicrographs from the brainstem at the rostrocaudal level of Sp5o. (K–M′) Sections from the level of Sp5ic. (N–P′) Sections from the level of Sp5c.
Mentions: In the retrograde tracing experiments, irrespective of the rostro-caudal location of the tracer deposit in the brainstem, we did not see any labeled cells in M1 cortex. Although this has been mentioned in the literature before (Miyashita et al., 1994; Desbois et al., 1999; Urbain and Deschênes, 2007; Alloway et al., 2010), we sought to confirm this by analyzing data from three animals from an earlier study which had received anterograde tracer deposits in M1 and S1. Figure 9 illustrates corticofugal projections from M1 and S1 to the trigeminal sensory nuclei whisker representations. In this case, a FR tracer deposit was made in the M1 whisker representation (Figures 9A,B), and BDA was placed in S1 barrel cortex (Figures 9C,D). Labeling in the ventral posterior medial nucleus (VPM) and posteromedial nucleus (POm) in thalamus confirmed that the tracer had been deposited in the S1 barrel field (Figure 9D). S1 corticofugal projections, as shown before, targeted mainly Pr5, Sp5ic and dorsal Sp5c (Figures 9G,J,M,P) whereas M1 corticofugal projections could not be seen in any of the trigeminal nuclei (Figures 9F,I,L,O). M1 labeling was however observed in other mescencephalic and brainstem structures such as the superior colliculus, the periaqueductal gray, the basal pons, the deep mescencephalic nucleus, the interstitial nucleus of the medial longitudinal fasciculus and the gigantocellular, parvocellular and intermediate reticular nuclei, consistent with previous reports (Hattox et al., 2002; Takatoh et al., 2013; Sreenivasan et al., 2014). For a detailed analysis of M1 projections to brainstem readers are referred to a previous study (Alloway et al., 2010).

Bottom Line: We confirmed our anterograde tracing results by injecting retrograde tracers at various rostro-caudal levels within the trigeminal sensory nuclei to determine the position of retrogradely labeled cortical cells with respect to S1 barrel cortex.Our results demonstrate that S1 and S2 projections terminate in largely overlapping regions but show some significant differences.Contrary to the view that sensory gating could be mediated by differential activation of inhibitory interconnections between the spinal trigeminal subnuclei, we observed that projections from S1 and S2 are largely overlapping in these subnuclei despite the differences noted earlier.

View Article: PubMed Central - PubMed

Affiliation: Department of Engineering Science and Mechanics, Pennsylvania State University University Park, PA, USA ; Center for Neural Engineering, Huck Institute of Life Sciences, Pennsylvania State University University Park, PA, USA.

ABSTRACT
The primary (S1) and secondary (S2) somatosensory cortices project to several trigeminal sensory nuclei. One putative function of these corticofugal projections is the gating of sensory transmission through the trigeminal principal nucleus (Pr5), and some have proposed that S1 and S2 project differentially to the spinal trigeminal subnuclei, which have inhibitory circuits that could inhibit or disinhibit the output projections of Pr5. Very little, however, is known about the origin of sensorimotor corticofugal projections and their patterns of termination in the various trigeminal nuclei. We addressed this issue by injecting anterograde tracers in S1, S2 and primary motor (M1) cortices, and quantitatively characterizing the distribution of labeled terminals within the entire rostro-caudal chain of trigeminal sub-nuclei. We confirmed our anterograde tracing results by injecting retrograde tracers at various rostro-caudal levels within the trigeminal sensory nuclei to determine the position of retrogradely labeled cortical cells with respect to S1 barrel cortex. Our results demonstrate that S1 and S2 projections terminate in largely overlapping regions but show some significant differences. Whereas S1 projection terminals tend to cluster within the principal trigeminal (Pr5), caudal spinal trigeminal interpolaris (Sp5ic), and the dorsal spinal trigeminal caudalis (Sp5c), S2 projection terminals are distributed in a continuum across all trigeminal nuclei. Contrary to the view that sensory gating could be mediated by differential activation of inhibitory interconnections between the spinal trigeminal subnuclei, we observed that projections from S1 and S2 are largely overlapping in these subnuclei despite the differences noted earlier.

No MeSH data available.


Related in: MedlinePlus