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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

Labeling patterns in the trigeminal sensory nuclei following dual anterograde tracer deposits in the whisker representations of primary (S1) and secondary somatosensory (S2) cortices. (A) Photomicrograph of tangential cortical section processed for Biotinylated Dextran Amine (BDA) (B). Locations of the tracer deposits in the (C,D) rows of S1 (BDA) and (B–D) rows of S2 (FR) shown on a tangential section of the cortex through layer IV, processed for cytochrome oxidase (CO). (C) Adjacent section processed for the fluorescent tracer Fluoro Ruby (FR), which was injected at two locations in the S2 whisker representation corresponding to the inset in (B). (D) Horizontal section through the contralateral trigeminal sensory nuclei processed for BDA shows different nuclei and anatomical landmarks (dotted lines), identified from an adjoining CO section. (E) The same section viewed using a TRITC filter for FR visualization showing labeled terminals across trigeminal sensory nuclei. (F,H,J) Photomicrographs of the areas in the insets of 1D show the morphology of BDA-labeled terminals in Pr5, Sp5ic and Sp5c, respectively. (G,I,K) The areas under the same insets (E) but viewed using a TRITC filter to show the morphology of FR labeled terminals. The BDA reaction product can be seen on the same photomicrographs. Abbreviations: M1, primary motor cortex; PPC/PM, posterior parietal cortex/posterio-medial cortex; Pr5, principal trigeminal nucleus; Sp5o, spinal trigeminal nucleus pars oralis; Sp5ir, spinal trigeminal nucleus pars interpolaris rostral; Sp5ic, spinal trigeminal nucleus pars interpolaris caudal; Sp5c, spinal trigeminal nucleus pars caudalis; Sp5t, spinal trigeminal tract; 7n, nucleus of the 7th cranial nerve; VCN, ventral cochlear nucleus.
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Figure 1: Labeling patterns in the trigeminal sensory nuclei following dual anterograde tracer deposits in the whisker representations of primary (S1) and secondary somatosensory (S2) cortices. (A) Photomicrograph of tangential cortical section processed for Biotinylated Dextran Amine (BDA) (B). Locations of the tracer deposits in the (C,D) rows of S1 (BDA) and (B–D) rows of S2 (FR) shown on a tangential section of the cortex through layer IV, processed for cytochrome oxidase (CO). (C) Adjacent section processed for the fluorescent tracer Fluoro Ruby (FR), which was injected at two locations in the S2 whisker representation corresponding to the inset in (B). (D) Horizontal section through the contralateral trigeminal sensory nuclei processed for BDA shows different nuclei and anatomical landmarks (dotted lines), identified from an adjoining CO section. (E) The same section viewed using a TRITC filter for FR visualization showing labeled terminals across trigeminal sensory nuclei. (F,H,J) Photomicrographs of the areas in the insets of 1D show the morphology of BDA-labeled terminals in Pr5, Sp5ic and Sp5c, respectively. (G,I,K) The areas under the same insets (E) but viewed using a TRITC filter to show the morphology of FR labeled terminals. The BDA reaction product can be seen on the same photomicrographs. Abbreviations: M1, primary motor cortex; PPC/PM, posterior parietal cortex/posterio-medial cortex; Pr5, principal trigeminal nucleus; Sp5o, spinal trigeminal nucleus pars oralis; Sp5ir, spinal trigeminal nucleus pars interpolaris rostral; Sp5ic, spinal trigeminal nucleus pars interpolaris caudal; Sp5c, spinal trigeminal nucleus pars caudalis; Sp5t, spinal trigeminal tract; 7n, nucleus of the 7th cranial nerve; VCN, ventral cochlear nucleus.

Mentions: The boundaries of the various trigeminal sensory nuclei were defined in alternate sections processed for CO visualization. The Sp5ic-Sp5c boundary was observed in all sections as a clear transition between the densely stained Sp5i and the lightly stained Sp5c neuropil in the CO sections at the level of the obex at the location of the newly discovered pars muralis nucleus (Matthews et al., 2015). The Sp5ic-Sp5ir boundary was defined using a transition from uniform staining in Sp5ir to CO labeled patches observed in Sp5ic. This coincided in most cases with the lateral bulge observed in the spinal trigeminal tract which imparts the Sp5i nucleus its characteristic teardrop shape. The Sp5o-Sp5ir boundary was the most difficult to demarcate as there were no clear transitions in CO labeling. Therefore the caudal edge of the ventral cochlear nucleus (VCN) was defined as the caudal boundary of Sp5o in keeping with earlier conventions (Furuta et al., 2006). Finally, Pr5 was defined as extending from the rostral boundary of intense CO labeling to the caudal edge of the nucleus of the 7th cranial nerve (7n). Finally the boundaries were drawn by two independent observers and averages across the two determined as the true boundary. Examples of boundaries can be seen in Figure 1.


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)

Labeling patterns in the trigeminal sensory nuclei following dual anterograde tracer deposits in the whisker representations of primary (S1) and secondary somatosensory (S2) cortices. (A) Photomicrograph of tangential cortical section processed for Biotinylated Dextran Amine (BDA) (B). Locations of the tracer deposits in the (C,D) rows of S1 (BDA) and (B–D) rows of S2 (FR) shown on a tangential section of the cortex through layer IV, processed for cytochrome oxidase (CO). (C) Adjacent section processed for the fluorescent tracer Fluoro Ruby (FR), which was injected at two locations in the S2 whisker representation corresponding to the inset in (B). (D) Horizontal section through the contralateral trigeminal sensory nuclei processed for BDA shows different nuclei and anatomical landmarks (dotted lines), identified from an adjoining CO section. (E) The same section viewed using a TRITC filter for FR visualization showing labeled terminals across trigeminal sensory nuclei. (F,H,J) Photomicrographs of the areas in the insets of 1D show the morphology of BDA-labeled terminals in Pr5, Sp5ic and Sp5c, respectively. (G,I,K) The areas under the same insets (E) but viewed using a TRITC filter to show the morphology of FR labeled terminals. The BDA reaction product can be seen on the same photomicrographs. Abbreviations: M1, primary motor cortex; PPC/PM, posterior parietal cortex/posterio-medial cortex; Pr5, principal trigeminal nucleus; Sp5o, spinal trigeminal nucleus pars oralis; Sp5ir, spinal trigeminal nucleus pars interpolaris rostral; Sp5ic, spinal trigeminal nucleus pars interpolaris caudal; Sp5c, spinal trigeminal nucleus pars caudalis; Sp5t, spinal trigeminal tract; 7n, nucleus of the 7th cranial nerve; VCN, ventral cochlear nucleus.
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Related In: Results  -  Collection

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Figure 1: Labeling patterns in the trigeminal sensory nuclei following dual anterograde tracer deposits in the whisker representations of primary (S1) and secondary somatosensory (S2) cortices. (A) Photomicrograph of tangential cortical section processed for Biotinylated Dextran Amine (BDA) (B). Locations of the tracer deposits in the (C,D) rows of S1 (BDA) and (B–D) rows of S2 (FR) shown on a tangential section of the cortex through layer IV, processed for cytochrome oxidase (CO). (C) Adjacent section processed for the fluorescent tracer Fluoro Ruby (FR), which was injected at two locations in the S2 whisker representation corresponding to the inset in (B). (D) Horizontal section through the contralateral trigeminal sensory nuclei processed for BDA shows different nuclei and anatomical landmarks (dotted lines), identified from an adjoining CO section. (E) The same section viewed using a TRITC filter for FR visualization showing labeled terminals across trigeminal sensory nuclei. (F,H,J) Photomicrographs of the areas in the insets of 1D show the morphology of BDA-labeled terminals in Pr5, Sp5ic and Sp5c, respectively. (G,I,K) The areas under the same insets (E) but viewed using a TRITC filter to show the morphology of FR labeled terminals. The BDA reaction product can be seen on the same photomicrographs. Abbreviations: M1, primary motor cortex; PPC/PM, posterior parietal cortex/posterio-medial cortex; Pr5, principal trigeminal nucleus; Sp5o, spinal trigeminal nucleus pars oralis; Sp5ir, spinal trigeminal nucleus pars interpolaris rostral; Sp5ic, spinal trigeminal nucleus pars interpolaris caudal; Sp5c, spinal trigeminal nucleus pars caudalis; Sp5t, spinal trigeminal tract; 7n, nucleus of the 7th cranial nerve; VCN, ventral cochlear nucleus.
Mentions: The boundaries of the various trigeminal sensory nuclei were defined in alternate sections processed for CO visualization. The Sp5ic-Sp5c boundary was observed in all sections as a clear transition between the densely stained Sp5i and the lightly stained Sp5c neuropil in the CO sections at the level of the obex at the location of the newly discovered pars muralis nucleus (Matthews et al., 2015). The Sp5ic-Sp5ir boundary was defined using a transition from uniform staining in Sp5ir to CO labeled patches observed in Sp5ic. This coincided in most cases with the lateral bulge observed in the spinal trigeminal tract which imparts the Sp5i nucleus its characteristic teardrop shape. The Sp5o-Sp5ir boundary was the most difficult to demarcate as there were no clear transitions in CO labeling. Therefore the caudal edge of the ventral cochlear nucleus (VCN) was defined as the caudal boundary of Sp5o in keeping with earlier conventions (Furuta et al., 2006). Finally, Pr5 was defined as extending from the rostral boundary of intense CO labeling to the caudal edge of the nucleus of the 7th cranial nerve (7n). Finally the boundaries were drawn by two independent observers and averages across the two determined as the true boundary. Examples of boundaries can be seen in Figure 1.

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