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Evolution of mammalian sensorimotor cortex: thalamic projections to parietal cortical areas in Monodelphis domestica.

Dooley JC, Franca JG, Seelke AM, Cooke DF, Krubitzer LA - Front Neuroanat (2015)

Bottom Line: Our results provide further evidence to support the hypothesized basic mammalian plan of thalamic projections to S1, with the lateral and medial ventral posterior thalamic nuclei (VPl and VPm) projecting to S1 body and S1 face, respectively.Notably, MM is distinguished from SC by relatively dense projections from the dorsal division of the lateral geniculate nucleus and pulvinar.Further we provide additional support for a primitive posterior parietal cortex which receives input from multiple modalities.

View Article: PubMed Central - PubMed

Affiliation: Center for Neuroscience, University of California, Davis Davis, CA, USA.

ABSTRACT
The current experiments build upon previous studies designed to reveal the network of parietal cortical areas present in the common mammalian ancestor. Understanding this ancestral network is essential for highlighting the basic somatosensory circuitry present in all mammals, and how this basic plan was modified to generate species specific behaviors. Our animal model, the short-tailed opossum (Monodelphis domestica), is a South American marsupial that has been proposed to have a similar ecological niche and morphology to the earliest common mammalian ancestor. In this investigation, we injected retrograde neuroanatomical tracers into the face and body representations of primary somatosensory cortex (S1), the rostral and caudal somatosensory fields (SR and SC), as well as a multimodal region (MM). Projections from different architectonically defined thalamic nuclei were then quantified. Our results provide further evidence to support the hypothesized basic mammalian plan of thalamic projections to S1, with the lateral and medial ventral posterior thalamic nuclei (VPl and VPm) projecting to S1 body and S1 face, respectively. Additional strong projections are from the medial division of posterior nucleus (Pom). SR receives projections from several midline nuclei, including the medial dorsal, ventral medial nucleus, and Pom. SC and MM show similar patterns of connectivity, with projections from the ventral anterior and ventral lateral nuclei, VPm and VPl, and the entire posterior nucleus (medial and lateral). Notably, MM is distinguished from SC by relatively dense projections from the dorsal division of the lateral geniculate nucleus and pulvinar. We discuss the finding that S1 of the short-tailed opossum has a similar pattern of projections as other marsupials and mammals, but also some distinct projections not present in other mammals. Further we provide additional support for a primitive posterior parietal cortex which receives input from multiple modalities.

No MeSH data available.


Related in: MedlinePlus

Boundaries of nuclei in the dorsal thalamus at the level of the ventral posterior nucleus in the short-tailed opossum. As in the previous figure, three different stains were used to delineate boundaries; CO (A), Nissl (B), and vGluT2 (C), with reconstructions derived from these stains illustrated in (D). The ventral posterior complex, including VPm and VPl can be seen as a darkly staining region in CO (A) and vGluT2 (C) stained tissue, with VPm staining more darkly. VMb can be seen medial to VP as a lightly stained line of tissue between two darkly stained sections. Lateral to VP, eml stains lightly in all three series. At this level of the thalamus, Pol is intermingled with eml. As in Figure 3, LGNd and LGNv are lateral to the ventral posterior complex, and are most apparent in CO (A) and vGluT2 (C) stained tissue. Near the midline, PF can be seen in CO (A) and vGluT2 (C) stained tissue, being slightly darker than the surrounding nuclei. Finally, dorsal to VMb and medial to VP, the caudal extent of VM could be identified as a lightly stained nuclei in all three series. Conventions as in Figure 3.
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Figure 4: Boundaries of nuclei in the dorsal thalamus at the level of the ventral posterior nucleus in the short-tailed opossum. As in the previous figure, three different stains were used to delineate boundaries; CO (A), Nissl (B), and vGluT2 (C), with reconstructions derived from these stains illustrated in (D). The ventral posterior complex, including VPm and VPl can be seen as a darkly staining region in CO (A) and vGluT2 (C) stained tissue, with VPm staining more darkly. VMb can be seen medial to VP as a lightly stained line of tissue between two darkly stained sections. Lateral to VP, eml stains lightly in all three series. At this level of the thalamus, Pol is intermingled with eml. As in Figure 3, LGNd and LGNv are lateral to the ventral posterior complex, and are most apparent in CO (A) and vGluT2 (C) stained tissue. Near the midline, PF can be seen in CO (A) and vGluT2 (C) stained tissue, being slightly darker than the surrounding nuclei. Finally, dorsal to VMb and medial to VP, the caudal extent of VM could be identified as a lightly stained nuclei in all three series. Conventions as in Figure 3.

Mentions: Lateral to these midline nuclei in more rostral portions of the thalamus we observed labeled neurons in the ventral anterior and the ventrolateral nuclei (VA and VL, respectively). The boundaries between these two nuclei were not always distinct in CO and Nissl-stained tissue, and so throughout the quantitative analysis performed in these studies they were combined into a single category (“VL/VA”). Both of these nuclei stained moderately for CO and showed a medium neuronal packing density in Nissl stains (Figures 3A,B). When tissue was stained for vGluT2, VA stained more darkly than VL and was located medial and ventral to VL (Figure 3C, boundary denoted by the dotted line in Figure 3D). Just medial to VA was VM, a densely packed nucleus that stained darker than the surrounding nuclei in Nissl-stained sections (Figure 3B). However, VM stained moderately for CO and lightly for vGluT2 (Figures 3A,C). VM extended further caudal than VL and VA (Figures 4A–D).


Evolution of mammalian sensorimotor cortex: thalamic projections to parietal cortical areas in Monodelphis domestica.

Dooley JC, Franca JG, Seelke AM, Cooke DF, Krubitzer LA - Front Neuroanat (2015)

Boundaries of nuclei in the dorsal thalamus at the level of the ventral posterior nucleus in the short-tailed opossum. As in the previous figure, three different stains were used to delineate boundaries; CO (A), Nissl (B), and vGluT2 (C), with reconstructions derived from these stains illustrated in (D). The ventral posterior complex, including VPm and VPl can be seen as a darkly staining region in CO (A) and vGluT2 (C) stained tissue, with VPm staining more darkly. VMb can be seen medial to VP as a lightly stained line of tissue between two darkly stained sections. Lateral to VP, eml stains lightly in all three series. At this level of the thalamus, Pol is intermingled with eml. As in Figure 3, LGNd and LGNv are lateral to the ventral posterior complex, and are most apparent in CO (A) and vGluT2 (C) stained tissue. Near the midline, PF can be seen in CO (A) and vGluT2 (C) stained tissue, being slightly darker than the surrounding nuclei. Finally, dorsal to VMb and medial to VP, the caudal extent of VM could be identified as a lightly stained nuclei in all three series. Conventions as in Figure 3.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4286717&req=5

Figure 4: Boundaries of nuclei in the dorsal thalamus at the level of the ventral posterior nucleus in the short-tailed opossum. As in the previous figure, three different stains were used to delineate boundaries; CO (A), Nissl (B), and vGluT2 (C), with reconstructions derived from these stains illustrated in (D). The ventral posterior complex, including VPm and VPl can be seen as a darkly staining region in CO (A) and vGluT2 (C) stained tissue, with VPm staining more darkly. VMb can be seen medial to VP as a lightly stained line of tissue between two darkly stained sections. Lateral to VP, eml stains lightly in all three series. At this level of the thalamus, Pol is intermingled with eml. As in Figure 3, LGNd and LGNv are lateral to the ventral posterior complex, and are most apparent in CO (A) and vGluT2 (C) stained tissue. Near the midline, PF can be seen in CO (A) and vGluT2 (C) stained tissue, being slightly darker than the surrounding nuclei. Finally, dorsal to VMb and medial to VP, the caudal extent of VM could be identified as a lightly stained nuclei in all three series. Conventions as in Figure 3.
Mentions: Lateral to these midline nuclei in more rostral portions of the thalamus we observed labeled neurons in the ventral anterior and the ventrolateral nuclei (VA and VL, respectively). The boundaries between these two nuclei were not always distinct in CO and Nissl-stained tissue, and so throughout the quantitative analysis performed in these studies they were combined into a single category (“VL/VA”). Both of these nuclei stained moderately for CO and showed a medium neuronal packing density in Nissl stains (Figures 3A,B). When tissue was stained for vGluT2, VA stained more darkly than VL and was located medial and ventral to VL (Figure 3C, boundary denoted by the dotted line in Figure 3D). Just medial to VA was VM, a densely packed nucleus that stained darker than the surrounding nuclei in Nissl-stained sections (Figure 3B). However, VM stained moderately for CO and lightly for vGluT2 (Figures 3A,C). VM extended further caudal than VL and VA (Figures 4A–D).

Bottom Line: Our results provide further evidence to support the hypothesized basic mammalian plan of thalamic projections to S1, with the lateral and medial ventral posterior thalamic nuclei (VPl and VPm) projecting to S1 body and S1 face, respectively.Notably, MM is distinguished from SC by relatively dense projections from the dorsal division of the lateral geniculate nucleus and pulvinar.Further we provide additional support for a primitive posterior parietal cortex which receives input from multiple modalities.

View Article: PubMed Central - PubMed

Affiliation: Center for Neuroscience, University of California, Davis Davis, CA, USA.

ABSTRACT
The current experiments build upon previous studies designed to reveal the network of parietal cortical areas present in the common mammalian ancestor. Understanding this ancestral network is essential for highlighting the basic somatosensory circuitry present in all mammals, and how this basic plan was modified to generate species specific behaviors. Our animal model, the short-tailed opossum (Monodelphis domestica), is a South American marsupial that has been proposed to have a similar ecological niche and morphology to the earliest common mammalian ancestor. In this investigation, we injected retrograde neuroanatomical tracers into the face and body representations of primary somatosensory cortex (S1), the rostral and caudal somatosensory fields (SR and SC), as well as a multimodal region (MM). Projections from different architectonically defined thalamic nuclei were then quantified. Our results provide further evidence to support the hypothesized basic mammalian plan of thalamic projections to S1, with the lateral and medial ventral posterior thalamic nuclei (VPl and VPm) projecting to S1 body and S1 face, respectively. Additional strong projections are from the medial division of posterior nucleus (Pom). SR receives projections from several midline nuclei, including the medial dorsal, ventral medial nucleus, and Pom. SC and MM show similar patterns of connectivity, with projections from the ventral anterior and ventral lateral nuclei, VPm and VPl, and the entire posterior nucleus (medial and lateral). Notably, MM is distinguished from SC by relatively dense projections from the dorsal division of the lateral geniculate nucleus and pulvinar. We discuss the finding that S1 of the short-tailed opossum has a similar pattern of projections as other marsupials and mammals, but also some distinct projections not present in other mammals. Further we provide additional support for a primitive posterior parietal cortex which receives input from multiple modalities.

No MeSH data available.


Related in: MedlinePlus