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Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species.

Elston GN, Benavides-Piccione R, Elston A, Manger PR, Defelipe J - Front Neuroanat (2011)

Bottom Line: Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates.We found marked heterogeneity in pyramidal cell structure within and between these regions.Moreover, trends for gradients in neuronal complexity varied among species.

View Article: PubMed Central - PubMed

Affiliation: Centre for Cognitive Neuroscience Sunshine Coast, QLD, Australia.

ABSTRACT
The most ubiquitous neuron in the cerebral cortex, the pyramidal cell, is characterized by markedly different dendritic structure among different cortical areas. The complex pyramidal cell phenotype in granular prefrontal cortex (gPFC) of higher primates endows specific biophysical properties and patterns of connectivity, which differ from those in other cortical regions. However, within the gPFC, data have been sampled from only a select few cortical areas. The gPFC of species such as human and macaque monkey includes more than 10 cortical areas. It remains unknown as to what degree pyramidal cell structure may vary among these cortical areas. Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates. We found marked heterogeneity in pyramidal cell structure within and between these regions. Moreover, trends for gradients in neuronal complexity varied among species. As the structure of neurons determines their computational abilities, memory storage capacity and connectivity, we propose that these specializations in the pyramidal cell phenotype are an important determinant of species-specific executive cortical functions in primates.

No MeSH data available.


Schematic illustrating how the study of pyramidal cell morphology in the transverse plane may bias for uniformity in structure. Illustrated are two cells sampled from the primary visual area (V1) and granular prefrontal cortex (gPFC) of the macaque monkey. At left are the basal dendritic trees of the two cells as seen in the tangential plane. In black is the part of the dendritic tree that would be seen in a 50-μm transverse section (of the type used in many Golgi studies). The portion of the dendrites extending beyond the section is illustrated in gray. Note the relative similarity in structure of the part of the dendritic tree revealed in the 50-μm transverse sections. At right are illustrated the dendrograms of each of the two cells, which resulted from reconstruction of the complete basal dendritic tree as seen in the tangential plane. Based on our observations, transverse sections would have to be of the order of 1 mm thick to include all dendrites (e.g., human temporal lobe; Elston et al., 2001).
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Figure 3: Schematic illustrating how the study of pyramidal cell morphology in the transverse plane may bias for uniformity in structure. Illustrated are two cells sampled from the primary visual area (V1) and granular prefrontal cortex (gPFC) of the macaque monkey. At left are the basal dendritic trees of the two cells as seen in the tangential plane. In black is the part of the dendritic tree that would be seen in a 50-μm transverse section (of the type used in many Golgi studies). The portion of the dendrites extending beyond the section is illustrated in gray. Note the relative similarity in structure of the part of the dendritic tree revealed in the 50-μm transverse sections. At right are illustrated the dendrograms of each of the two cells, which resulted from reconstruction of the complete basal dendritic tree as seen in the tangential plane. Based on our observations, transverse sections would have to be of the order of 1 mm thick to include all dendrites (e.g., human temporal lobe; Elston et al., 2001).

Mentions: In the present study we focused on cells at the base of layer III, enabling comparison with data obtained at the base of layer III in visual, somatosensory, motor, and cingulate cortex of these an other species. Layer III was easily identified in the DAPI-labeled sections immediately above the neuron-dense granular layer. Even in tangential sections it is easy to distinguish the transition from layer III to layer IV due to the change in density and size of somata (see Figure 3 of Elston and Rosa, 1997). Neurons were injected in tangential sections so as to be able to reconstruct the entire basal dendritic tree. Such an approach has been central to the demonstration of regional and species specializations in pyramidal cell dendritic structure as the entire tangential extent of the basal dendritic tree is revealed, unlike in most previous studies in transverse sections in which many of the basal dendrites are truncated thus selecting for uniformity (Figure 3). In addition, by injecting neurons in the tangential plane aspects of their structure can be related directly with features reported elsewhere such as intrinsic axon patches and receptive fields (Levitt et al., 1993; Kritzer and Goldman-Rakic, 1995; Pucak et al., 1996; Melchitzky et al., 1998, 2001; González-Burgos et al., 2000). However, unfortunately, it is difficult to inject large numbers of cells under visual control in sections thick enough to contain the entire dendritic arborization (both apical and basal). Thus, we have focused on one dendritic “compartment” of a select group of pyramidal cells (those in layer III). It remains to be determined to what extent regional and species variation in the basal dendritic trees reflects any potential variation in their apical dendrites, and how this may differ from patterns of connectivity in other cortical areas/species (Binzegger et al., 2004).


Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species.

Elston GN, Benavides-Piccione R, Elston A, Manger PR, Defelipe J - Front Neuroanat (2011)

Schematic illustrating how the study of pyramidal cell morphology in the transverse plane may bias for uniformity in structure. Illustrated are two cells sampled from the primary visual area (V1) and granular prefrontal cortex (gPFC) of the macaque monkey. At left are the basal dendritic trees of the two cells as seen in the tangential plane. In black is the part of the dendritic tree that would be seen in a 50-μm transverse section (of the type used in many Golgi studies). The portion of the dendrites extending beyond the section is illustrated in gray. Note the relative similarity in structure of the part of the dendritic tree revealed in the 50-μm transverse sections. At right are illustrated the dendrograms of each of the two cells, which resulted from reconstruction of the complete basal dendritic tree as seen in the tangential plane. Based on our observations, transverse sections would have to be of the order of 1 mm thick to include all dendrites (e.g., human temporal lobe; Elston et al., 2001).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 3: Schematic illustrating how the study of pyramidal cell morphology in the transverse plane may bias for uniformity in structure. Illustrated are two cells sampled from the primary visual area (V1) and granular prefrontal cortex (gPFC) of the macaque monkey. At left are the basal dendritic trees of the two cells as seen in the tangential plane. In black is the part of the dendritic tree that would be seen in a 50-μm transverse section (of the type used in many Golgi studies). The portion of the dendrites extending beyond the section is illustrated in gray. Note the relative similarity in structure of the part of the dendritic tree revealed in the 50-μm transverse sections. At right are illustrated the dendrograms of each of the two cells, which resulted from reconstruction of the complete basal dendritic tree as seen in the tangential plane. Based on our observations, transverse sections would have to be of the order of 1 mm thick to include all dendrites (e.g., human temporal lobe; Elston et al., 2001).
Mentions: In the present study we focused on cells at the base of layer III, enabling comparison with data obtained at the base of layer III in visual, somatosensory, motor, and cingulate cortex of these an other species. Layer III was easily identified in the DAPI-labeled sections immediately above the neuron-dense granular layer. Even in tangential sections it is easy to distinguish the transition from layer III to layer IV due to the change in density and size of somata (see Figure 3 of Elston and Rosa, 1997). Neurons were injected in tangential sections so as to be able to reconstruct the entire basal dendritic tree. Such an approach has been central to the demonstration of regional and species specializations in pyramidal cell dendritic structure as the entire tangential extent of the basal dendritic tree is revealed, unlike in most previous studies in transverse sections in which many of the basal dendrites are truncated thus selecting for uniformity (Figure 3). In addition, by injecting neurons in the tangential plane aspects of their structure can be related directly with features reported elsewhere such as intrinsic axon patches and receptive fields (Levitt et al., 1993; Kritzer and Goldman-Rakic, 1995; Pucak et al., 1996; Melchitzky et al., 1998, 2001; González-Burgos et al., 2000). However, unfortunately, it is difficult to inject large numbers of cells under visual control in sections thick enough to contain the entire dendritic arborization (both apical and basal). Thus, we have focused on one dendritic “compartment” of a select group of pyramidal cells (those in layer III). It remains to be determined to what extent regional and species variation in the basal dendritic trees reflects any potential variation in their apical dendrites, and how this may differ from patterns of connectivity in other cortical areas/species (Binzegger et al., 2004).

Bottom Line: Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates.We found marked heterogeneity in pyramidal cell structure within and between these regions.Moreover, trends for gradients in neuronal complexity varied among species.

View Article: PubMed Central - PubMed

Affiliation: Centre for Cognitive Neuroscience Sunshine Coast, QLD, Australia.

ABSTRACT
The most ubiquitous neuron in the cerebral cortex, the pyramidal cell, is characterized by markedly different dendritic structure among different cortical areas. The complex pyramidal cell phenotype in granular prefrontal cortex (gPFC) of higher primates endows specific biophysical properties and patterns of connectivity, which differ from those in other cortical regions. However, within the gPFC, data have been sampled from only a select few cortical areas. The gPFC of species such as human and macaque monkey includes more than 10 cortical areas. It remains unknown as to what degree pyramidal cell structure may vary among these cortical areas. Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates. We found marked heterogeneity in pyramidal cell structure within and between these regions. Moreover, trends for gradients in neuronal complexity varied among species. As the structure of neurons determines their computational abilities, memory storage capacity and connectivity, we propose that these specializations in the pyramidal cell phenotype are an important determinant of species-specific executive cortical functions in primates.

No MeSH data available.