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"Subpial Fan Cell" - A Class of Calretinin Neuron in Layer 1 of Adult Monkey Prefrontal Cortex.

Gabbott PL - Front Neuroanat (2016)

Bottom Line: SPF-SPF cell innervation was not observed.The distribution and connectivity of SPF cells suggest they act as integrative hubs in upper layer 1 during postnatal maturation.The main synaptic output of SPF cells likely provides a transminicolumnar excitatory influence across swathes of apical dendritic tufts - thus affecting information processing in discrete patches of layer 1 in adult monkey PFC.

View Article: PubMed Central - PubMed

Affiliation: Neural Architectonics CentreOxford, UK; Department of Life, Health, and Chemical Sciences, The Open UniversityMilton Keynes, UK; University Department of Pharmacology, University of OxfordOxford, UK.

ABSTRACT
Layer 1 of the cortex contains populations of neurochemically distinct neurons and afferent fibers which markedly affect neural activity in the apical dendritic tufts of pyramidal cells. Understanding the causal mechanisms requires knowledge of the cellular architecture and synaptic organization of layer 1. This study has identified eight morphological classes of calretinin immunopositive (CRet+) neurons (including Cajal-Retzius cells) in layer 1 of the prefrontal cortex (PFC) in adult monkey (Macaca fasicularis), with a distinct class - termed "subpial fan (SPF) cell" - described in detail. SPF cells were rare horizontal unipolar CRet+ cells located directly beneath the pia with a single thick primary dendrite that branched into a characteristic fan-like dendritic tree tangential to the pial surface. Dendrites had spines, filamentous processes and thorny branchlets. SPF cells lay millimeters apart with intralaminar axons that ramified widely in upper layer 1. Such cells were GABA immunonegative (-) and occurred in areas beyond PFC. Interspersed amidst SPF cells displaying normal structural integrity were degenerating CRet+ neurons (including SPF cells) and clumps of lipofuscin-rich cellular debris. The number of degenerating SPF cells increased during adulthood. Ultrastructural analyses indicated SPF cell somata received asymmetric (A - presumed excitatory) and symmetric (S - presumed inhibitory) synaptic contacts. Proximal dendritic shafts received mainly S-type and distal shafts mostly A-type input. All dendritic thorns and most dendritic spines received both synapse types. The tangential areal density of SPF cell axonal varicosities varied radially from parent somata - with dense clusters in more distal zones. All boutons formed A-type contacts with CRet- structures. The main post-synaptic targets were dendritic shafts (67%; mostly spine-bearing) and dendritic spines (24%). SPF-SPF cell innervation was not observed. Morphometry of SPF cells indicated a unique class of CRet+/GABA- neuron in adult monkey PFC - possibly a subtype of persisting Cajal-Retzius cell. The distribution and connectivity of SPF cells suggest they act as integrative hubs in upper layer 1 during postnatal maturation. The main synaptic output of SPF cells likely provides a transminicolumnar excitatory influence across swathes of apical dendritic tufts - thus affecting information processing in discrete patches of layer 1 in adult monkey PFC.

No MeSH data available.


Related in: MedlinePlus

(A) Area 24b. Somatic profile of an identified CRet+ SPF cell (N) in layer 1. Lipofuscin granules and vacuoles in the cytoplasm are indicated (black arrows). Nucleus, n. Large vacuole (v). Fine filamentous astroglial processes in layer 1 (f). Dense membranous inclusions in a dendrite are visible (asterisk). Scale bar: 5 μm. (B) Yellow/brown profile of lipofuscin-rich cellular debris (arrow). Note the gray (SG) soma of a CRet+ neuron (N) beneath focal plane. Scale bar: 10 μm. (C) Ultrastructural profile of electron-dense cellular profile with a highly condensed pyknotic nucleus (n). Note vacuolated appearance. Large lysosome (asterisk). Scale bar: 5 μm. (D) Microglial cell (m — with dark clumped inclusions) associated with lipofuscin-rich cellular debris (arrow). Scale bar: 10 μm. (E) Pyknotic neuronal profile (n) with dark cytoplasm (d) that extends into cellular processes (white arrow). Note also normal ultrastructure of asymmetric synaptic junctions in the neuropil (dark arrows). Scale bar: 2 μm. (F) Perpendicular reconstruction of a SPF cell (n) in area 24b (perpendicular view). Primary dendritic branch point is indicated (double headed arrow). (Axon, ax). Scale bar: 20 μm. Inset shows SPF cell and a neighboring capillary (c). (G) Untreated semithin resin section (2 μm thick) through the somata of the SPF cell in (F) (arrow). Positions of fiducial capillary (c) and an unlabeled cellular profile (asterisk) are indicated. The nucleus (n) contains weak immunolabeling. Bifurcation of the primary dendrite is indicated (double headed arrow). Axon, ax. Scale bar: 10 μm. (H) Semithin section in (G) reacted using post-embedding GABA immunocytochemistry (CRet & GABA). GABA+ cells (white asterisk) have intensely immunoreactive nuclei. Especially note GABA+ fusiform cell beneath pial surface (encircled). Boxed region identifies the CRet+ SPF cell seen in G to be GABA- (i.e., lack of intense GABA nuclear immunolabeling). Axon, ax. (Fiducial markers with (F,G): capillary, c; unlabeled cellular profile, black asterisk). Scale bar: 50 μm. (I) Profile of a GABA- pyramidal cell (P) devoid of cytoplasmic and nuclear (n) immunolabeling. Nucleolus (arrow). Scale bar: 10 μm. (J). Drawings by Gustaf Retzius (1893: Plates I and II) showing Golgi-impregnated cells in developing layer 1 of the human neocortex. Retzius illustrates several unipolar cells (e.g., 1, 2, 4, and 5). The somata of cells 2, 4, 5, and 6 are drawn with numerous small ovoid pale regions in the cytoplasm/nucleus (?) — shown enlarged with high contrast in the boxed region (right). These features are similar to degenerating CRet+ cell bodies (see Figures 13E and especially F/F′). Cell 7 is similar to the class 1 cell in Figures 2A–F (this study). Cell 8 resembles the class 4 cell shown in Figure 2O. Scale bar = 100 μm. (The original drawings by Retzius have been altered to display only cells of interest).
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Figure 14: (A) Area 24b. Somatic profile of an identified CRet+ SPF cell (N) in layer 1. Lipofuscin granules and vacuoles in the cytoplasm are indicated (black arrows). Nucleus, n. Large vacuole (v). Fine filamentous astroglial processes in layer 1 (f). Dense membranous inclusions in a dendrite are visible (asterisk). Scale bar: 5 μm. (B) Yellow/brown profile of lipofuscin-rich cellular debris (arrow). Note the gray (SG) soma of a CRet+ neuron (N) beneath focal plane. Scale bar: 10 μm. (C) Ultrastructural profile of electron-dense cellular profile with a highly condensed pyknotic nucleus (n). Note vacuolated appearance. Large lysosome (asterisk). Scale bar: 5 μm. (D) Microglial cell (m — with dark clumped inclusions) associated with lipofuscin-rich cellular debris (arrow). Scale bar: 10 μm. (E) Pyknotic neuronal profile (n) with dark cytoplasm (d) that extends into cellular processes (white arrow). Note also normal ultrastructure of asymmetric synaptic junctions in the neuropil (dark arrows). Scale bar: 2 μm. (F) Perpendicular reconstruction of a SPF cell (n) in area 24b (perpendicular view). Primary dendritic branch point is indicated (double headed arrow). (Axon, ax). Scale bar: 20 μm. Inset shows SPF cell and a neighboring capillary (c). (G) Untreated semithin resin section (2 μm thick) through the somata of the SPF cell in (F) (arrow). Positions of fiducial capillary (c) and an unlabeled cellular profile (asterisk) are indicated. The nucleus (n) contains weak immunolabeling. Bifurcation of the primary dendrite is indicated (double headed arrow). Axon, ax. Scale bar: 10 μm. (H) Semithin section in (G) reacted using post-embedding GABA immunocytochemistry (CRet & GABA). GABA+ cells (white asterisk) have intensely immunoreactive nuclei. Especially note GABA+ fusiform cell beneath pial surface (encircled). Boxed region identifies the CRet+ SPF cell seen in G to be GABA- (i.e., lack of intense GABA nuclear immunolabeling). Axon, ax. (Fiducial markers with (F,G): capillary, c; unlabeled cellular profile, black asterisk). Scale bar: 50 μm. (I) Profile of a GABA- pyramidal cell (P) devoid of cytoplasmic and nuclear (n) immunolabeling. Nucleolus (arrow). Scale bar: 10 μm. (J). Drawings by Gustaf Retzius (1893: Plates I and II) showing Golgi-impregnated cells in developing layer 1 of the human neocortex. Retzius illustrates several unipolar cells (e.g., 1, 2, 4, and 5). The somata of cells 2, 4, 5, and 6 are drawn with numerous small ovoid pale regions in the cytoplasm/nucleus (?) — shown enlarged with high contrast in the boxed region (right). These features are similar to degenerating CRet+ cell bodies (see Figures 13E and especially F/F′). Cell 7 is similar to the class 1 cell in Figures 2A–F (this study). Cell 8 resembles the class 4 cell shown in Figure 2O. Scale bar = 100 μm. (The original drawings by Retzius have been altered to display only cells of interest).

Mentions: In the light microscope, irregular profiles (d.circ. c.5–17 μm) with a dark yellow/orange color (indicative of lipofuscin) were frequently found in the upper tier of layer 1, particularly beneath the pia (Figures 2–8, 13). Such profiles were present in all PFC areas studied and occurred, either singly or in clusters, with a linear density of 1–6 per mm length of pia (Figures 4A,B,D,J,K). They were commonly associated with the processes and somata of SPF cells — as well class 1/2 neurons (Figures 2A,C,C′, 2H–J, 4A,B,I–K, 6A–F, 7, 8B, 13A,C,E, especially G,I,J″). Some of the profiles were clearly vacuolated with closely apposed microglial cells (Figures 5E′, 14D). The coloration of these lipofuscin-rich profiles darkened following treatment with osmium tetroxide. Figures 13G,I, 14B show the distinction between gray immunolabeling for CRet alone (using Vector SG kit) and the lipofuscin containing profiles. Accordingly, it was possible to identify a large number of CRet+ SG labeled cellular profiles in upper layer 1 with lipofuscin in their cytoplasmata (Figure 4I).


"Subpial Fan Cell" - A Class of Calretinin Neuron in Layer 1 of Adult Monkey Prefrontal Cortex.

Gabbott PL - Front Neuroanat (2016)

(A) Area 24b. Somatic profile of an identified CRet+ SPF cell (N) in layer 1. Lipofuscin granules and vacuoles in the cytoplasm are indicated (black arrows). Nucleus, n. Large vacuole (v). Fine filamentous astroglial processes in layer 1 (f). Dense membranous inclusions in a dendrite are visible (asterisk). Scale bar: 5 μm. (B) Yellow/brown profile of lipofuscin-rich cellular debris (arrow). Note the gray (SG) soma of a CRet+ neuron (N) beneath focal plane. Scale bar: 10 μm. (C) Ultrastructural profile of electron-dense cellular profile with a highly condensed pyknotic nucleus (n). Note vacuolated appearance. Large lysosome (asterisk). Scale bar: 5 μm. (D) Microglial cell (m — with dark clumped inclusions) associated with lipofuscin-rich cellular debris (arrow). Scale bar: 10 μm. (E) Pyknotic neuronal profile (n) with dark cytoplasm (d) that extends into cellular processes (white arrow). Note also normal ultrastructure of asymmetric synaptic junctions in the neuropil (dark arrows). Scale bar: 2 μm. (F) Perpendicular reconstruction of a SPF cell (n) in area 24b (perpendicular view). Primary dendritic branch point is indicated (double headed arrow). (Axon, ax). Scale bar: 20 μm. Inset shows SPF cell and a neighboring capillary (c). (G) Untreated semithin resin section (2 μm thick) through the somata of the SPF cell in (F) (arrow). Positions of fiducial capillary (c) and an unlabeled cellular profile (asterisk) are indicated. The nucleus (n) contains weak immunolabeling. Bifurcation of the primary dendrite is indicated (double headed arrow). Axon, ax. Scale bar: 10 μm. (H) Semithin section in (G) reacted using post-embedding GABA immunocytochemistry (CRet & GABA). GABA+ cells (white asterisk) have intensely immunoreactive nuclei. Especially note GABA+ fusiform cell beneath pial surface (encircled). Boxed region identifies the CRet+ SPF cell seen in G to be GABA- (i.e., lack of intense GABA nuclear immunolabeling). Axon, ax. (Fiducial markers with (F,G): capillary, c; unlabeled cellular profile, black asterisk). Scale bar: 50 μm. (I) Profile of a GABA- pyramidal cell (P) devoid of cytoplasmic and nuclear (n) immunolabeling. Nucleolus (arrow). Scale bar: 10 μm. (J). Drawings by Gustaf Retzius (1893: Plates I and II) showing Golgi-impregnated cells in developing layer 1 of the human neocortex. Retzius illustrates several unipolar cells (e.g., 1, 2, 4, and 5). The somata of cells 2, 4, 5, and 6 are drawn with numerous small ovoid pale regions in the cytoplasm/nucleus (?) — shown enlarged with high contrast in the boxed region (right). These features are similar to degenerating CRet+ cell bodies (see Figures 13E and especially F/F′). Cell 7 is similar to the class 1 cell in Figures 2A–F (this study). Cell 8 resembles the class 4 cell shown in Figure 2O. Scale bar = 100 μm. (The original drawings by Retzius have been altered to display only cells of interest).
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Figure 14: (A) Area 24b. Somatic profile of an identified CRet+ SPF cell (N) in layer 1. Lipofuscin granules and vacuoles in the cytoplasm are indicated (black arrows). Nucleus, n. Large vacuole (v). Fine filamentous astroglial processes in layer 1 (f). Dense membranous inclusions in a dendrite are visible (asterisk). Scale bar: 5 μm. (B) Yellow/brown profile of lipofuscin-rich cellular debris (arrow). Note the gray (SG) soma of a CRet+ neuron (N) beneath focal plane. Scale bar: 10 μm. (C) Ultrastructural profile of electron-dense cellular profile with a highly condensed pyknotic nucleus (n). Note vacuolated appearance. Large lysosome (asterisk). Scale bar: 5 μm. (D) Microglial cell (m — with dark clumped inclusions) associated with lipofuscin-rich cellular debris (arrow). Scale bar: 10 μm. (E) Pyknotic neuronal profile (n) with dark cytoplasm (d) that extends into cellular processes (white arrow). Note also normal ultrastructure of asymmetric synaptic junctions in the neuropil (dark arrows). Scale bar: 2 μm. (F) Perpendicular reconstruction of a SPF cell (n) in area 24b (perpendicular view). Primary dendritic branch point is indicated (double headed arrow). (Axon, ax). Scale bar: 20 μm. Inset shows SPF cell and a neighboring capillary (c). (G) Untreated semithin resin section (2 μm thick) through the somata of the SPF cell in (F) (arrow). Positions of fiducial capillary (c) and an unlabeled cellular profile (asterisk) are indicated. The nucleus (n) contains weak immunolabeling. Bifurcation of the primary dendrite is indicated (double headed arrow). Axon, ax. Scale bar: 10 μm. (H) Semithin section in (G) reacted using post-embedding GABA immunocytochemistry (CRet & GABA). GABA+ cells (white asterisk) have intensely immunoreactive nuclei. Especially note GABA+ fusiform cell beneath pial surface (encircled). Boxed region identifies the CRet+ SPF cell seen in G to be GABA- (i.e., lack of intense GABA nuclear immunolabeling). Axon, ax. (Fiducial markers with (F,G): capillary, c; unlabeled cellular profile, black asterisk). Scale bar: 50 μm. (I) Profile of a GABA- pyramidal cell (P) devoid of cytoplasmic and nuclear (n) immunolabeling. Nucleolus (arrow). Scale bar: 10 μm. (J). Drawings by Gustaf Retzius (1893: Plates I and II) showing Golgi-impregnated cells in developing layer 1 of the human neocortex. Retzius illustrates several unipolar cells (e.g., 1, 2, 4, and 5). The somata of cells 2, 4, 5, and 6 are drawn with numerous small ovoid pale regions in the cytoplasm/nucleus (?) — shown enlarged with high contrast in the boxed region (right). These features are similar to degenerating CRet+ cell bodies (see Figures 13E and especially F/F′). Cell 7 is similar to the class 1 cell in Figures 2A–F (this study). Cell 8 resembles the class 4 cell shown in Figure 2O. Scale bar = 100 μm. (The original drawings by Retzius have been altered to display only cells of interest).
Mentions: In the light microscope, irregular profiles (d.circ. c.5–17 μm) with a dark yellow/orange color (indicative of lipofuscin) were frequently found in the upper tier of layer 1, particularly beneath the pia (Figures 2–8, 13). Such profiles were present in all PFC areas studied and occurred, either singly or in clusters, with a linear density of 1–6 per mm length of pia (Figures 4A,B,D,J,K). They were commonly associated with the processes and somata of SPF cells — as well class 1/2 neurons (Figures 2A,C,C′, 2H–J, 4A,B,I–K, 6A–F, 7, 8B, 13A,C,E, especially G,I,J″). Some of the profiles were clearly vacuolated with closely apposed microglial cells (Figures 5E′, 14D). The coloration of these lipofuscin-rich profiles darkened following treatment with osmium tetroxide. Figures 13G,I, 14B show the distinction between gray immunolabeling for CRet alone (using Vector SG kit) and the lipofuscin containing profiles. Accordingly, it was possible to identify a large number of CRet+ SG labeled cellular profiles in upper layer 1 with lipofuscin in their cytoplasmata (Figure 4I).

Bottom Line: SPF-SPF cell innervation was not observed.The distribution and connectivity of SPF cells suggest they act as integrative hubs in upper layer 1 during postnatal maturation.The main synaptic output of SPF cells likely provides a transminicolumnar excitatory influence across swathes of apical dendritic tufts - thus affecting information processing in discrete patches of layer 1 in adult monkey PFC.

View Article: PubMed Central - PubMed

Affiliation: Neural Architectonics CentreOxford, UK; Department of Life, Health, and Chemical Sciences, The Open UniversityMilton Keynes, UK; University Department of Pharmacology, University of OxfordOxford, UK.

ABSTRACT
Layer 1 of the cortex contains populations of neurochemically distinct neurons and afferent fibers which markedly affect neural activity in the apical dendritic tufts of pyramidal cells. Understanding the causal mechanisms requires knowledge of the cellular architecture and synaptic organization of layer 1. This study has identified eight morphological classes of calretinin immunopositive (CRet+) neurons (including Cajal-Retzius cells) in layer 1 of the prefrontal cortex (PFC) in adult monkey (Macaca fasicularis), with a distinct class - termed "subpial fan (SPF) cell" - described in detail. SPF cells were rare horizontal unipolar CRet+ cells located directly beneath the pia with a single thick primary dendrite that branched into a characteristic fan-like dendritic tree tangential to the pial surface. Dendrites had spines, filamentous processes and thorny branchlets. SPF cells lay millimeters apart with intralaminar axons that ramified widely in upper layer 1. Such cells were GABA immunonegative (-) and occurred in areas beyond PFC. Interspersed amidst SPF cells displaying normal structural integrity were degenerating CRet+ neurons (including SPF cells) and clumps of lipofuscin-rich cellular debris. The number of degenerating SPF cells increased during adulthood. Ultrastructural analyses indicated SPF cell somata received asymmetric (A - presumed excitatory) and symmetric (S - presumed inhibitory) synaptic contacts. Proximal dendritic shafts received mainly S-type and distal shafts mostly A-type input. All dendritic thorns and most dendritic spines received both synapse types. The tangential areal density of SPF cell axonal varicosities varied radially from parent somata - with dense clusters in more distal zones. All boutons formed A-type contacts with CRet- structures. The main post-synaptic targets were dendritic shafts (67%; mostly spine-bearing) and dendritic spines (24%). SPF-SPF cell innervation was not observed. Morphometry of SPF cells indicated a unique class of CRet+/GABA- neuron in adult monkey PFC - possibly a subtype of persisting Cajal-Retzius cell. The distribution and connectivity of SPF cells suggest they act as integrative hubs in upper layer 1 during postnatal maturation. The main synaptic output of SPF cells likely provides a transminicolumnar excitatory influence across swathes of apical dendritic tufts - thus affecting information processing in discrete patches of layer 1 in adult monkey PFC.

No MeSH data available.


Related in: MedlinePlus