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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

Degenerating class 8 — SPF cells. (A) Perpendicular view of a degenerating SPF cell in area 46v. (Reconstruction of cell in A′). Vacuoles in the main dendritic processes (lines). Note the dark profile (white arrow) abutting the soma (n). Scale bar: 25 μm. (B–D) Surface (tangential) views of three unipolar CRet+ SPF cells with vacuolated primary and secondary processes (arrows). Presumptive axon-like processes (ax) emerge from opposite poles of the labeled somata in (B,C). (B, area 9; C, area 25; D, area 24b). In (C), dark circular profiles are indicated (arrows): Scale bars: (B,C) 50 μm, (D) 25 μm. (E) Surface (tangential) views. Drawings of CRet+ unipolar thorn cells with vacuolated processes. Several vacuoles are indicated (lines). Note the vacuolated remnants of two regions (asterisks) of terminal processes in cell a (compare with cell n2 in Figure 6, cell g in Figure 7, and the cells in Figures 8A,C). Positions of dark lipofuscin profiles (thick arrows) indicated (thick arrows — see also photographic insert) Cell nuclei (n). (Areal locations of cells: a, area 32; b, area 24a; c, area 46d; d, area 9). Scale bars: 25 μm. (F,F′) Area 32. Degenerating CRet+ somata lying beneath the pia. Numerous discrete ovoid regions in the cytoplasm of both cells are devoid of immunoreactivity (thin white arrows). Capillary, c. Scale bar: 5 μm. (G) Yellow/brown lipofuscin-rich profile abutting the soma of a degenerating neuron (outlined). Note disruption of the SPF cell body. Dendrite, d; axon, ax. [CRet+ immunoreactivity visualized using gray (Vector SG) peroxidase substrate]. Scale bar: 20 μm. (H) Area 46d. Degenerating CRet+ SPF cell (arrow). Numerous CRet+ neurons are present in layer 2. Scale bar: 100 μm. (H′) Higher magnification image of the neuron indicated in (H). The primary dendrite courses toward the viewer and is obscured by the vacuolated secondary and higher order dendrites (lines). (I) Yellow/brown lipofuscin-rich profiles (white arrows) one of which is in close contact with a degenerating dendrite. (Vacuole, line). Scale bar: 5 μm. (J) Area 32. Photographic montage of a degenerating SPF cell body. Numerous vacuoles are present in the soma (white arrows) and in proximal portion of the main process (lines). Scale bar: 10 μm. (J′) Drawing of the neuron seen in (J). Fine perpendicularly disposed processes arising from the main vacuolated dendrite (arrows). (J″) Photomicrograph of the region boxed in (J′). A fine caliber process derived from the main dendrite (d) comes into close association with a dense cellular profile (arrow). Scale bar: 5 μm.
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Figure 13: Degenerating class 8 — SPF cells. (A) Perpendicular view of a degenerating SPF cell in area 46v. (Reconstruction of cell in A′). Vacuoles in the main dendritic processes (lines). Note the dark profile (white arrow) abutting the soma (n). Scale bar: 25 μm. (B–D) Surface (tangential) views of three unipolar CRet+ SPF cells with vacuolated primary and secondary processes (arrows). Presumptive axon-like processes (ax) emerge from opposite poles of the labeled somata in (B,C). (B, area 9; C, area 25; D, area 24b). In (C), dark circular profiles are indicated (arrows): Scale bars: (B,C) 50 μm, (D) 25 μm. (E) Surface (tangential) views. Drawings of CRet+ unipolar thorn cells with vacuolated processes. Several vacuoles are indicated (lines). Note the vacuolated remnants of two regions (asterisks) of terminal processes in cell a (compare with cell n2 in Figure 6, cell g in Figure 7, and the cells in Figures 8A,C). Positions of dark lipofuscin profiles (thick arrows) indicated (thick arrows — see also photographic insert) Cell nuclei (n). (Areal locations of cells: a, area 32; b, area 24a; c, area 46d; d, area 9). Scale bars: 25 μm. (F,F′) Area 32. Degenerating CRet+ somata lying beneath the pia. Numerous discrete ovoid regions in the cytoplasm of both cells are devoid of immunoreactivity (thin white arrows). Capillary, c. Scale bar: 5 μm. (G) Yellow/brown lipofuscin-rich profile abutting the soma of a degenerating neuron (outlined). Note disruption of the SPF cell body. Dendrite, d; axon, ax. [CRet+ immunoreactivity visualized using gray (Vector SG) peroxidase substrate]. Scale bar: 20 μm. (H) Area 46d. Degenerating CRet+ SPF cell (arrow). Numerous CRet+ neurons are present in layer 2. Scale bar: 100 μm. (H′) Higher magnification image of the neuron indicated in (H). The primary dendrite courses toward the viewer and is obscured by the vacuolated secondary and higher order dendrites (lines). (I) Yellow/brown lipofuscin-rich profiles (white arrows) one of which is in close contact with a degenerating dendrite. (Vacuole, line). Scale bar: 5 μm. (J) Area 32. Photographic montage of a degenerating SPF cell body. Numerous vacuoles are present in the soma (white arrows) and in proximal portion of the main process (lines). Scale bar: 10 μm. (J′) Drawing of the neuron seen in (J). Fine perpendicularly disposed processes arising from the main vacuolated dendrite (arrows). (J″) Photomicrograph of the region boxed in (J′). A fine caliber process derived from the main dendrite (d) comes into close association with a dense cellular profile (arrow). Scale bar: 5 μm.

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)

Degenerating class 8 — SPF cells. (A) Perpendicular view of a degenerating SPF cell in area 46v. (Reconstruction of cell in A′). Vacuoles in the main dendritic processes (lines). Note the dark profile (white arrow) abutting the soma (n). Scale bar: 25 μm. (B–D) Surface (tangential) views of three unipolar CRet+ SPF cells with vacuolated primary and secondary processes (arrows). Presumptive axon-like processes (ax) emerge from opposite poles of the labeled somata in (B,C). (B, area 9; C, area 25; D, area 24b). In (C), dark circular profiles are indicated (arrows): Scale bars: (B,C) 50 μm, (D) 25 μm. (E) Surface (tangential) views. Drawings of CRet+ unipolar thorn cells with vacuolated processes. Several vacuoles are indicated (lines). Note the vacuolated remnants of two regions (asterisks) of terminal processes in cell a (compare with cell n2 in Figure 6, cell g in Figure 7, and the cells in Figures 8A,C). Positions of dark lipofuscin profiles (thick arrows) indicated (thick arrows — see also photographic insert) Cell nuclei (n). (Areal locations of cells: a, area 32; b, area 24a; c, area 46d; d, area 9). Scale bars: 25 μm. (F,F′) Area 32. Degenerating CRet+ somata lying beneath the pia. Numerous discrete ovoid regions in the cytoplasm of both cells are devoid of immunoreactivity (thin white arrows). Capillary, c. Scale bar: 5 μm. (G) Yellow/brown lipofuscin-rich profile abutting the soma of a degenerating neuron (outlined). Note disruption of the SPF cell body. Dendrite, d; axon, ax. [CRet+ immunoreactivity visualized using gray (Vector SG) peroxidase substrate]. Scale bar: 20 μm. (H) Area 46d. Degenerating CRet+ SPF cell (arrow). Numerous CRet+ neurons are present in layer 2. Scale bar: 100 μm. (H′) Higher magnification image of the neuron indicated in (H). The primary dendrite courses toward the viewer and is obscured by the vacuolated secondary and higher order dendrites (lines). (I) Yellow/brown lipofuscin-rich profiles (white arrows) one of which is in close contact with a degenerating dendrite. (Vacuole, line). Scale bar: 5 μm. (J) Area 32. Photographic montage of a degenerating SPF cell body. Numerous vacuoles are present in the soma (white arrows) and in proximal portion of the main process (lines). Scale bar: 10 μm. (J′) Drawing of the neuron seen in (J). Fine perpendicularly disposed processes arising from the main vacuolated dendrite (arrows). (J″) Photomicrograph of the region boxed in (J′). A fine caliber process derived from the main dendrite (d) comes into close association with a dense cellular profile (arrow). Scale bar: 5 μm.
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Figure 13: Degenerating class 8 — SPF cells. (A) Perpendicular view of a degenerating SPF cell in area 46v. (Reconstruction of cell in A′). Vacuoles in the main dendritic processes (lines). Note the dark profile (white arrow) abutting the soma (n). Scale bar: 25 μm. (B–D) Surface (tangential) views of three unipolar CRet+ SPF cells with vacuolated primary and secondary processes (arrows). Presumptive axon-like processes (ax) emerge from opposite poles of the labeled somata in (B,C). (B, area 9; C, area 25; D, area 24b). In (C), dark circular profiles are indicated (arrows): Scale bars: (B,C) 50 μm, (D) 25 μm. (E) Surface (tangential) views. Drawings of CRet+ unipolar thorn cells with vacuolated processes. Several vacuoles are indicated (lines). Note the vacuolated remnants of two regions (asterisks) of terminal processes in cell a (compare with cell n2 in Figure 6, cell g in Figure 7, and the cells in Figures 8A,C). Positions of dark lipofuscin profiles (thick arrows) indicated (thick arrows — see also photographic insert) Cell nuclei (n). (Areal locations of cells: a, area 32; b, area 24a; c, area 46d; d, area 9). Scale bars: 25 μm. (F,F′) Area 32. Degenerating CRet+ somata lying beneath the pia. Numerous discrete ovoid regions in the cytoplasm of both cells are devoid of immunoreactivity (thin white arrows). Capillary, c. Scale bar: 5 μm. (G) Yellow/brown lipofuscin-rich profile abutting the soma of a degenerating neuron (outlined). Note disruption of the SPF cell body. Dendrite, d; axon, ax. [CRet+ immunoreactivity visualized using gray (Vector SG) peroxidase substrate]. Scale bar: 20 μm. (H) Area 46d. Degenerating CRet+ SPF cell (arrow). Numerous CRet+ neurons are present in layer 2. Scale bar: 100 μm. (H′) Higher magnification image of the neuron indicated in (H). The primary dendrite courses toward the viewer and is obscured by the vacuolated secondary and higher order dendrites (lines). (I) Yellow/brown lipofuscin-rich profiles (white arrows) one of which is in close contact with a degenerating dendrite. (Vacuole, line). Scale bar: 5 μm. (J) Area 32. Photographic montage of a degenerating SPF cell body. Numerous vacuoles are present in the soma (white arrows) and in proximal portion of the main process (lines). Scale bar: 10 μm. (J′) Drawing of the neuron seen in (J). Fine perpendicularly disposed processes arising from the main vacuolated dendrite (arrows). (J″) Photomicrograph of the region boxed in (J′). A fine caliber process derived from the main dendrite (d) comes into close association with a dense cellular profile (arrow). Scale bar: 5 μm.
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