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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) Class 8. Area 46d. Reconstruction of a CRet+ SPF cell. Note the radiate fan-like distribution of the dendritic processes. Numerous thorn-like protrusions emanate from the main processes. Swellings along the axonal process (ax) are indicated. Scale bar: 50 μm. Inset (A′): Enlarged image of the region in (A) illustrating several long, fine thorn-like protrusions arising from a thick secondary dendrite. (B) Photomicrographic montage of the dendritic arbor indicated by the polygonal region in (A). (C) 3D rotations showing the distribution of the cellular processes viewed in the plane perpendicular to the pial surface (90°) and viewed parallel with the pial surface (0°). (D) Class 8. Area 24b. CRet immunolabeling in superficial layers 1–2. A CRet+ SPF cell is indicated (arrow). Note the paucity of other CRet+ neurons in layer 1 compared with the increased density of labeled neuronal somata in layer 2 (asterisk). The slanted white double headed arrow indicates the plane of the pial surface which lies oblique to the axis of viewing. Capillary, c. Scale bar: 200 μm. (E) Enlarged image of the SPF cell in (H). One pole of the ellipsoid soma (arrow) gives rise to a thick branching dendrite that recurves and courses tangentially directly beneath the pial surface. Thorn-like processes arising proximally from the main dendrite are indicated (small white arrows). Region outlined is enlarged in inset which shows a CRet+ puncta abutting a dendritic thorn (d, dendrite). A dark vacuolated cellular profile is shown enlarged in (E′) Capillary, c. Scale bar: 100 μm. Inset shows (F) Reconstruction of the neuron in (E) (arrow). Fine thorn-like processes (small arrows) emanate from the thick main process (see inset). A small-caliber terminal process gives rise to several varicosities (one of which is encircled). Scale bar: 100 μm (G) Photomicrograph of the SPF soma — note lack of filaments arising from soma (c.f. Figures 2C,F). A thin axon-like processes (ax) emerges from one pole of the soma. Swelling along an immunopositive process (black circle). CRet+ punctae (presumed synaptic boutons) are present in the neighboring neuropil (white circle). Scale bar: 25 μm. (G′) A CRet+ axonal swelling (white arrow) closely opposed to a CRet+ distal dendritic process (d). Another CRet+ puncta is indicated (black arrow). (H) 3D-rotations of the SPF cell to show the distribution of the immunolabeled cellular processes when viewed in the perpendicular plane and in surface view. Note the fan-like spread of the labeled processes. Indicated are the visible CRet+ punctae (green dots) abutting the processes of the SPF cell. Scale bar: 100 μm. (I) Surface view of a group of three neighboring CRet+ neurons in upper layer 1 of area 46d. Categorized as a class 8 SPF cell, a superficial class 7 cell and the profile of a partly immunolabeled neuron. Clumps of lipofuscin (arrows) (Axon, ax). Scale bar: 100 μm.
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Figure 5: (A) Class 8. Area 46d. Reconstruction of a CRet+ SPF cell. Note the radiate fan-like distribution of the dendritic processes. Numerous thorn-like protrusions emanate from the main processes. Swellings along the axonal process (ax) are indicated. Scale bar: 50 μm. Inset (A′): Enlarged image of the region in (A) illustrating several long, fine thorn-like protrusions arising from a thick secondary dendrite. (B) Photomicrographic montage of the dendritic arbor indicated by the polygonal region in (A). (C) 3D rotations showing the distribution of the cellular processes viewed in the plane perpendicular to the pial surface (90°) and viewed parallel with the pial surface (0°). (D) Class 8. Area 24b. CRet immunolabeling in superficial layers 1–2. A CRet+ SPF cell is indicated (arrow). Note the paucity of other CRet+ neurons in layer 1 compared with the increased density of labeled neuronal somata in layer 2 (asterisk). The slanted white double headed arrow indicates the plane of the pial surface which lies oblique to the axis of viewing. Capillary, c. Scale bar: 200 μm. (E) Enlarged image of the SPF cell in (H). One pole of the ellipsoid soma (arrow) gives rise to a thick branching dendrite that recurves and courses tangentially directly beneath the pial surface. Thorn-like processes arising proximally from the main dendrite are indicated (small white arrows). Region outlined is enlarged in inset which shows a CRet+ puncta abutting a dendritic thorn (d, dendrite). A dark vacuolated cellular profile is shown enlarged in (E′) Capillary, c. Scale bar: 100 μm. Inset shows (F) Reconstruction of the neuron in (E) (arrow). Fine thorn-like processes (small arrows) emanate from the thick main process (see inset). A small-caliber terminal process gives rise to several varicosities (one of which is encircled). Scale bar: 100 μm (G) Photomicrograph of the SPF soma — note lack of filaments arising from soma (c.f. Figures 2C,F). A thin axon-like processes (ax) emerges from one pole of the soma. Swelling along an immunopositive process (black circle). CRet+ punctae (presumed synaptic boutons) are present in the neighboring neuropil (white circle). Scale bar: 25 μm. (G′) A CRet+ axonal swelling (white arrow) closely opposed to a CRet+ distal dendritic process (d). Another CRet+ puncta is indicated (black arrow). (H) 3D-rotations of the SPF cell to show the distribution of the immunolabeled cellular processes when viewed in the perpendicular plane and in surface view. Note the fan-like spread of the labeled processes. Indicated are the visible CRet+ punctae (green dots) abutting the processes of the SPF cell. Scale bar: 100 μm. (I) Surface view of a group of three neighboring CRet+ neurons in upper layer 1 of area 46d. Categorized as a class 8 SPF cell, a superficial class 7 cell and the profile of a partly immunolabeled neuron. Clumps of lipofuscin (arrows) (Axon, ax). Scale bar: 100 μm.

Mentions: Simple unipolar neurons aligned horizontally in layer 1. Most common in the lower two-thirds of layer 1 (c.50–150 μm below pia; Figure 1C). These cells possessed a single small/medium-caliber dendrite and a fine axonal process (Figures 3D, 4G, 5I). The somata of these neurons were smooth and dendrites could sometimes issue appendages (Figure 5I). (The unidendritic nature of these cells was not due to sectioning artifacts); and,


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

Gabbott PL - Front Neuroanat (2016)

(A) Class 8. Area 46d. Reconstruction of a CRet+ SPF cell. Note the radiate fan-like distribution of the dendritic processes. Numerous thorn-like protrusions emanate from the main processes. Swellings along the axonal process (ax) are indicated. Scale bar: 50 μm. Inset (A′): Enlarged image of the region in (A) illustrating several long, fine thorn-like protrusions arising from a thick secondary dendrite. (B) Photomicrographic montage of the dendritic arbor indicated by the polygonal region in (A). (C) 3D rotations showing the distribution of the cellular processes viewed in the plane perpendicular to the pial surface (90°) and viewed parallel with the pial surface (0°). (D) Class 8. Area 24b. CRet immunolabeling in superficial layers 1–2. A CRet+ SPF cell is indicated (arrow). Note the paucity of other CRet+ neurons in layer 1 compared with the increased density of labeled neuronal somata in layer 2 (asterisk). The slanted white double headed arrow indicates the plane of the pial surface which lies oblique to the axis of viewing. Capillary, c. Scale bar: 200 μm. (E) Enlarged image of the SPF cell in (H). One pole of the ellipsoid soma (arrow) gives rise to a thick branching dendrite that recurves and courses tangentially directly beneath the pial surface. Thorn-like processes arising proximally from the main dendrite are indicated (small white arrows). Region outlined is enlarged in inset which shows a CRet+ puncta abutting a dendritic thorn (d, dendrite). A dark vacuolated cellular profile is shown enlarged in (E′) Capillary, c. Scale bar: 100 μm. Inset shows (F) Reconstruction of the neuron in (E) (arrow). Fine thorn-like processes (small arrows) emanate from the thick main process (see inset). A small-caliber terminal process gives rise to several varicosities (one of which is encircled). Scale bar: 100 μm (G) Photomicrograph of the SPF soma — note lack of filaments arising from soma (c.f. Figures 2C,F). A thin axon-like processes (ax) emerges from one pole of the soma. Swelling along an immunopositive process (black circle). CRet+ punctae (presumed synaptic boutons) are present in the neighboring neuropil (white circle). Scale bar: 25 μm. (G′) A CRet+ axonal swelling (white arrow) closely opposed to a CRet+ distal dendritic process (d). Another CRet+ puncta is indicated (black arrow). (H) 3D-rotations of the SPF cell to show the distribution of the immunolabeled cellular processes when viewed in the perpendicular plane and in surface view. Note the fan-like spread of the labeled processes. Indicated are the visible CRet+ punctae (green dots) abutting the processes of the SPF cell. Scale bar: 100 μm. (I) Surface view of a group of three neighboring CRet+ neurons in upper layer 1 of area 46d. Categorized as a class 8 SPF cell, a superficial class 7 cell and the profile of a partly immunolabeled neuron. Clumps of lipofuscin (arrows) (Axon, ax). Scale bar: 100 μm.
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Figure 5: (A) Class 8. Area 46d. Reconstruction of a CRet+ SPF cell. Note the radiate fan-like distribution of the dendritic processes. Numerous thorn-like protrusions emanate from the main processes. Swellings along the axonal process (ax) are indicated. Scale bar: 50 μm. Inset (A′): Enlarged image of the region in (A) illustrating several long, fine thorn-like protrusions arising from a thick secondary dendrite. (B) Photomicrographic montage of the dendritic arbor indicated by the polygonal region in (A). (C) 3D rotations showing the distribution of the cellular processes viewed in the plane perpendicular to the pial surface (90°) and viewed parallel with the pial surface (0°). (D) Class 8. Area 24b. CRet immunolabeling in superficial layers 1–2. A CRet+ SPF cell is indicated (arrow). Note the paucity of other CRet+ neurons in layer 1 compared with the increased density of labeled neuronal somata in layer 2 (asterisk). The slanted white double headed arrow indicates the plane of the pial surface which lies oblique to the axis of viewing. Capillary, c. Scale bar: 200 μm. (E) Enlarged image of the SPF cell in (H). One pole of the ellipsoid soma (arrow) gives rise to a thick branching dendrite that recurves and courses tangentially directly beneath the pial surface. Thorn-like processes arising proximally from the main dendrite are indicated (small white arrows). Region outlined is enlarged in inset which shows a CRet+ puncta abutting a dendritic thorn (d, dendrite). A dark vacuolated cellular profile is shown enlarged in (E′) Capillary, c. Scale bar: 100 μm. Inset shows (F) Reconstruction of the neuron in (E) (arrow). Fine thorn-like processes (small arrows) emanate from the thick main process (see inset). A small-caliber terminal process gives rise to several varicosities (one of which is encircled). Scale bar: 100 μm (G) Photomicrograph of the SPF soma — note lack of filaments arising from soma (c.f. Figures 2C,F). A thin axon-like processes (ax) emerges from one pole of the soma. Swelling along an immunopositive process (black circle). CRet+ punctae (presumed synaptic boutons) are present in the neighboring neuropil (white circle). Scale bar: 25 μm. (G′) A CRet+ axonal swelling (white arrow) closely opposed to a CRet+ distal dendritic process (d). Another CRet+ puncta is indicated (black arrow). (H) 3D-rotations of the SPF cell to show the distribution of the immunolabeled cellular processes when viewed in the perpendicular plane and in surface view. Note the fan-like spread of the labeled processes. Indicated are the visible CRet+ punctae (green dots) abutting the processes of the SPF cell. Scale bar: 100 μm. (I) Surface view of a group of three neighboring CRet+ neurons in upper layer 1 of area 46d. Categorized as a class 8 SPF cell, a superficial class 7 cell and the profile of a partly immunolabeled neuron. Clumps of lipofuscin (arrows) (Axon, ax). Scale bar: 100 μm.
Mentions: Simple unipolar neurons aligned horizontally in layer 1. Most common in the lower two-thirds of layer 1 (c.50–150 μm below pia; Figure 1C). These cells possessed a single small/medium-caliber dendrite and a fine axonal process (Figures 3D, 4G, 5I). The somata of these neurons were smooth and dendrites could sometimes issue appendages (Figure 5I). (The unidendritic nature of these cells was not due to sectioning artifacts); and,

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