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.
Highlights
Specific CRet+ immunolabeling was present throughout layers 1–6 of the prefrontal cortex (PFC) areas studied and in the underlying white matter
The peak distributions of CRet+ neurons in primate PFC was in layer 2 with a small fraction (
Several classes of CRet+ neurons were immunolabeled throughout the depth of layer 1 and were present across all PFC areas (Figures 2, 3A–F, 4D,G,H)
Summary
The early Golgi-impregnation studies of Ramón y Cajal (1890, 1891, 1899a,b,c), Retzius (1893, 1894), and others (Kölliker, 1894; Campbell, 1905; Ranke, 1910; Oppermann, 1929) identified the wide morphological variety of neurons in layer 1 (molecular/plexiform layer) present during the preand postnatal development of the cerebral cortex in several mammalian species, including humans — with the most studied family of neurons being the horizontal cells described by Ramón y Cajal and by Retzius (Fairén et al, 2002; Gil et al, 2014; Martinez-Cerdeno and Noctor, 2014; Marín-Padilla, 2015). Subsequent studies have refined and extended morphological descriptions of the “special” Cajal’sche Zellen (Retzius, 1894) and the Retzius’sche Zellen (Kölliker, 18941) and other neuron phenotypes in layer 1 (for example: Marín-Padilla, 1984, 1998, 2015; Huntley and Jones, 1990; Frotscher, 1998; Meyer et al, 1999; Fairén et al, 2002; Rakic and Zecevic, 2003; Soriano and Del Río, 2005; Kirischuk et al, 2014; Martinez-Cerdeno and Noctor, 2014; Lee et al, 2015). The secretion of reelin by Cajal-Retzius cells (and other neurons) plays an important role in choreographing the developmental blueprint of radial cell migration, laminar and columnar differentiation, as well as the formation and plasticity of synaptic circuitry during cortical maturation (Frotscher, 1998, 2010; Nishikawa et al, 2002; Fatemi, 2008; Meyer, 2010; GonzálezGómez and Meyer, 2014; Lee et al, 2014; Ramos-Moreno and Clascá, 2014; Chai et al, 2015; Varga et al, 2015)
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