Comparative ultrastructural features of excitatory synapses in the visual and frontal cortices of the adult mouse and monkey

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Early neuroanatomists established that the mammalian cerebral cortex can be differentiated into many structurally and functionally distinct cytoarchitectonic areas (Brodmann, 1909). With the advent of high‐resolution neuroimaging and neuroanatomical methods, our understanding of cortical areal heterogeneity has expanded dramatically over the past several decades. Highly detailed information about the quantitative cytoarchitecture of (i.e., cellular constituents) and connectivity between distinct cortical areas has been obtained from post‐mortem histological analyses in the nonhuman primate animal model (Felleman & Van Essen, 1991), review: (Barbas, 2015; Pandya, Seltzer, Petrides, & Cipolloni, 2015) as well as in the human brain (review: Petrides, Tomaiuolo, Yeterian, & Pandya, 2012; Zilles, Palomero,‐Gallagher, & Schleicher, 2004). Recent studies have reliably recapitulated this detailed cortical map in the human brain using noninvasive in vivo imaging methods and novel software algorithms (Amunts & Zilles, 2015; Glasser et al., 2016). These macro‐level cortical maps in humans and monkeys reflect functionally distinct cortical areas, but the detailed local circuit, cellular and subcellular underpinnings of cortical areal specialization remains to be fully elucidated. An intrinsic relationship between cortical cytoarchitecture and inter‐areal connectivity is one fundamental determinant of cortical specialization (Hilgetag, Burns, O'Neill, Scannell, & Young, 2000; Hilgetag, Medalla, Beul, & Barbas, 2016), review (Barbas, 2015; Barbas & Garcia‐Cabezas, 2016; Rakic, 2002). The patterns of connections among distinct cortical areas are related to graded differences in cortical cytoarchitecture, such that areas with similar cytoarchitecture have the strongest inter‐connections, and thus are part of the same functional network (Hilgetag et al., 2016). In line with this idea is the finding of graded differences in dendritic architecture across distinct cortical visual areas coinciding with a gradient of cortical lamination and complexity of visual information processing in the nonhuman primate (Elston, 2002).
That the dendritic architecture of pyramidal neurons varies depending on cortical area has been known since the time of Cajal (Conel, 1941; Ramón y Cajal, 1894). Recent studies have used high resolution anatomical and electrophysiological methods to further elaborate on the structural and functional properties of individual pyramidal neurons across distinct cortical areas (Amatrudo et al., 2012; DeFelipe, Alonso‐Nanclares, & Arellano, 2002; Elston, 2000; Medalla & Luebke, 2015). In the rhesus monkey, layer 3 (L3) pyramidal neurons in the lateral prefrontal cortex (LPFC) and V1 are strikingly different in terms of both their morphological and electrophysiological properties. Structurally, the dendritic arbors of L3 pyramidal neurons in LPFC are 3–4x larger, more complex and contain ∼16x higher number of dendritic spines than those of V1 (Amatrudo et al., 2012; Elston, 2000; Gilman, Medalla, & Luebke, 2016). Functionally, LPFC neurons are less excitable and have significantly more frequent excitatory synaptic events with larger amplitude and longer decay time, compared to V1 neurons (Medalla & Luebke, 2015). To determine whether the differences in synaptic properties could be explained by differences in the excitatory synapses themselves, Medalla and Luebke (2015) assessed the ultrastructural properties of excitatory synapses in the layers 2–3 (L2–3) neuropil. Interestingly, both presynaptic boutons and postsynaptic densities of axospinous synapses were significantly larger in LPFC compared to V1. Further, there was a higher proportion of large perforated synapses in LPFC than in V1. These findings of much larger synapses in LPFC (together with the much higher density of spines) is consistent with the idea that significantly larger and more frequent synaptic currents are likely due to more numerous, larger and more powerful synapses in LPFC compared to V1.
By contrast to the highly distinctive characteristics of L3 pyramidal neurons in the monkey visual versus lateral prefrontal cortices, neurons in analogous areas of the mouse are remarkably similar both functionally and structurally (DeFelipe, 2011; DeFelipe et al.
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