Neuronal types of the human cortical amygdaloid nucleus

Abstract

The human cortical amygdaloid nucleus (CoA) receives exteroceptive sensory stimuli, modulates the functions coded by the intrinsic amygdaloid circuit, and constitutes the beginning of the limbic lobe continuum with direct and indirect connections toward subcortical, allocortical, and higher order neocortical areas. To provide basic data on the human CoA, we characterized and classified the neurons using the thionin and the "single-section" Golgi method adapted for postmortem brain tissue and light microscopy. We found 10 different types of neurons named according to the morphological features of the cell body, dendritic branches, and spine distribution. Most cells are multipolar spiny neurons with two or more primary dendrites, including pyramidal-like ones. Three-dimensional reconstructions evidenced the types and diversity of the dendritic spines in each neuron. The unlike density of spines along dendritic branches, from proximal to distal ones, indicate that the synaptic processing and plasticity can be different in each CoA neuron. Our study provides novel data on the neuronal composition of the human CoA indicating that the variety of cells in this region can have phylogenetic, ontogenetic, morphological, and likely functional implications for the integrated human brain function. This can reflect both a more complex subcortical synaptic processing of sensory and emotional information and an adaptation for species-specific social behavior display.

Dendritic and Spine Heterogeneity of von Economo Neurons in the Human Cingulate Cortex

“…The "single-section" Golgi method was adapted to provide reliable results for the neuronal cell body and the dendritic and spines features in long-term fixed human brains (Dall'Oglio et al, 2010). The consistency of the present procedure is the same that served for previous characterization of neurons and dendritic spines in subcortical and cortical human brain areas (e.g., the medial and cortical amygdaloid nuclei and the CA3 hippocampal area; Dall'Oglio et al, 2013, 2015Reberger et al, 2018;Vásquez et al, 2018).…”

“…Following Reberger et al (2018), spines were 3D reconstructed using an algorithm performed in the MATLAB software (R2105b, The MathWorks, United States). That is, after processing the gray-scale slices independently or using median 3D filters in smaller sub-volumes, images were processed using the following steps: (a) outlier removal; (b) edge enhancement using a variant of the "unsharp masking method" and image-filtering approach based on domain transforms ("edge-aware"); (c) binarization using an adaptive thresholding approach; (d) false-positive pruning; (e) 2D flood-fill operation with each slice of the binary volume; (f) tricubic interpolation to smooth transitions between adjacent slices; and (g) visualization of the final volume of the sampled images containing the selected dendritic shafts and their spines (Vásquez et al, 2018) using the "Fiji" ImageJ software (Schindelin et al, 2012) with the "Volume Viewer" plug-in 1 . Images had final adjustments of brightness and contrast made in Photoshop CS3 without altering spine counting or classification.…”

“…The pattern of dendritic branching and the presence of pleomorphic spines provide relevant morphological criteria for the classification of neurons ( Ramón y Cajal, 1909-1911 ; Ramón-Moliner, 1962 ; Braak, 1980 ; Gabbott et al, 1997 ; Vásquez et al, 2018 ). This is an important issue because the dendritic architecture relates to the biophysical properties of the neuron, the membrane available for contacts and integration of excitatory and inhibitory inputs, and the establishment of spatiotemporal domains for the synaptic computations ( Spruston, 2008 ; Spruston et al, 2013 ; Rollenhagen and Lübke, 2016 ).…”

The Subcortical-Allocortical- Neocortical continuum for the Emergence and Morphological Heterogeneity of Pyramidal Neurons in the Human Brain

“…Pyramidal neurons have been studied using complementary techniques, from the Nissl (or thionine) staining and the Golgi silver impregnation procedure to different approaches for intracellular microinjection of fluorescent dyes, serial sections for ultrastructural connectional and neurochemical profiles, in vitro and in vivo electrophysiological recordings, computational and in silico models (Ramón y Cajal, 1909-1911Lorente de Nó, 1934;Szentágothai, 1978;Mountcastle, 1979;Braak, 1980;Peters and Jones, 1984;Sims and Williams, 1990;Peters et al, 1991;McCormick et al, 1993;Segev et al, 1995;Somogyi et al, 1998;Valverde et al, 2002;Andersen et al, 2007;Spruston, 2008;Larriva-Sahd, 2010;Ramaswamy and Markram, 2015;Eyal et al, 2018;Soltesz and Losonczy, 2018;Cembrowski and Spruston, 2019;Oruro et al, 2019;Benavides-Piccione et al, 2020). For example, the Golgi method adapted for formalin-fixed human brain and light microscopy provides images of pyramidal dendrites and spine shapes from different cortical and subcortical regions (Dall'Oglio et al, 2010;Reberger et al, 2018;Vásquez et al, 2018;Correa-Júnior et al, 2020). This can eventually add fundamental data to identify the brain cellular components and their connectivity toward physiology and behavior, as well as for modeling and theory approaches on neural structure and integrated functions of human brain areas (see a current discussion in Zeng, 2020).…”

“…Here, we illustrate and discuss the morphological findings of three-dimensional (3D) reconstruction of heterogeneous pyramidal neurons with pleomorphic dendritic spines in the anatomical and functional subcortical-allocortical-neocortical continuum in the human brain (from adult males; samples and methodological procedures are described in Dall'Oglio et al, 2010, 2013Reberger et al, 2018;Vásquez et al, 2018). Our aim is not to exhaustively elaborate the data available in the literature.…”