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

Nivaldo D Correa-Júnior,Josué Renner,Francisco Fuentealba-Villarroel,Alberto A Rasia-Filho,Arlete Hilbig

doi:10.3389/fnsyn.2020.00025

Abstract

The human cingulate cortex (CC), included in the paralimbic cortex, participates in emotion, visceral responses, attention, cognition, and social behaviors. The CC has spindle-shaped/fusiform cell body neurons in its layer V, the von Economo neurons (VENs). VENs have further developed in primates, and the characterization of human VENs can benefit from the detailed descriptions of the shape of dendrites and spines. Here, we advance this issue and studied VENs in the anterior and midcingulate cortex from four neurologically normal adult subjects. We used the thionin technique and the adapted “single-section” Golgi method for light microscopy. Three-dimensional (3D) reconstructions were carried out for the visualization of Golgi-impregnated VENs’ cell body, ascending and descending dendrites, and collateral branches. We also looked for the presence, density, and shape of spines from proximal to distal dendrites. These neurons have a similar aspect for the soma, but features of spiny dendrites evidenced a morphological heterogeneity of CC VENs. Only for the description of this continuum of shapes, we labeled the most common feature as VEN 1, which has main dendritic shafts but few branches and sparse spines. VEN 2 shows an intermediate aspect, whereas VEN 3 displays the most profuse dendritic ramification and more spines with varied shapes from proximal to distal branches. Morphometric data exemplify the dendritic features of these cells. The heterogeneity of the dendritic architecture and spines suggests additional functional implications for the synaptic and information processing in VENs in integrated networks of normal and, possibly, neurological/psychiatric conditions involving the human CC.

Highlights

The cingulate cortex (CC) is part of the “proisocortex” in the paralimbic cortex, which is phylogenetically older than the neocortex along with the evolution of the mammalian brain (Braak, 1979; Kolb and Whishaw, 2015; Pandya et al, 2015)
The human CC begins adjacent to the genu of the corpus callosum corresponding to the cortical area 24 of Brodmann and the agranular
The cell body shape of these cells is similar to those reported by other authors (e.g., Nimchinsky et al, 1995; Allman et al, 2010)

Summary

Introduction

The cingulate cortex (CC) is part of the “proisocortex” in the paralimbic cortex, which is phylogenetically older than the neocortex along with the evolution of the mammalian brain (Braak, 1979; Kolb and Whishaw, 2015; Pandya et al, 2015). The CC integrates specialized networks for attentional processes/executive functions with sensory, high-order associative and limbic brain areas. In this regard, the human CC elaborates focused attention for problemsolving, goal-directed, and exploratory behaviors; long-term memory and cognitive processing; premotor planning with motivational features; social awareness and emotions as love, trust, empathy, deception, guilt, and fear; feeding and aggression; and sympathetic and parasympathetic responses to modulate heart rate and arterial pressure, respiratory, and gastrointestinal responses (Allman et al, 2001, 2010, 2011a; Watson, 2006; Watson et al, 2006; Xuan et al, 2016; Rangwala et al, 2017 and references therein)

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Conclusion