Abstract
Human cortical and subcortical areas integrate emotion, memory, and cognition when interpreting various environmental stimuli for the elaboration of complex, evolved social behaviors. Pyramidal neurons occur in developed phylogenetic areas advancing along with the allocortex to represent 70–85% of the neocortical gray matter. Here, we illustrate and discuss morphological features of heterogeneous spiny pyramidal neurons emerging from specific amygdaloid nuclei, in CA3 and CA1 hippocampal regions, and in neocortical layers II/III and V of the anterolateral temporal lobe in humans. Three-dimensional images of Golgi-impregnated neurons were obtained using an algorithm for the visualization of the cell body, dendritic length, branching pattern, and pleomorphic dendritic spines, which are specialized plastic postsynaptic units for most excitatory inputs. We demonstrate the emergence and development of human pyramidal neurons in the cortical and basomedial (but not the medial, MeA) nuclei of the amygdala with cells showing a triangular cell body shape, basal branched dendrites, and a short apical shaft with proximal ramifications as “pyramidal-like” neurons. Basomedial neurons also have a long and distally ramified apical dendrite not oriented to the pial surface. These neurons are at the beginning of the allocortex and the limbic lobe. “Pyramidal-like” to “classic” pyramidal neurons with laminar organization advance from the CA3 to the CA1 hippocampal regions. These cells have basal and apical dendrites with specific receptive synaptic domains and several spines. Neocortical pyramidal neurons in layers II/III and V display heterogeneous dendritic branching patterns adapted to the space available and the afferent inputs of each brain area. Dendritic spines vary in their distribution, density, shapes, and sizes (classified as stubby/wide, thin, mushroom-like, ramified, transitional forms, “atypical” or complex forms, such as thorny excrescences in the MeA and CA3 hippocampal region). Spines were found isolated or intermingled, with evident particularities (e.g., an extraordinary density in long, deep CA1 pyramidal neurons), and some showing a spinule. We describe spiny pyramidal neurons considerably improving the connectional and processing complexity of the brain circuits. On the other hand, these cells have some vulnerabilities, as found in neurodegenerative Alzheimer’s disease and in temporal lobe epilepsy.
Highlights
Ramón y Cajal (1894b) described cortical pyramidal neurons as “progressively larger and more complex in ascending the animal scale. . . to assume that at least part of its increased functional role is a result of increased morphological complexity
The presence of different spines in human pyramidal neurons “aligns well with emerging theoretical models of synaptic learning that demonstrate that synapses exhibiting a gradation of states, each bridged by distinct metaplastic transitions, bestow neural networks with enhanced information storage capacity” (Lee et al, 2012; Dall’Oglio et al, 2015 and references therein). These morphological features of human pyramidal neurons can reflect a more complex subcortical to cortical synaptic processing of sensory, emotional, and cognitive information adapted for species-specific social behaviors (Dall’Oglio et al, 2013, 2015)
Neurodegeneration advancing in the limbic lobe harms the dendrites and spines of pyramidal neurons in the subiculum, the CA1 hippocampal region, and the entorhinal cortex in the mesial temporal lobe, further progressing to involve the nucleus basalis of Meynert and associative areas in the frontal, parietal, and temporal lobes (Hyman et al, 1984; Saper and Chelimsky, 1984; Braak and Braak, 1991; Ishunina and Swaab, 2001; Thompson et al, 2001; Peçanha and Neri, 2007; Serrano-Pozo et al, 2011; Liu et al, 2015)
Summary
Ramón y Cajal (1894b) described cortical pyramidal neurons (or “psychic cells”) as “progressively larger and more complex in ascending the animal scale. . . to assume that at least part of its increased functional role is a result of increased morphological complexity. We would like to highlight and instigate further 3D morphological studies on the emergence and development of human pyramidal neurons, including the features of dendritic spine number and shapes, as essential steps for understanding the integrative capacities of these neurons in distinct, functionally specialized brain areas (Spruston, 2008; Luebke, 2017; Soltesz and Losonczy, 2018; Cembrowski and Spruston, 2019; BenavidesPiccione et al, 2020).
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