The human medial amygdala: structure, diversity, and complexity of dendritic spines

Abstract

The medial nucleus of the amygdala (Me) is a component of the neural circuit for the interpretation of multimodal sensory stimuli and the elaboration of emotions and social behaviors in primates. We studied the presence, distribution, diverse shape, and connectivity of dendritic spines in the human Me of adult postmortem men. Data were obtained from the five types of multipolar neurons found in the Me using an adapted Golgi method and light microscopy, the carbocyanine DiI fluorescent dye and confocal microscopy, and transmission electron microscopy. Three-dimensional reconstruction of spines showed a continuum of shapes and sizes, with the spines either lying isolated or forming clusters. These dendritic spines were classified as stubby/wide, thin, mushroom-like, ramified or with an atypical morphology including intermediate shapes, double spines, and thorny excrescences. Pleomorphic spines were found from proximal to distal dendritic branches suggesting potential differences for synaptic processing, strength, and plasticity in the Me neurons. Furthermore, the human Me has large and thin spines with a gemmule appearance, spinules, and filopodium. The ultrastructural data showed dendritic spines forming monosynaptic or multisynaptic contacts at the spine head and neck, and with asymmetric or symmetric characteristics. Additional findings included en passant, reciprocal, and serial synapses in the Me. Complex long-necked thin spines were observed in this subcortical area. These new data reveal the diversity of the dendritic spines in the human Me likely involved with the integration and processing of local synaptic inputs and with functional implications in physiological and various neuropathological conditions.

Remodeling of the number and structure of dendritic spines in the medial amygdala: From prepubertal sexual dimorphism to puberty and effect of sexual experience in male rats

“…This is consistent with the possibility that thin spines are related to “learning” processes, showing a labile aspect prone to changes in the synaptic processing, whereas mushroom spines are related to “memory” elaboration, showing a higher stability, great postsynaptic density with glutamatergic receptors and strong synaptic responses (Bourne & Harris, ; but see Segal, ). Spines classified as atypical might represent transient forms at varying stages of development or retraction and can have, as the ramified ones, functional microdomains in the same spine (Chen & Sabatini, ; Dall'Oglio et al., and references therein). These data indicate that the synaptic input and strength can be fine regulated at small segments of the MePD dendrites.…”

“…Length was defined as the distance from the base at the dendritic shaft to the top of the spine or its neck; diameter was defined as the maximum distance perpendicular to the long axis of the spine and was measured for the neck or and the head of the spine (Ryu et al., ). Then, from the 3D reconstructed images, spines were classified and counted according to morphological criteria based on spine length (SL), neck length (NL), neck diameter (ND), head diameter (HD) and the number of protrusions from a single stalk (Dall'Oglio, Dutra, Moreira, & Rasia‐Filho, ; Zancan et al., and references therein). Based on their shapes, spines were classified into the following: (a) thin (when SL > HD and HD > ND), (b) mushroom‐like (HD ≫ ND), (c) stubby/wide (HD > SL), (d) ramified (with a single stalk that branches in two heads) or (e) atypical (when showing a transitional aspect between classes or an unusual shape not classified in the other classes (based on Arellano, Benavides‐Piccione, DeFelipe, & Yuste, ; Brusco et al., , ; Dall'Oglio et al., ; Harris et al., ; Stewart, Popov, Kraev, Medvedev, & Davies, ; Zancan et al., and references therein).…”

“…Proximal dendritic spines are at a strategical site to modulate the cell body and axonal voltage and the output activity of the MePD. The structure-function coupling of spines and the activity-driven changes related to synaptic demand, stability and plasticity can be set at the level of each single spine (Arellano et al, 2007;Becker, Dall′Oglio, Rigatto, Giovenardi, & Rasia-Filho, 2015;Chen, Leischner, Rochefort, Nelken, & Konnerth, 2011;Dall'Oglio et al, 2015;Dalpian, Brusco, Calcagnotto, Moreira, & Rasia-Filho, 2015;Hansberg-Pastor, González-Arenas, Piña-Medina, & Camacho-Arroyo, 2015;Rochefort & Konnerth, 2012;Stewart et al, 2014). Interestingly, prepubertal males have more stubby/wide spines than prepubertal females.…”

Might the olfactory bulb be an origin of olfactory auras in focal epilepsy?

“…The amygdala, associated with emotions, fear, anxiety, and other psychological phenomena is another region of great synaptic plasticity throughout life and may be influenced by hormones, DNA methylation by alcohol, hypoxia, neurotoxins, and other exogenous factors (Arruda‐Carvalho and Clem, ; Alisch et al ., ; Kuhn et al ., ; Li and Rainnie, ; Marin, ; Boitard et al ., ; Dall’Oglio et al ., ; Galvin et al ., ; Kim et al ., ; Stolyarova and Izquierdo, ).…”

“…The hippocampus must be plastic to enable the formation of new memory engrams and to facilitate deletion of others of no permanent importance (Moser et al, 1994;Engert and Bornhoeffer, 1999;Sanders et al, 2012;Yang et al, 2014;Attardo et al, 2015;Ryan et al, 2015), whereas stability of hippocampal dendritic spines is associated with the conservation of long-term memories (Yang et al, 2009). The amygdala, associated with emotions, fear, anxiety, and other psychological phenomena is another region of great synaptic plasticity throughout life and may be influenced by hormones, DNA methylation by alcohol, hypoxia, neurotoxins, and other exogenous factors (Arruda-Carvalho and Clem, 2014;Alisch et al, 2014;Kuhn et al, 2014;Li and Rainnie, 2014;Marin, 2014;Boitard et al, 2015;Dall'Oglio et al, 2015;Galvin et al, 2015;Kim et al, 2015;Stolyarova and Izquierdo, 2015). The olfactory bulb is another of the most synaptically plastic structures of the brain (Pomeroy et al, 1990;Mouly and Sullivan, 2010), yet its epileptogenic potential is unknown because this aspect has been little investigated or even considered in animals or humans.…”