Ultrastructure of serotonin‐immunoreactive terminals in the core and shell of the rat nucleus accumbens: Cellular substrates for interactions with catecholamine afferents

Abstract

The nucleus accumbens is composed of a core region involved in motor functions and a shell region implicated in emotional and motivational processes. Both of these regions receive serotonin‐ and dopamine‐containing afferents. We examined whether the serotonin innervation or relation to catecholamine (mainly dopamine) axons in the nucleus accumbens shows common features or specializations corresponding to the noted functional differences in core and shell subregions. To address this question, we examined the ultrastructure of serotonin‐containing axons and their relation to catecholamine‐containing afferents in either the core or shell of the nucleus accumbens. Single coronal sections through the rat forebrain were processed for immunoperoxidase labeling of serotonin and immunogold silver labeling of tyrosine hydroxylase, the catecholamine‐synthesizing enzyme. Varicose processes showing peroxidase product for serotonin by light microscopy were confirmed to be axons and terminals by electron microscopy. In a quantitative analysis of serotonin‐immunoreactive terminals forming one or more contacts in single sections, some common features were observed. For the core (n = 120) and the shell (n = 82), 41% formed synaptic junctions with unlabeled dendrites, 75% were in apposition with unlabeled terminals, which often formed asymmetric junctions, and 20% were in apposition with axons or terminals containing tyrosine hydroxylase. Thus, in both the core and shell of the nucleus accumbens, serotonin terminals synapse on postsynaptic neurons and are likely to modulate or be modulated by presynaptic interactions with excitatory axons forming asymmetric junctions and by catecholaminergic afferents. Marked differences in the morphology of serotonin axons were also seen in the core versus shell of the nucleus accumbens. By light microscopy, serotonin‐immunoreactive axons were thicker and more varicose than those found in the core. Ultrastructural analysis confirmed that, in contrast to the core, serotonin‐immunoreactive axons and terminals in the shell were larger in cross‐sectional diameter size (0.7 μm vs. 0.3 μm). Additionally, serotonin axon terminals in the shell contained more numerous immunoreactive large dense core vesicles and more frequently formed symmetric as opposed to asymmetric contacts with dendrites. The larger size and more numerous dense core vesicles in serotonin‐immunoreactive terminals in the shell support the concept that serotonin or co‐existing neurotransmitter may be more tonically released in the shell versus core of the nucleus accumbens. © 1993 Wiley‐Liss, Inc.