Marked differences in the number and type of synapses innervating the somata and primary dendrites of midbrain dopaminergic neurons, striatal cholinergic interneurons, and striatal spiny projection neurons in the rat

• Published in: Journal of comparative neurology (1911) 2016-04, Vol.524 (5), p.1062-1080
• Main Authors: Sizemore, Rachel J., Zhang, Rong, Lin, Naili, Goddard, Liping, Wastney, Timothy, Parr-Brownlie, Louise C., Reynolds, John N.J., Oorschot, Dorothy E.
• Format: Article
• Language: English
• Subjects: Animals; Cholinergic Neurons - ultrastructure; Corpus Striatum - ultrastructure; Dendrites - ultrastructure; Dopaminergic Neurons - ultrastructure; dorsal striatum; Interneurons - ultrastructure; Male; Mesencephalon - ultrastructure; Rats; Rats, Sprague-Dawley; Rats, Wistar; RRID:AB_39024; RRID:AB_94647; Species Specificity; substantia nigra pars compacta; Synapses - ultrastructure; synaptic innervation; transmission electron microscopy; ventral tegmental area
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23891

ABSTRACT Elucidating the link between cellular activity and goal‐directed behavior requires a fuller understanding of the mechanisms underlying burst firing in midbrain dopaminergic neurons and those that suppress activity during aversive or non‐rewarding events. We have characterized the afferent synaptic connections onto these neurons in the rat substantia nigra pars compacta (SNpc) and ventral tegmental area (VTA), and compared these findings with cholinergic interneurons and spiny projection neurons in the striatum. We found that the average absolute number of synapses was three to three and one‐half times greater onto the somata of dorsal striatal spiny projection neurons than onto the somata of dopaminergic neurons in the SNpc or dorsal striatal cholinergic interneurons. A similar comparison between populations of dopamine neurons revealed a two times greater number of somatic synapses on VTA dopaminergic neurons than SNpc dopaminergic neurons. The percentage of symmetrical, presumably inhibitory, synaptic inputs on somata was significantly higher on spiny projection neurons and cholinergic interneurons compared with SNpc dopaminergic neurons. Synaptic data on the primary dendrites yielded similar significant differences for the percentage of symmetrical synapses for VTA dopaminergic vs. striatal neurons. No differences in the absolute number or type of somatic synapses were evident for dopaminergic neurons in the SNpc of Wistar vs. Sprague‐Dawley rat strains. These data from identified neurons are pivotal for interpreting their electrophysiological responses to afferent activity and for generating realistic computer models of neuronal networks of striatal and midbrain dopaminergic function. J. Comp. Neurol. 524:1062–1080, 2016. © 2015 Wiley Periodicals, Inc. VTA dopaminergic neurons have two times more somatic synapses, and no differences in the type of synapses, compared with nigral dopaminergic neurons in the Sprague‐Dawley rat. The number and type of somatic synapses does not differ between nigral dopaminergic neurons of the Sprague‐Dawley and Wistar rat strains. Dorsal spiny projection neurons have 3–3.5 times more somatic synapses compared with nigral dopaminergic neurons and striatal cholinergic interneurons, and dorsal spiny projection neurons and cholinergic interneurons have a significantly higher percentage of symmetrical somatic synapses compared with nigral dopaminergic neurons, in the Wistar rat.